Extremophiles
Draft Manuscript for Review
Microbial diversity and adaptation to high hydrostatic pressure in deep sea hydrothermal vents prokaryotes
Journal:For Extremophiles Peer Review Manuscript ID: EXT-15-Feb-0030.R1
Manuscript Type: Review
Date Submitted by the Author: n/a
Complete List of Authors: jebbar, mohamed; Université de Bretagne Occidentale, Institut Universitaire Europeen de la Mer Franzetti, Bruno; CNRS, Institut de Biologie Structurale Girard, Eric; CNRS, Institut de Biologie Structurale Oger, Phil; Laboratoire de Sciences de la Terre, Ecole Normale Superieure
(Extreme) thermophilic microorganisms and their enzymology, Anaerobes, Keyword: Archaea, Hyperthermophiles, Piezophiles, Enzymes, Deep sea vent microbiology, Ecology, phylogeny, physiology of thermophiles
Page 1 of 82 Extremophiles
1 2 3 1 Microbial diversity and adaptation to high hydrostatic pressure in deep sea 4 5 2 hydrothermal vents prokaryotes 6 7 3 Mohamed Jebbar 1,2, 3*, Bruno Franzetti 4,5,6, Eric Girard 4,5,6, and Philippe Oger 7 8 9 10 4 11 1 12 5 Université de Bretagne Occidentale, UMR 6197 Laboratoire de Microbiologie des 13 14 6 Environnements Extrêmes (LM2E), Institut Universitaire Européen de la Mer (IUEM), 15 16 7 rue Dumont d’Urville, 29 280 Plouzané, France 17 18 8 2 CNRS, UMRFor 6197 Laboratoire Peer de MicrobiologieReview des Environnements Extrêmes 19 20 21 9 (LM2E), Institut Universitaire Européen de la Mer (IUEM), rue Dumont d’Urville, 29 22
23 10 280 Plouzané, France 24 25 11 3 Ifremer, UMR 6197 Laboratoire de Microbiologie des Environnements Extrêmes 26 27 12 (LM2E), Technopôle Brest Iroise, BP70, 29 280 Plouzané, France 28 29 4 30 13 Centre National de la Recherche Scientifique, IBS, F 38027 Grenoble, France 31 5 32 14 Université Grenoble Alpes, Institut de Biologie Structurale (IBS), F 38027 Grenoble, 33 34 15 France 35 36 16 6Commissariat à l'Energie Atomique et aux Energies Alternatives, Direction des 37 38 17 Sciences du Vivant, IBS, F 38027 Grenoble, France 39 40 7 41 18 CNRS, UMR 5276, Ecole Normale Supérieure de Lyon, Lyon, France 42 43 19 44 45 20 46 47 21 *Corresponding author: 48 22 Prof. Mohamed Jebbar 49 50 23 Institut Universitaire Européen de la Mer (IUEM) 51 24 Laboratoire de Microbiologie des Environnements Extrêmes (UMR 6197) 52 25 Technopole Brest Iroise 53 26 Rue Dumont d’Urville 54 27 29280 Plouzané 55 28 Phone : +33 298 498 817 56 29 Fax : +33 298 498 705 57 30 e mail : mohamed.jebbar@univ brest.fr 58 31 59 60 1 Extremophiles Page 2 of 82
1 2 3 1 Abstract 4 5 2 Prokaryotes inhabiting in the deep sea vent ecosystem will thus experience harsh conditions 6 7 3 of temperature, pH, salinity or high hydrostatic pressure (HHP) stress. Among the fifty two 8 9 10 4 piezophilic and piezotolerant prokaryotes isolated so far from different deep sea 11 12 5 environments, only fifteen (four Bacteria and eleven Archaea ) that are true 13 14 6 hyper/thermophiles and piezophiles have been isolated from deep sea hydrothermal vents, 15 16 7 these belong mainly to the Thermococcales order. Different strategies are used by 17 18 8 microorganisms toFor thrive in deepPeer sea hydrothermal Review vents in which "extreme" physico 19 20 21 9 chemical conditions prevail and where non adapted organisms cannot live, or even survive. 22 23 10 HHP is known to impact the structure of several cellular components and functions, such as 24 25 11 membrane fluidity, protein activity and structure. Physically the impact of pressure resembles 26 27 12 a lowering of temperature, since it reinforces the structure of certain molecules, such as 28 29 30 13 membrane lipids, and an increase in temperature, since it will also destabilize other structures, 31 32 14 such as proteins. However, universal molecular signatures of HHP adaptation are not yet 33 34 15 known and are still to be deciphered. 35 36 16 37 38 17 Key words : deep biosphere, diversity, high hydrostatic pressure, enzymatic function, 39 40 41 18 molecular adaptation 42 43 19 44 45 20 46 47 21 48 49 50 22 51 52 23 53 54 24 55 56 25 57 58 59 60 2 Page 3 of 82 Extremophiles
1 2 3 1 Introduction 4 5 2 Hydrostatic pressure increases with depth at an approximate rate of 10 MPa (~100 6 7 3 atmospheres/bars) per km in the water column and 30 MPa per km underground (Oger and 8 9 10 4 Jebbar 2010). The definition of the deep biosphere is conveniently and arbitrarily defined as 11 12 5 applying to water depths of 1000 m or more. Consequently, all environments above 10 MPa 13 14 6 qualify as high hydrostatic pressure (HHP) biotopes. HHP waters account for 88% of the 15 16 7 volume of the oceans, which have an average depth of 3800 m, and thus an average 17 18 8 hydrostatic pressureFor ca. 38 MPa, Peer but reach 110 ReviewMPa in the trenches. The average temperature 19 20 21 9 in the deep ocean is 2 3 degree, except for hydrothermal vents. In contrast, the average 22 1 23 10 geothermal gradient in the continental system is ca. 25°C km . The currently known 24 25 11 temperature limit for life, 122°C (Takai et al. 2008), would thus place the "deep" limit for the 26 27 12 putative continental biosphere at ca. 5 km below ground on average, under maximal pressures 28 29 30 13 of 150 MPa (Zeng et al. 2009; Oger and Jebbar 2010). 31 32 14 HHP affects chemical equilibria and reaction rates, depending on the reaction ( V) 33 34 15 and activation ( V≠) volumes involved. The behavior of all systems under HHP is governed 35 36 37 16 by Le Châtelier’s principle, which states that the application of pressure shifts equilibrium 38 39 17 towards the state that occupies the smallest volume. It accelerates a process whose transition 40 41 18 state has a smaller volume than that of the ground state. For example, if the volume of a 42 43 19 protein is smaller in its unfolded form, then this protein will be denatured by the application 44 45 20 of HHP. Several cellular processes such as RNA synthesis, membrane fluidity, motility, cell 46 47 48 21 division, nutrient uptake, membrane protein function, protein synthesis and replication are 49 50 22 also impaired by HHP. HHP greater than 200 MPa can kill most microorganisms and is used 51 52 23 as a means to preserve foodstuffs. 53 54 24 55 56 57 25 58 59 60 3 Extremophiles Page 4 of 82
1 2 3 1 The discovery of deep sea hydrothermal vent ecosystems is rather recent in the history 4 5 2 of biological sciences (Corliss, J. B. and Ballard 1977; Paull et al. 1984; Jannasch and Mottl 6 7 3 1985; Eder et al. 1999). The most significant microbial process taking place at these sites is 8 9 10 4 "bacterial chemosynthesis", which contrasts with the well known process of photosynthesis. 11 12 5 Both processes involve the biosynthesis of organic carbon compounds from CO 2, with the 13 14 6 source of energy being either chemical oxidations or light, respectively (Jannasch and Mottl 15 16 7 1985). Chemoautotrophic prokaryotes will assimilate CO 2 and is coupled in some prokaryotes 17 18 8 with chemolithotrophy,For which enablesPeer them to Reviewreduce some inorganic compounds as energy 19 20 21 9 sources. Due to the mixture between the hot reduced hydrothermal fluids enriched in 22 23 10 dissolved gas (H 2S, H 2, CH 4, CO/CO 2) and metals (Fe, Mn) and the cold oxidized sea water 24 25 11 containing sulfates and nitrates, a wide variety of electron donors and acceptors are available 26 27 12 to supply different microbial metabolisms. 28 29 30 13 Most of the Earth’s prokaryotes live in deep biosphere environments under HHP. 31 28 32 14 From global estimates of volume, the upper 200 m of the ocean contains a total of 3.6 10 33 34 15 prokaryotic cells of which 2.9 10 27 cells are autotrophs; whereas the ocean water below 200 m 35 36 16 contains 6.5 10 28 prokaryotic cells (Whitman et al. 1998). A recent study has estimated the 37 38 17 total cell abundance in subseafloor sediment at 2.9 10 29 , which is 92% lower than the previous 39 40 29 41 18 standard estimate (35.5 ×10 ) (Whitman et al. 1998; Kallmeyer et al. 2012). Thus, even 42 43 19 though the maximal productivity of the high pressure continental or marine biosphere is 44 45 20 orders of magnitude lower than that of surface biotopes due to their extremely large volume, 46 47 21 these high pressure biotopes contribute significantly to the production and recycling of 48 49 50 22 organic carbon. 51 52 23 In less than 30 years, microbiologists have isolated and described many new microbial 53 54 24 species involved in most major biogeochemical cycles and some of which are able to grow at 55 56 25 more than 110°C and 150 MPa. Psychrophiles, mesophiles, hyper/thermophiles, acidophiles, 57 58 59 60 4 Page 5 of 82 Extremophiles
1 2 3 1 piezophiles and even moderate halophiles were isolated from samples originating from deep 4 5 2 sea hydrothermal vents constituting cultivable representatives of at least 20 phyla, 89 genus 6 7 3 and 175 species. This represents a little more than 1% of ∼12,391 prokaryotic cultured type 8 9 10 4 species (451 Archaea and 11,940 Bacteria ) (http://www.bacterio.net/ number.html#notea) 11 12 5 whose taxonomy has been well described (Euzéby 2013). These species belong to 35 13 14 6 different phyla (30 bacterial phyla and 5 archaeal phyla). The latest molecular biology 15 16 7 techniques allow us to see that the cultured and described species represent only ∼1‒2% of 17 18 For Peer Review 19 8 the Earth’s Bacteria and Archaea according to the SILVA database (http://www.arb silva.de), 20 21 9 which contains 534,968 of non redundant 16S rRNA sequences distributed as follows: 22 23 10 Bacteria (86.9%), Archaea (3.5%) and Eukarya (9.6%). 24 25 11 This review aims to provide an overview of the diversity of microorganisms thriving 26 27 12 in deep sea hydrothermal vents, their metabolic characteristics and the adaptive mechanisms 28 29 30 13 they have evolved to cope with HHP. 31 32 14 33 34 15 Deep sea hydrothermal vent ecosystems 35 36 16 Hydrothermalism 37 38 39 17 Deep sea hydrothermal vent sites (700 to 5000 m below the ocean surface) are located 40 41 18 in areas of high tectonic activity (Figure 1) such as areas of accretion along mid ocean ridges 42 43 19 (e.g. the mid Atlantic Ridge [MAR] or East Pacific Rise [EPR]), subduction zones, the back 44 45 20 arc basins (e.g. the North Fiji or Lau Basins) and finally hot spot volcanism (e.g. Loihi 46 47 21 Seamount near Hawaii) (Van Dover et al. 2002). According to the InterRidge Global 48 49 50 22 Database, about 600 active or ancient Submarine Hydrothermal Vent Fields have been 51 52 23 recorded in more than 200 locations throughout the Pacific, Atlantic, and Indian Oceans 53 54 24 confirmed or inferred (Figure 1), including 46 locations in Indian Ocean (depth from 1500 to 55 56 25 4200 m), 64 locations in the Atlantic Ocean (depth from 800 to 4530 m) and 100 locations in 57 58 59 60 5 Extremophiles Page 6 of 82
1 2 3 1 Pacific Ocean (depth from 850 to 5000 m). The activity of the tectonic plates generates 4 5 2 seafloor spreading centers (rifts), regions where hot basalt and magma near the sea floor cause 6 7 3 the floor to slowly drift apart. Seawater seeping into these cracked regions mixes with hot 8 9 10 4 minerals (Edmond et al. 1982) and, is emitted from the springs; these underwater hot springs 11 12 5 are known as hydrothermal vents. The mineral rich hot water (270 460°C) forms a cloud of 13 14 6 precipitated material upon mixing with oxygenated cold seawater (2‒3°C), these 15 16 7 hydrothermal vents are called black smokers. 17 18 8 InteractionsFor between deep Peer basaltic or ultramaficReview rocks and sea water brought to high 19 20 21 9 temperature and high pressure, which therefore has a high solvent power, will produce 22 23 10 hydrothermal fluids. These fluids may reach a temperature as high as 460°C, with an acidic 24 25 11 pH. They are anoxic and contain high concentrations of dissolved gases (H 2S, CH 4, CO, CO 2, 26 27 12 and H ) and minerals (Mn 2+ , Fe 2+ , Si +, Zn 2+ , etc.) (Figure 2) (Jannasch and Mottl 1985; 28 2 29 30 13 Johnson et al. 1986; Von Damm 2000; Charlou et al. 2002; Charlou et al. 2010). In contact 31 32 14 with sea water (cold, oxic with alkaline pH), minerals precipitate and form black smokers. 33 34 15 35 36 16 Metabolic and phylogenetic diversity of deep sea hydrothermal vents 37 38 17 Many Bacteria and Archaea can use sulfur, sulfates, thiosulfate, and Iron (III) oxide as 39 40 41 18 electron acceptors in anaerobic respiration and drive metabolisms like sulfur respiration, 42 43 19 sulfato respiration and thiosulfate respiration, iron respiration and Anaerobic Oxidation of 44 45 20 Methane (AOM). Fermentative metabolism is also a principal feature of many archaeal and 46 47 21 bacterial species isolated from deep sea hydrothermal vents (Takai and Nakamura 2011). 48 49 50 22 Except for some Thaumarchaeota that perform nitrification, oxygen and nitrate are 51 52 23 used as electrons acceptors by almost all bacteria that specific drive metabolisms such as 53 54 24 aerobic respiration, hydrogen oxidation, nitrification, methanotrophy and methylotrophy, 55 56 25 sulfur compound oxidation, iron oxidation, manganese oxidation, denitrification and 57 58 59 60 6 Page 7 of 82 Extremophiles
1 2 3 1 Annamox. Some metabolisms like methanogenesis and ammonia oxidation are specifically to 4 5 2 Archaea . The culture independent approach was used to describe the microbial phylogenetic 6 7 3 diversity in active deep sea hydrothermal vents from chimney fluid sediments and macrofauna 8 9 10 4 samples. Archaea are associated with hydrothermal edifices, fluids and sediments and 11 12 5 encompass archaeal groups like Thermococcales , Archaeoglobales , Desulfurococcales , 13 14 6 Ignicoccales , Methanococcales and Methanopyrales (Huber et al. 1989; Takai and Horikoshi 15 16 7 1999; Takai et al. 2001; Teske et al. 2002; Schrenk et al. 2004; Nunoura et al. 2010; Roussel 17 18 8 et al. 2011; Takai andFor Nakamura Peer 2011). Other groupsReview like Halobacteriales , Thaumarchaeota , 19 20 21 9 DHVE2 and MCG divisions were also detected in these ecosystems (Takai et al. 2001; 22 23 10 Roussel et al. 2011; Orcutt et al. 2011; Flores et al. 2012). 24 25 11 The Bacteria domain is dominated by Epsilonproteobacteria detected in hydrothermal 26 27 12 fluids, in sea water, hydrothermal sediments, microbial mats and in association with 28 29 30 13 macrofauna (Reysenbach et al. 2000; Alain et al. 2002b; Reysenbach et al. 2002; Teske et al. 31 32 14 2002; Huber et al. 2003; Page et al. 2004; Suzuki et al. 2005; Campbell et al. 2006; 33 34 15 Gerasimchuk et al. 2010; Crépeau et al. 2011; Sylvan et al. 2012); other bacterial groups were 35 36 16 also detected, such as Alpha , Beta , Delta and Gammaproteobacteria , Aquificales , 37 38 17 Desulfobacteriales , Thermotogales , Deinococcus-Thermus , Deferribacteres , Firmicutes , CFB 39 40 41 18 (Cytophaga-Flavobacteria-Bacteroidetes ), Acidobacteria , Verrumicrobia and 42 43 19 Planctomycetes (Alain et al. 2002a; Reysenbach et al. 2002; Teske et al. 2002; Huber et al. 44 45 20 2003; Page et al. 2004; Crépeau et al. 2011; Orcutt et al. 2011; Sylvan et al. 2012). More than 46 47 21 one hundred species of Bacteria (17 phyla, 72 genera, 113 species) and Archaea (3 phyla, 17 48 49 50 22 genera and 62 species) were isolated and cultured from deep sea hydrothermal vents, mainly 51 52 23 from the Pacific ocean (69‒77% of species) and, in lesser numbers, from the Atlantic 53 54 24 (19‒28% of species) and Indian (2‒4% of species) Oceans. 55 56 25 57 58 59 60 7 Extremophiles Page 8 of 82
1 2 3 1 4 5 2 Knowledge on piezophiles vs other extremophiles from deep sea hydrothermal 6 7 3 vents 8 9 10 4 The field of piezomicrobiology has been held back by requirements for expensive 11 12 5 high pressure laboratory equipment for sample containment and culture. The first HHP 13 14 6 adapted prokaryotes were bacteria isolated from deep sea sediments in 1949 by ZoBell and 15 16 7 Johnson (Zobell and Johnson 1949). In 1979, the group of Professor Yayanos reported the 17 18 8 isolation of the firstFor piezophilic Peer bacterium from Review the cold deep ocean and two years later 19 20 21 9 (Yayanos et al. 1981) isolated the first obligate piezophile microorganism, a psychrophilic 22 23 10 bacterium isolated from a decaying amphipod fished from the bottom of the Mariana Trench. 24 25 11 However, although deep sea hydrothermal vent fields were explored at depths ranging 26 27 12 from 800 to 5000 m, rather few attempts to enrich isolates under in situ pressures have been 28 29 30 13 carried out. Almost all hyper/thermophilic vent prokaryotes have been isolated under 31 32 14 atmospheric pressure, and few of them have been exposed to HHP. To our knowledge, only a 33 34 15 few microorganisms have been described that are both piezotolerant and piezophilic, these 35 36 16 include representatives from across both Archaea and Bacteria domains: Pyrococcus abyssi 37 38 17 (Erauso et al. 1993) Thermococcus barophilus (Marteinsson et al. 1999), Thermococcus 39 40 41 18 aggregans (Canganella et al., 2000), Thermococcus guaymasensis (Canganella et al., 1998), 42 43 19 Thermococcus peptonophilus (Canganella et al. 1997), Thermococcus eurythermalis (Zhao et 44 45 20 al., 2015), Palaeococcus ferrophilus (Takai et al. 2000), Palaeococcus pacificus (Zeng et al. 46 47 21 2012), Methanopyrus kandleri (Takai et al. 2008), Marinitoga piezophila (Alain et al. 2002a), 48 49 50 22 Thermosipho japonicus (Takai and Horikoshi, 2000), Thioprofundum lithotrophica , 51 52 23 Piezobacter thermophilus (Takai et al. 2009) and Desulfovibrio hydrothermalis (Alazard 53 54 24 2003). The first obligate piezophilic anaerobic hyperthermophilic archaeon discovered was 55 56 25 Pyrococcus yayanosii , isolated from ultramafic a deep sea hydrothermal vent field named 57 58 59 60 8 Page 9 of 82 Extremophiles
1 2 3 1 “Ashadze” located on the Mid Atlantic Ridge at 4100 m depth (Zeng et al. 2009; Birrien et al. 4 5 2 2011). P. yayanosii , T. barophilus and M. piezophila were isolated after enrichment cultures 6 7 3 performed under both high temperatures and HHP; they showed the highest growth rates 8 9 10 4 when grown under hydrostatic pressures and their genomes were entirely sequenced and 11 12 5 annotated (Jun et al. 2011; Vannier et al. 2011; Lucas et al. 2012). However, when T. 13 14 6 barophilus and M. piezophila grew under atmospheric pressure, their growth rates were 15 16 7 lower. 17 18 8 Microbes inFor the deep seaPeer hydrothermal Review environment face contrasted and fluctuating 19 20 21 9 environmental conditions, to which they need to adapt or die. Hydrothermal vents are 22 23 10 characterized by large fluctuations in salinity and temperature, from 0.1 to twice the salinity 24 25 11 of seawater (Jannasch and Mottl 1985), and from fluid temperatures as high as 460°C at the 26 27 12 heart of the vent, to 2°C, the average temperature of the surrounding deep ocean waters (Oger 28 29 30 13 and Jebbar, 2010). Prokaryotes residing in the vent ecosystem will thus experience situations 31 32 14 of heat, cold, acidic, or salinity stresses. In addition in the deepest parts of the oceans, 33 34 15 hydrothermal vent ecosystems are also submitted to extremely HHP, which is known to 35 36 16 impact the structure of several cellular components and functions, such as membrane fluidity, 37 38 17 protein activity and structure (Oger and Jebbar 2010). Physically the impact of pressure bears 39 40 41 18 resemblance to both a lowering of temperature, since it will reinforce the structure of certain 42 43 19 molecules, such as membrane lipids, and an increase in temperature, since it will as well 44 45 20 destabilize other structures, such as proteins. These environmental stressors will affect the cell 46 47 21 structure and metabolism. 48 49 50 22 The hyper/thermophiles piezophiles prokaryotes may have evolved a combination of 51 52 23 several adaptive mechanisms (compatible solutes accumulation, efficient expression and 53 54 24 activity of prefoldins, membrane fluidity maintaining, robust biocatalysts, etc) to face harsh 55 56 25 and fluctuating conditions prevailing in deep sea hydrothermal vents, thus their cellular 57 58 59 60 9 Extremophiles Page 10 of 82
1 2 3 1 processes such as motility, cell division, nutrient uptake, membrane protein function, protein 4 5 2 synthesis and replication are not or less impaired by HHP such as it was observed in 6 7 3 piezosensitive species E. coli or S. cerevisiae . 8 9 10 4 In the following two sections we will, respectively, address a quick overview of the 11 12 5 main physiological adaptive strategies of vent prokaryotes and molecular adaptations in the 13 14 6 structure of proteins. 15 16 7 17 18 8 Physiology Forand adaptation Peer Review 19 20 21 9 Due to the environmental fluctuations, microorganisms from hydrothermal vents are 22 23 10 expected to show strong osmotic adaptation. In a simplistic way, the effect of salinity and heat 24 25 11 stresses may be reduced to one factor, e.g. the reduced activity of water within or in the 26 27 12 vicinity of the cells, with a number of consequences, e.g. for the inward or outward fluxes of 28 29 30 13 cellular salts and the destabilization of the function and structure of cellular components. 31 32 14 Under reduced water activity, proteins fold incorrectly, which reduces or stops protein 33 34 15 activity. We know two strategies of osmoadaptation to high temperature or salinity in hyper 35 36 16 thermophilic prokaryotes isolated from shallow or deep sea hydrothermal vents (da Costa et 37 38 17 al. 1998). Extremely halophilic Archaea and a few halophilic Bacteria accumulate K +, Na + 39 40 41 18 and Cl in response to changes in extracellular salinity (Vreeland 1987; Csonka and Hanson 42 43 19 1991; Galinski and Truper 1994), while a common strategy among microorganisms to cope 44 45 20 with osmotic stress is the accumulation of low molecular mass organic compounds, also 46 47 21 known as compatible solutes because they do not interfere with cellular metabolism (Brown 48 49 50 22 1976; Galinski 1995; Ventosa et al. 1998). Compatible solutes of hyperthermophiles are 51 52 23 similar to those used by mesophiles, i.e. sugars, amino acids, polyols. In addition, 53 54 24 hyperthermophiles also accumulate solutes little or never encountered in mesophiles such as 55 56 25 mannosylglycerate (MG) (Martins et al. 1997), di myo 1,1' inositol phosphate (DIP) (Martins 57 58 59 60 10 Page 11 of 82 Extremophiles
1 2 3 1 et al. 1996), diglycerol phosphate and derivatives of these compounds (da Costa et al. 1998; 4 5 2 Santos and da Costa 2001). These two solutes are essentially restricted to thermophiles 6 7 3 (Santos and da Costa 2002). MG is accumulated mostly in response to salt stress in Archaea 8 9 10 4 such as Pyrococcus furiosus , Pyrococcus horikoshii , Thermococcus celer , Thermococcus 11 12 5 stetteri or Thermococcus litoralis and Bacteria such as Thermus thermophilus (Martins and 13 14 6 Santos 1995; Nunes et al. 1995; Lamosa et al. 1998; Empadinhas et al. 2001). In the same 15 16 7 Archaea , DIP is accumulated in response to supra optimal temperature of growth. In the 17 18 8 family ThermococcalesFor, there Peer are three noticeable Review exceptions to this shared osmolyte 19 20 21 9 accumulation pattern. First, Thermococcus kodakarensis , which does not seem to accumulate 22 23 10 MG under heat or salt stress; second, Pyrolobus fumarii , which only accumulates DIP as a 24 25 11 response to both stresses (Goncalves et al. 2008); and finally P. ferrophilus , which lacks the 26 27 12 DIP synthesis genes and accumulates only MG as a response to both stresses. MG is mostly 28 29 30 13 accumulated in response to high salinity, in amounts above 0.6 µmol/mg protein, in the 31 32 14 genera Palaeococcus (Neves et al. 2005), Pyrococcus (Martins and Santos 1995; Empadinhas 33 34 15 et al. 2001) or Thermococcus (Lamosa et al. 1998). DIP is usually accumulated in response to 35 36 16 high temperatures in amounts above 1 µmol/mg of protein in T. celer (Lamosa et al. 1998) 37 38 17 and P. furiosus (Martins and Santos 1995). Osmolytes, such as MG or DIP, create a protective 39 40 41 18 shell surrounding the proteins, which helps maintain proper folding and protein functions 42 43 19 (Lamosa et al. 2003). Natural osmolytes increase protein thermal stability in vitro (Santos and 44 45 20 da Costa 2002). In hyperthermophiles, MG has been shown to preserve protein folding 46 47 21 through an increase of protein rigidity (Borges et al. 2002). 48 49 50 22 In piezophiles, studies devoted to characterizing the role of compatible solutes in 51 52 23 response to HHP have been very limited. Interestingly, P. profundum accumulates β 53 54 24 hydroxybutyrate (both monomers and oligomers) in response to hydrostatic pressure (Martin 55 56 25 et al. 2002), M. piezophila accumulates only amino acids ( α glutamate, proline and alanine) 57 58 59 60 11 Extremophiles Page 12 of 82
1 2 3 1 under atmospheric pressure, but the role of these compatible solutes in adaptation to HHP has 4 5 2 not been investigated (Lamosa et al. 2013). 6 7 3 As the first and ultimate barrier between the intracellular space and the outside world, 8 9 10 4 biological membranes play a fundamental role in the adaptation of microbes to their 11 12 5 environment. The function of the membrane is threefold: 1) to act as a physical barrier to 13 14 6 regulate inward and outward trafficking, 2) to play a central role in energy storage and 15 16 7 processing via ion gradients, and 3) to provide a matrix for environmental sensing, 17 18 8 multicomponent metabolicFor and Peer signaling pathways Review and motility. Thus, maintaining optimal 19 20 21 9 membrane biological function is crucial for any organism. Temperature , pH , salinity or 22 23 10 hydrostatic pressure induced perturbations in membrane organization pose a serious challenge 24 25 11 for the cell. Archaeal and bacterial membranes are very dissimilar in structure, although they 26 27 12 perform identical functions. However, as will be demonstrated below, the mechanisms 28 29 30 13 employed to adapt to extreme conditions and fluctuating environments are essentially similar. 31 32 14 Bacterial polar lipids, apart from a few rare exceptions, are based on straight chain 33 34 15 hydrocarbons linked by ester bonds on the sn 1 and sn 2 positions of glycerol. Archaeal polar 35 36 16 lipids are composed of isoprenoid hydrocarbon chains bound by ether bonds to the sn 2 and 37 38 17 sn 3 positions of glycerol (Figure 3). Polar headgroups consist of phosphodiester linked polar 39 40 41 18 groups or sugar moieties on the sn 1 ( Archaea ) or sn 3 ( Bacteria ) positions of the glycerol 42 43 19 backbone ( sn glycerol 1 phosphate, or G 1 P, structure and sn glycerol 3 phosphate, or G 3 44 45 20 P, structure). 46 47 21 Based on the observation that the membrane lipids of E. coli cells grown under the 48 49 50 22 contrasting temperatures of 43°C and 15°C were different (Marr and Ingraham 1962; 51 52 23 Sinensky 1971) while the respective membranes displayed similar physical properties at their 53 54 24 respective growth temperatures, Sinensky modeled the basis of homeoviscous adaptation 55 56 25 (Sinensky 1974; Oger and Cario 2013). This theory states that organisms adapt their 57 58 59 60 12 Page 13 of 82 Extremophiles
1 2 3 1 membrane lipid composition to favor the maintenance of the appropriate membrane fluidity 4 5 2 for it to function optimally. This concept is now understood in a broader sense to include 6 7 3 adaptation to proton/water permeability and the dynamic nature of the plasmic membranes 8 9 10 4 (McElhaney 1984a; McElhaney 1984b; van de Vossenberg et al. 1999; Oger and Cario 2013). 11 12 5 Homeoviscous adaptation must also be understood as a means to rapidly adapt the 13 14 6 composition, and thus the functionality, of the membrane to brutal environmental fluctuations, 15 16 7 or aggressions, including those of heat and cold, salinity, osmotic stress, pressure and pH. 17 18 8 Under normalFor physiological Peer conditions, Review membranes are relatively fluid, disordered 19 20 21 9 liquid crystalline phases. When the temperature drops, or hydrostatic pressure increases, the 22 23 10 membrane lipids may undergo the fluid to gel phase transition. When the temperature 24 25 11 increases above the physiological conditions, or the pressure decreases from these, the rate of 26 27 12 motion of lipids in the membrane will be increased, this may impact membrane stability and 28 29 30 13 intrinsic permeability. As can be expected, perturbation in lipid phase state has profound 31 32 14 consequences on membrane structure and function (Lee 2003; Lee 2004). Transition to the gel 33 34 15 phase may induce the clustering of membrane proteins, which appear de facto, excluded from 35 36 16 the zones in the gel phase, reducing the diffusion and the activity of proteins in the membrane 37 38 17 and slowing the flux of transported solutes, but increasing the permeability to cations and 39 40 41 18 water. 42 43 19 Adaptation of bacterial membrane properties follows four major routes. 1) The 44 45 20 variation of acyl chain length: an increase of the chain length by two carbons increases the 46 47 21 phase transition temperature of the lipid by 10 to 20°C, and decreases membrane permeability 48 49 50 22 to proton and water (Winter 2002). 2) The accumulation of unsaturated fatty acids: the 51 52 23 incorporation of a single unsaturation can shift the fluid/gel phase transition by 10 to 20°C 53 54 24 (Russell and Nichols 1999; Winter 2002). 3) The accumulation of specific polar headgroups 55 56 25 such as phosphatidylcholine (PC) or phosphatidylglycerol (PG) in place of 57 58 59 60 13 Extremophiles Page 14 of 82
1 2 3 1 phosphatidylethanolamine (PE). The presence of PC as a polar headgroup results in a drastic 4 5 2 shift of the fluid/gel transition temperature (Yano et al. 1998; Winter 2002; Mangelsdorf et al. 6 7 3 2005; Winter and Jeworrek 2009). This is due in part to the reduced hydration and stearic 8 9 10 4 bulk of the ethanolamine compared to choline, and the capacity of PE, and incapacity of PC, 11 12 5 groups to form hydrogen bonds. 4) The accumulation of branched fatty acid. 13 14 6 Archaeal lipid membranes generally have much lower phase transition temperature 15 16 7 than fatty acyl ester lipids (Yamauchi et al. 1993). Part of the adaptation of the archaeal 17 18 8 membrane to extremeFor environments Peer may originate Review from the original structure of its lipids. 19 20 21 9 While membranes made of fatty acyl ester lipids are in the gel phase or in the liquid 22 23 10 crystalline phase depending mostly on their fatty acid composition, archaeol and 24 25 11 caldarchaeol based polar lipid membranes of Archaea are assumed to be in the liquid 26 27 12 crystalline phase at a wide temperature range of 0–100°C (Stewart et al. 1990; Dannenmuller 28 29 30 13 et al. 2000). In addition, most if not all Archaea from the hydrothermal environments 31 32 14 synthesize membrane spanning bipolar tetraether lipids that form monolayers. The monolayer 33 34 15 organization provides extreme rigidity to these membranes. Lateral mobility studies 35 36 16 demonstrate that the lateral diffusion rate at 80°C is comparable between Sulfolobus 37 38 17 acidocaldarius or T. acidphilum and E. coli at 37°C. However, in contrast to bacterial lipids, 39 40 41 18 which exhibit similar lateral diffusion rates for temperatures close to the phase transition 42 43 19 temperature, in T. acidphilum these values are observed approximately 65°C above the 44 45 20 nominal lipid phase transition temperature (Jarrell et al. 1998). 46 47 21 The adaptation of archaeal membrane properties is very similar in its physics to that of 48 49 50 22 bacteria, although it takes slightly different routes to converge to the same effects. There exist 51 52 23 several different routes, as follows. 1) The incorporation of cyclopentane rings along the 53 54 24 isoprenoid chain as a function of fluctuating temperature (De Rosa et al. 1980a; De Rosa et al. 55 56 25 1980b; Ernst et al. 1998; Uda et al. 2001; Uda et al. 2004) or pH (Shimada et al. 2008) 57 58 59 60 14 Page 15 of 82 Extremophiles
1 2 3 1 increases the packing efficiency of the membrane lipids (Gliozzi et al. 1983), which increases 4 5 2 membrane stability as a function of increasing temperature or salinity and decreasing pressure 6 7 3 or pH, and consequently lowers the permeability (Chong et al. 2012). 2) The regulation of the 8 9 10 4 tetraether to diether lipid ratio (Sprott et al. 1991; Lai et al. 2008; Matsuno et al. 2009): 11 12 5 increase in tetraether lipids will stabilize the membranes by forming monolayer type 13 14 6 membranes or domains in the membrane, helping to regulate the flux of solutes and protons 15 16 7 across the membrane. 3) The crosslinking of the two acyl chains of the lipids to yield 17 18 8 macrocyclic archaeolFor or caldarchaeol Peer derivatives Review by a covalent bond between the isoprenoid 19 20 21 9 chains reduces the motion of the molecule creating a more closely packed structure and 22 23 10 increasing the membrane stability, creating an efficient barrier against water, proton and 24 25 11 solute leakage (Dannenmuller et al. 2000; Mathai et al. 2001). 4) The increase in unsaturation 26 27 12 along the isoprenoid chains of the lipids as a function of temperature (Nichols et al. 2004) or 28 29 30 13 salinity (Dawson et al. 2012) has to date only been described in the psychrophilic methanogen 31 32 14 Methanococcoides burtonii (Franzmann et al. 1992; Nichols et al. 2004), but unsaturated 33 34 15 lipids have been characterized in several species of hyperthermophiles (Hafenbradl et al. 35 36 16 1993; Gonthier et al. 2001), which might indicate the occurrence of a similar adaptive strategy 37 38 17 in hydrothermal vent organisms. 39 40 41 18 Adaptation of bacterial and archaeal membranes to the harsh environment of the 42 43 19 hydrothermal system is clearly visible in the lipids most commonly present. However, 44 45 20 responding to the variations of environmental stressors might only involve a fraction of the 46 47 21 adaptive traits mentioned above. Indeed, in order to be efficient, the membrane composition 48 49 50 22 adaptation response needs to be very quick. The routes described require different timeframes. 51 52 23 Thus, certain adaptive mechanisms will prevail over others. For example, the increasing 53 54 24 unsaturation of membrane lipids will decrease the gel/fluid transition temperature to the same 55 56 25 extent as the shortening of one of the acyl chains, or the substitution of a phosphatidylcholine 57 58 59 60 15 Extremophiles Page 16 of 82
1 2 3 1 by a phosphatidylethanolamine polar head, but will be quicker because it is performed inside 4 5 2 the cytoplasmic membrane on existing lipids by a membrane protein (Kasai et al. 1976; 6 7 3 Cybulski et al. 2002; Aguilar and de Mendoza 2006; Beranova et al. 2008), while the other 8 9 10 4 actions would need de novo lipid synthesis. 11 12 5 13 14 6 Molecular adaptation of deep sea enzymes 15 16 7 While extremophilic adaptation has been extensively studied for temperature and salt 17 18 8 adapted enzymes,For very little Peer is known aboutReview pressure adaptation. Pressure induced 19 20 21 9 modifications of the protein volume may arise from a global elastic compression within 22 23 10 closely related conformational sub states or from promotion of conformational sub states 24 25 11 presenting lower specific volumes, up to complete unfolding of the protein (Fourme et al. 26 27 12 2006; Akasaka 2006; Akasaka et al. 2013). These modifications originate from changes in the 28 29 30 13 various interactions between amino acids (hydrogen bond, ionic, van der Waals and 31 32 14 hydrophobic interactions), from changes in the internal voids and cavities found in proteins, 33 34 15 and from changes in the hydration properties (Li et al. 1998; Marchi and Akasaka 2001; 35 36 16 Boonyaratanakornkit et al. 2002; Refaee et al. 2003; Girard et al. 2005; Nisius and Grzesiek 37 38 17 2012). As protein folding, substrate recognition, protein protein interactions and protein 39 40 41 18 hydration rely upon a combination of these various interactions, pressure may affect all 42 43 19 protein mechanisms through its influence on them (Masson et al. 2004; Occhipinti et al. 2006; 44 45 20 Ohmae et al. 2008; Rosenbaum et al. 2012). 46 47 21 Studies that link pressure induced structural modifications to alterations or 48 49 50 22 stimulations of biological functions are rare. However, it was shown that, for example, 51 52 23 pressure induces minor changes in the orientation of a chromophore in the protein citrine, 53 54 24 leading to a pressure induced continuous shift of the fluorescence peak (Barstow et al. 2008). 55 56 25 The effect of pressure on the internal solvent excluded void volume has been proposed as a 57 58 59 60 16 Page 17 of 82 Extremophiles
1 2 3 1 major contribution to protein activity (Fourme et al. 2006; Girard et al. 2010), but mainly in 4 5 2 protein pressure induced unfolding (Collins et al. 2005; Rouget et al. 2011; Roche et al. 6 7 3 2012). Indeed, the role of a hydrophobic cavity, positioned close to the active site pocket, has 8 9 10 4 been proposed to play a major role in urate oxidase (Girard et al. 2010). Pressure induced an 11 12 5 expansion of the active site pocket correlated with a volume reduction of the hydrophobic 13 14 6 cavity, leading to an inactivation of the protein. It was proposed (Girard et al. 2010) and 15 16 7 confirmed (Marassio et al. 2011) that this particular cavity acts as ballast, providing the 17 18 8 required plasticity ofFor the active Peersite pocket durin Reviewg the urate oxidase catalytic process. A recent 19 20 21 9 study (Roche et al. 2012) provided evidence that cavities that are present in the folded state 22 23 10 and absent in the unfolded state make a large contribution to the volume difference between 24 25 11 folded and unfolded states that govern pressure induced unfolding of proteins. Such internal 26 27 12 cavities might also play a role in the pressure dissociation of protein oligomers and aggregates 28 29 30 13 (Foguel et al. 2003; Girard et al. 2010). 31 32 14 In general, monomeric proteins are quite resistant to high pressure and do not undergo 33 34 15 denaturation under a pressure of 300 MPa (Robb and Clark 1999; Sun et al. 1999), but in 35 36 16 some cases unfolding has been observed at moderate pressure (Gorovits et al. 1995). 37 38 17 Oligomeric proteins can be dissociated by lower pressure than monomeric proteins; 39 40 41 18 for example, in the GroEl chaperonin complex (14 subunits) from E. coli , dissociation 42 43 19 occurred at 130 MPa (Gorovits et al. 1995), while the RuBisCO from Rhodospirillum rubrum 44 45 20 already started to dissociate at 40 MPa (Erijman et al. 1993). Interestingly, these pressure 46 47 21 values lie within the physiological range of many deep sea organisms. However, the picture is 48 49 50 22 more complex than this would make it appear because some oligomeric assemblies have been 51 52 23 described to withstand pressure up to 1 GPa for the dimeric protein, bovine erythrocyte Cu, 53 54 24 Zn superoxide dismutase (Ascone et al. 2010), up to 400 MPa for the cowpea mosaic virus 55 56 57 58 59 60 17 Extremophiles Page 18 of 82
1 2 3 1 capsid (Fourme et al. 2002) or up to 300 MPa and 90°C for the 12 subunit TET 4 5 2 aminopeptidase from the archaeon P. horikoshii (Rosenbaum et al. 2012). 6 7 3 The existence of a specific molecular adaptation to prolonged exposure to pressure 8 9 10 4 such as the one encountered in the deep sea or in the sediments is suggested by the recent 11 12 5 discovery of obligate piezophilic microbes such as P. yayanosii (Zeng et al. 2009; Birrien et 13 14 6 al. 2011) or Shewanella benthica (Lauro et al. 2013). Moreover, as already mentioned above, 15 16 7 piezophilic strains display a typical cellular stress response when they are grown at 17 18 8 atmospheric pressure.For This suggests Peer that a signific Reviewant part of the proteome is adapted at the 19 20 21 9 molecular level and, conversely, that the stabilization and enzymatic processes of many 22 23 10 proteins must be adapted to colonize the deeper part of the biosphere. As said before, each 24 25 11 protein will experience pressure differently depending on its specific 3D structure and the 26 27 12 pressure sensitivity of an organism may be controlled by a limited number of proteins. 28 29 30 13 Most deep sea organisms are exposed to hydrostatic pressures of 20 to 110 MPa. Due 31 32 14 to the prominent effects of pressure on intermolecular surfaces, it is commonly believed that 33 34 15 large molecular systems are significantly affected in this pressure range. It is apparently the 35 36 16 case, for instance, for the translational activity that is entirely lost when the pressure was up to 37 38 17 90 MPa (Lu et al. 1997). Pressure induced dissociation of ribosomes has been considered a 39 40 41 18 major cause of the inhibition of bacterial growth in the deep sea. Cell free assays showed that 42 43 19 the post translocational complex represents the most pressure sensitive intermediate of the 44 45 20 elongation cycle and is possibly the limiting factor for the pressure induced block of protein 46 47 21 biosynthesis (Gross et al. 1993). High hydrostatic pressure (HHP) has also been suggested to 48 49 50 22 influence the structure and function of membrane proteins. The effect of hydrostatic pressure 51 + 52 23 on mitochondrial H ATPase revealed that the complex was inactivated in the pressure range 53 54 24 of 60‒180 MPa (Dreyfus et al. 1988). The effect of high hydrostatic pressure was also studied 55 56 25 on the bacterial mechanosensitive channel. In this case, pressure significantly affected channel 57 58 59 60 18 Page 19 of 82 Extremophiles
1 2 3 1 kinetics between 0 and 90 MPa. The reduced activity was attributed to a shortening of the 4 5 2 channel openings due to lateral compression of the bilayer under high hydrostatic pressure 6 7 3 (Macdonald and Martinac 2005). Dimer dissociation of Vibrio cholerae ToxR membrane 8 9 10 4 protein was observed at 20 to 50 MPa in vivo in E. coli reporter strains (Macdonald and 11 12 5 Martinac 2005). These observations indicated that piezophilic adaptation principally targeted 13 14 6 large molecular machines and membrane systems. Accordingly, the volume change upon 15 16 7 Actin polymerization was found to be smaller in the case of a deep sea fish than commonly 17 18 8 measured in surfaceFor organisms Peer (Morita 2003). ReviewThe transcriptional activities and the subunit 19 20 21 9 dissociations of the RNA polymerases from the piezophile Shewanella violacea and the one 22 23 10 of E. coli were compared and revealed a better resistance of the deep sea machinery after 24 25 11 pressure treatment (Kawano et al. 2004). All these observations suggest that important 26 27 12 structural modifications occur in large supramolecular assemblies that make it possible to 28 29 30 13 adapt to a high pressure environment. However, the structure determination of such large 31 32 14 protein complexes is a technical challenge in structural biology that hampers the comparative 33 34 15 structural and biophysical studies of large molecular systems arising from different pressure 35 36 16 environments. 37 38 17 Compared to complex cellular machines, the metabolic enzymes represent tractable 39 40 41 18 systems to reveal the structural determinants of piezophilicity. For many enzymes, the 42 43 19 biochemistry involves simple substrates and cofactors, and kinetics parameters can be 44 45 20 extracted straightforwardly to assess whether or not the reaction is favoured by high pressure. 46 47 21 It also exists a consistent knowledge for their structure function relationships and, in some 48 49 50 22 cases, such as the Lactate Malate deshydrogenase family, the molecular determinants for 51 52 23 thermal or halophilic adaptations have already been explored (Madern et al. 2000; Luke et al. 53 54 24 2007; Sawle and Ghosh 2011). Considering that the stability and the enzymatic properties of 55 56 25 most studied mesophilic proteins do not show important alterations in the pressure range that 57 58 59 60 19 Extremophiles Page 20 of 82
1 2 3 1 is encountered in the deep sea; the existence of a piezophilic adaptation at the enzyme level 4 5 2 remains controversial. However, comparative biochemical studies on enzymes arising from 6 7 3 surfaces and deep sea organisms revealed differences indicating that catalytic reactions are 8 9 10 4 more efficient under high pressure for deep sea enzymes. The study of tetrameric lactate 11 12 5 dehydrogenases (LDH) from hagfish living at different depth showed that pressure 13 14 6 inactivation was less pronounced for the abyssal species (Nishiguchi et al. 2008). Several 15 16 7 studies were performed on thermophilic enzymes. They revealed an increase in half life at 17 18 8 high temperature withFor increasing Peer pressure, thus Review suggesting that high pressure should be taken 19 20 21 9 into account in temperature adaptation (Hei and Clark 1994; Sun et al. 1999; Mombelli et al. 22 23 10 2002). However, these studies focused on residual activities and do not allow us to conclude 24 25 11 whether pressure inactivation and thermal stabilization are due to differences in oligomers 26 27 12 (Hei and Clark 1994) dissociation, unfolding or subtle structural changes, for example at the 28 29 30 13 active site level. A study on a large aminopeptidase tetrahedral complex (TET) from the deep 31 32 14 sea archaeon P. horikoshii , in which small angle X ray scattering (SAXS) and activity 33 34 15 measurements were performed under high pressure and high temperature, showed that the 12 35 36 16 subunits molecular edifice maintains its quaternary structure up to 300 MPa (Rosenbaum et 37 38 17 al. 2012). This study suggested that large molecular complexes could maintain high pressure 39 40 41 18 stability far beyond the pressure that the organisms could encounter in the deepest part of the 42 43 19 oceans. Interestingly, the catalytic behaviour of the system was enhanced by pressure. The 44 45 20 determination of the volume changes associated with catalysis indicated a change in the 46 47 21 reaction rate limiting step at 180 MPa. This suggested that pressure adaptation could occur at 48 49 50 22 the active site level in this peptidase family. However, comparative studies on different TET 51 52 23 peptidases arising from surface and deep sea organisms are essential to draw a conclusion on 53 54 24 this matter. Such comparative studies have been performed on dihydrofolate reductases 55 56 25 (DHFR) from Shewanella species living in deep sea and atmospheric pressure environments 57 58 59 60 20 Page 21 of 82 Extremophiles
1 2 3 1 (Ohmae et al. 2012). The stabilities of these enzymes were found to be similar and the 4 5 2 pressure effects did not indicate that the catalytic processes of deep sea DHFR enzymes are 6 7 3 better adapted to high pressure environments. However, 3 isopropylmalate dehydrogenase 8 9 10 4 from the obligate piezophile Shewanella benthica DB21MT 2 (SbIPMDH) remains active in 11 12 5 extreme conditions whereas that isolated from the land bacterium S. oneidensis MR 1 13 14 6 (SoIPMDH) becomes inactivated. Comparison of the structures of the two enzymes shows 15 16 7 that SbIPMDH has a larger internal cavity volume than SoIPMDH. This loosely packed 17 18 8 structure of SbIPMDHFor may limitPeer pressure induced Review modification of the native structure, 19 20 21 9 keeping it active at higher pressures compared to SoIPMDH (Nagae et al. 2012). This study 22 23 10 highlighted the potential role of internal cavity in high pressure adaptation. 24 25 11 26 27 12 Conclusions 28 29 30 13 Based on the studies described above, a number of mechanisms explaining pressure 31 32 14 resistance and possible adaptation to HHP can be proposed. However, comparative 33 34 15 experimental studies combining enzymology, biophysics, structure and microbiology 35 36 16 approaches performed under high pressure are still essential to make a decisive statement on 37 38 17 the existence of a specific kind of pressure adaptation in deep sea organisms. As already 39 40 41 18 underlined, proteins are dynamic entities. High pressure adaptive traits might therefore only 42 43 19 be revealed by molecular dynamics studies such as high pressure crystallography or neutron 44 45 20 spectroscopy. Finally, transcriptomic and proteomic studies are vital for revealing the identity 46 47 21 of the proteins that are mostly impacted by high or low pressure, either to compensate for 48 49 50 22 losses of cellular functions or as bona fide key players in pressure adaptation. 51 52 23 At this time it is not yet clear if HHP adaptations require just a change of one or a few 53 54 24 genes in a few pathways, an overall alteration of many genes in a genome, or mainly 55 56 25 regulatory modulations. Several reasons may explain our present inability to identify specific 57 58 59 60 21 Extremophiles Page 22 of 82
1 2 3 1 signatures associated with HHP. First, thus far, only piezosensitive ( E. coli , S. cerevisiae ) or 4 5 2 moderately piezophile strains ( P. profundum strain SS9, Popt = 28 MPa) have been studied 6 7 3 extensively. As a consequence, HHP adaptation, if it exists, might not be sufficient to be 8 9 10 4 demonstrated. Secondly, all results converge to demonstrate a large overlap between cold and 11 12 5 HHP regulation. 13 14 6 The diversity of piezophiles isolated so far from deep sea hydrothermal vents is 15 16 7 narrow and consists of prokaryotes driving metabolisms such as sulfatoreduction, 17 18 8 sulforeduction, methanogenesisFor Peer and fermentation, Review which does not represent the large 19 20 21 9 metabolic diversity encountered in these ecosystems. Autochthonous microorganisms of the 22 23 10 deep sea hydrothermal vents are inherently adapted to the extreme conditions of their 24 25 11 environment, i.e. to the high pressure, low to high temperature, low to high pH, anaerobiosis 26 27 12 to aerobiosis conditions found throughout the deep sea hydrothermal vents. Much more effort 28 29 30 13 should be put into isolating new and varied piezophiles from deep sea hydrothermal vents, 31 32 14 including i) development of adapted and specialized high pressure equipment to maintain 33 34 15 samples at in situ pressure and temperature once onboard ship, ii) improvement of knowledge 35 36 16 and imagination about geochemistry of their ambient environment, extracellular milieu and 37 38 17 try to recreate viable laboratory conditions, and iii) patience, which has sometimes been 39 40 41 18 rewarded by very long term incubation of cultures. 42 43 19 44 45 20 Acknowledgments This work was supported by the Agence Nationale de la Recherche 46 47 21 (ANR 10 BLAN 1725 01 Living deep). We are indebted to Helen McCombie [Bureau de 48 49 50 22 Traduction de l’Université (BTU), Université de Bretagne Occidentale Brest] for helpful 51 52 23 language improvement. 53 54 24 55 56 25 57 58 59 60 22 Page 23 of 82 Extremophiles
1 2 3 1 References 4 5 6 2 Aguilar PS, de Mendoza D (2006) Control of fatty acid desaturation: a mechanism conserved 7 3 from bacteria to humans. Mol Microbiol 62:1507–1514. 8 9 10 4 Akasaka K (2006) Probing conformational fluctuation of proteins by pressure perturbation. 11 5 Chem Rev 106:1814–35. doi: 10.1021/cr040440z 12 13 6 Akasaka K, Kitahara R, Kamatari YO (2013) Exploring the folding energy landscape with 14 7 pressure. Arch Biochem Biophys 531:110–5. doi: 10.1016/j.abb.2012.11.016 15 16 8 Alain K, Marteinsson VT, Miroshnichenko ML, et al. (2002a) Marinitoga piezophila sp. nov., 17 9 a rod shaped, thermo piezophilic bacterium isolated under high hydrostatic pressure 18 For Peer Review 19 10 from a deep sea hydrothermal vent. Int J Syst Evol Microbiol 52:1331–1339. 20 21 11 Alain K, Olagnon M, Desbruyères D, et al. (2002b) Phylogenetic characterization of the 22 12 bacterial assemblage associated with mucous secretions of the hydrothermal vent 23 13 polychaete Paralvinella palmiformis . FEMS Microbiol Ecol 42:463–476. 24 25 14 Alazard D (2003) Desulfovibrio hydrothermalis sp. nov., a novel sulfate reducing bacterium 26 15 isolated from hydrothermal vents. Int J Syst Evol Microbiol 53:173–178. doi: 27 16 10.1099/ijs.0.02323 0 28 29 30 17 Ascone I, Savino C, Kahn R, Fourme R (2010) Flexibility of the Cu,Zn superoxide dismutase 31 18 structure investigated at 0.57 GPa. Acta Crystallogr D Biol Crystallogr 66:654–63. doi: 32 19 10.1107/S0907444910012321 33 34 20 Bale SJ, Goodman K, Rochelle P a, et al. (1997) Desulfovibrio profundus sp. nov., a novel 35 21 barophilic sulfate reducing bacterium from deep sediment layers in the Japan Sea. Int J 36 22 Syst Bacteriol 47:515–21. 37 38 39 23 Barstow B, Ando N, Kim CU, Gruner SM (2008) Alteration of citrine structure by hydrostatic 40 24 pressure explains the accompanying spectral shift. Proc Natl Acad Sci U S A 41 25 105:13362–6. doi: 10.1073/pnas.0802252105 42 43 26 Beranova J, Jemiola Rzeminska M, Elhottova D, et al. (2008) Metabolic control of the 44 27 membrane fluidity in Bacillus subtilis during cold adaptation. Biochim Biophys Acta 45 28 Biomembranes 1778:445–453. 46 47 48 29 Birrien JL, Zeng X, Jebbar M, et al. (2011) Pyrococcus yayanosii sp. nov., an obligate 49 30 piezophilic hyperthermophilic archaeon isolated from a deep sea hydrothermal vent. Int 50 31 J Syst Evol Microbiol 61:2827–2831. doi: 10.1099/ijs.0.024653 0 51 52 32 Boonyaratanakornkit BB, Park CB, Clark DS (2002) Pressure effects on intra and 53 33 intermolecular interactions within proteins. Biochim Biophys Acta 1595:235–249. 54 55 34 Borges N, Ramos A, Raven NDH, et al. (2002) Comparative study of the thermostabilizing 56 35 properties of mannosylglycerate and other compatible solutes on model enzymes. 57 58 36 Extremophiles 6:209–216. 59 60 23 Extremophiles Page 24 of 82
1 2 3 1 Brown AD (1976) Microbial water stress. Bacteriol Rev 40:803–846. 4 5 2 Campbell B, Engel A, Porter M, Takai K (2006) The versatile epsilon proteobacteria: key 6 3 players in sulphidic habitats. Nat Rev Microbio 4:458–468. 7 8 4 Canganella, F., Gambacorta, A., Kato, C., Horikoshi, K., 2000. Effects of hydrostatic pressure 9 10 5 and temperature on physiological traits of Thermococcus guaymasensis and 11 6 Thermococcus aggregans growing on starch. Microbiological Research 154:297 306 12 13 7 Canganella, F., Gonzalez, J.M., Yanagibayashi, M., Kato, C., Horikoshi, K., 1997. Pressure 14 8 and temperature effects on growth and viability of the hyperthermophilic archaeon 15 9 Thermococcus peptonophilus . Arch. Microbiol. 168:1 7 16 17 10 Canganella, F., Jones, W.J., Gambacorta, A., Antranikian, G., 1998. Thermococcus 18 For Peer Review 19 11 guaymasensis sp. nov. and Thermococcus aggregans sp. nov., two novel thermophilic 20 12 archaea isolated from the Guaymas Basin hydrothermal vent site. International Journal of 21 13 Systematic Bacteriology 48:1181 1185 22 23 14 Chamieh H, Marty V, Guetta D, et al. (2012) Stress regulation of the PAN proteasome system 24 15 in the extreme halophilic archaeon Halobacterium . Extremophiles 16:215–225. doi: 25 16 10.1007/s00792 011 0421 0 26 27 17 Charlou JL, Donval JP, Fouquet Y, et al. (2002) Geochemistry of high H(2) and CH(4) vent 28 29 18 fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36 degrees 14 ’ 30 19 N, MAR). Chem Geol 191:345–359. doi: 10.1016/s0009 2541(02)00134 1 31 32 20 Charlou JL, Donval JP, Konn C, et al. (2010) High production of H 2 and CH4 and abiotic 33 21 hydrocarbons in ultramafic hosted hydrothermal systems on the Mid Atlantic Ridge. 34 22 Geochim Cosmochim Acta 74:A163–A163. 35 36 23 Chong PL, Ayesa U, Daswani VP, Hur EC (2012) On physical properties of tetraether lipid 37 24 membranes: effects of cyclopentane rings. Archaea 2012:138439. doi: 38 39 25 10.1155/2012/138439 40 41 26 Colletier J P, Aleksandrov A, Coquelle N, et al. (2012) Sampling the conformational energy 42 27 landscape of a hyperthermophilic protein by engineering key substitutions. Mol Biol 43 28 Evol 29:1683–94. doi: 10.1093/molbev/mss015 44 45 29 Collins MD, Hummer G, Quillin ML, et al. (2005) Cooperative water filling of a nonpolar 46 30 protein cavity observed by high pressure crystallography and simulation. Proc Natl Acad 47 48 31 Sci U S A 102:16668–71. doi: 10.1073/pnas.0508224102 49 50 32 Coquelle N, Fioravanti E, Weik M, et al. (2007) Activity, stability and structural studies of 51 33 lactate dehydrogenases adapted to extreme thermal environments. J Mol Biol 374:547– 52 34 562. doi: 10.1016/j.jmb.2007.09.049 53 54 35 Coquelle N, Talon R, Juers DH, et al. (2010) Gradual adaptive changes of a protein facing 55 36 high salt concentrations. J Mol Biol 404:493–505. doi: 10.1016/j.jmb.2010.09.055 56 57 58 59 60 24 Page 25 of 82 Extremophiles
1 2 3 1 Da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of 4 2 compatible solutes in Bacteria and Archaea. Adv Biochem Eng Biotechnol 61:117–153. 5 6 3 Crépeau V, Cambon Bonavita, MA Lesongeur F, Randrianalivelo H, et al. (2011) Diversity 7 4 and function in microbial mats from the Lucky Strike hydrothermal vent field. FEBS 8 5 Lett 76:524–540. 9 10 11 6 Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation Genetics and physiology. Annu 12 7 Rev Microbiol 45:569–606. 13 14 8 Cybulski LE, Albanesi D, Mansilla MC, et al. (2002) Mechanism of membrane fluidity 15 9 optimization: isothermal control of the Bacillus subtilis acyl lipid desaturase. Mol 16 10 Microbiol 45:1379–1388. 17 18 For Peer Review 19 11 Von Damm KL (2000) Chemistry of hydrothermal vent fluids from 9 degrees 10 degrees N, 20 12 East Pacific Rise: “Time zero,” the immediate posteruptive period. J Geophys Res Earth 21 13 105:11203–11222. doi: 10.1029/1999jb900414 22 23 14 Dannenmuller O, Arakawa K, Eguchi T, et al. (2000) Membrane properties of archaeal 24 15 macrocyclic diether phospholipids. Chemistry (Easton) 6:645–654. 25 26 16 Dawson KS, Freeman KH, Macalady JL (2012) Molecular characterization of core lipids 27 17 from halophilic archaea grown under different salinity conditions. Org Geochem 48:1–8. 28 29 30 18 Dobson CM (2003) Protein folding and misfolding. Nature 426:884–890. doi: 31 19 10.1038/nature02261 32 33 20 Van Dover CL, German CR, Speer KG, et al. (2002) Evolution and biogeography of deep sea 34 21 vent and seep invertebrates. Science (80 ) 295:1253–1257. doi: 35 22 10.1126/science.1067361 36 37 23 Dreyfus G, Guimaraes Motta H, Silva J (1988) Effect of hydrostatic pressure on the 38 39 24 mitochondrial ATP synthase. Biochemistry 27:6704–6710. 40 41 25 Ebel C, Costenaro L, Pascu M, et al. (2002) Solvent interactions of halophilic malate 42 26 dehydrogenase. Biochemistry 41:13234–13244. 43 44 27 Edmond JM, Vondamm KL, McDuff RE, Measures CI (1982) Chemistry of hot springs on 45 28 the east pacific rise and their effluent dispersal.. Nature 297:187–191. doi: 46 29 10.1038/297187a0 47 48 49 30 Empadinhas N, Marugg JD, Borges N, et al. (2001) Pathway for the synthesis of 50 31 mannosylglycerate in the hyperthermophilic archaeon Pyrococcus horikoshii 51 32 Biochemical and genetic characterization of key enzymes. J Biol Chem 276:43580– 52 33 43588. 53 54 34 Erauso G, Reysenbach AL, Godfroy A, et al. (1993) Pyrococcus abyssi sp nov, a new 55 35 hyperthermophilic archaeon isolated from a deep sea hydrothermal vent. Arch Microbiol 56 36 160:338–349. 57 58 59 60 25 Extremophiles Page 26 of 82
1 2 3 1 Erijman L, Lorimer G, Weber G (1993) Reversible dissociation and conformational stability 4 2 of dimeric ribulose bisphosphate carboxylase. Biochemistry 32:5187–5195. 5 6 3 Ernst M, Freisleben HJ, Antonopoulos E, et al. (1998) Calorimetry of archaeal tetraether lipid 7 4 indication of a novel metastable thermotropic phase in the main phospholipid from 8 5 Thermoplasma acidophilum cultured at 59 degrees C. Chem Phys Lipids 94:1–12. 9 10 11 6 Euzéby J (2013) List of prokaryotic names with standing in nomenclature. 12 7 http://www.bacterio.net/number.html . Accessed 26 July 2013. 13 14 8 Flores GE, Wagner ID, Liu Y, Reysenbach A L (2012) Distribution, abundance, and diversity 15 9 patterns of the thermoacidophilic “deep sea hydrothermal vent euryarchaeota 2”. Front 16 10 Microbiol 3:47. doi: 10.3389/fmicb.2012.00047 17 18 For Peer Review 19 11 Foguel D, Suarez MC, Ferrão Gonzales AD, et al. (2003) Dissociation of amyloid fibrils of 20 12 alpha synuclein and transthyretin by pressure reveals their reversible nature and the 21 13 formation of water excluded cavities. Proc Natl Acad Sci U S A 100:9831–6. doi: 22 14 10.1073/pnas.1734009100 23 24 15 Fourme R, Ascone I, Kahn R, et al. (2002) Opening the High Pressure Domain beyond 2 kbar 25 16 to Protein and Virus Crystallography. Structure 10:1409–1414. 26 27 17 Fourme R, Girard E, Kahn R, et al. (2006) High pressure macromolecular crystallography 28 29 18 (HPMX): status and prospects. Biochim Biophys Acta 1764:384–90. doi: 30 19 10.1016/j.bbapap.2006.01.008 31 32 20 Franzmann PD, Springer N, Ludwig W, et al. (1992) A methanogenic archaeon from Ace 33 21 Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15:573–581. 34 35 22 Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:272–328. 36 37 23 Galinski EA, Truper HG (1994) Microbial behavior in salt stressed ecosystems. FEMS 38 39 24 Microbiol Rev 15:95–108. 40 41 25 Gerasimchuk a. L, Shatalov a. a., Novikov a. L, et al. (2010) The search for sulfate reducing 42 26 bacteria in mat samples from the lost city hydrothermal field by molecular cloning. 43 27 Microbiology 79:96–105. doi: 10.1134/S0026261710010133 44 45 28 Girard E, Kahn R, Mezouar M, et al. (2005) The first crystal structure of a macromolecular 46 29 assembly under high pressure: CpMV at 330 MPa. Biophys J 88:3562–71. doi: 47 48 30 10.1529/biophysj.104.058636 49 50 31 Girard E, Marchal S, Perez J, et al. (2010) Structure function perturbation and dissociation of 51 32 tetrameric urate oxidase by high hydrostatic pressure. Biophys J 98:2365–73. doi: 52 33 10.1016/j.bpj.2010.01.058 53 54 34 Gliozzi A, Rolandi R, De Rosa M, Gambacorta A (1983) Monolayer black membranes from 55 35 bipolar lipids of archaebacteria and their temperature induced structural changes. J 56 36 Membr Biol 75:45–56. 57 58 59 60 26 Page 27 of 82 Extremophiles
1 2 3 1 Goncalves LG, Lamosa P, Huber R, Santos H (2008) Di myo inositol phosphate and novel 4 2 UDP sugars accumulate in the extreme hyperthermophile Pyrolobus fumarii . 5 3 Extremophiles 12:383–389. doi: 10.1007/s00792 008 0143 0 6 7 4 Gonthier I, Rager MN, Metzger P, et al. (2001) A di O dihydrogeranylgeranyl glycerol from 8 5 Thermococcus S557, a novel ether lipid, and likely intermediate in the biosynthesis of 9 10 6 diethers in Archaea. Tetrahedron Lett 42:2795–2797. 11 12 7 Gorovits B, Raman C, Horowitz P (1995) High hydrostatic pressure induces the dissociation 13 8 of cpn60 tetradecamers and reveals a plasticity of the monomers. J Biol Chem 270:2061– 14 9 2066. 15 16 10 Gross M, Auerbach G, Jaenicke R (1993) The catalytic activities of monomeric enzymes 17 11 show complex pressure dependence. FEBS Lett 321:256–260. 18 For Peer Review 19 20 12 Hafenbradl D, Keller M, Thiericke R, Stetter KO (1993) A novel unsaturated archael ether 21 13 core lipid from the hyperthermophile Methanopyrus kandleri . Syst Appl Microbiol 22 14 16:165–169. 23 24 15 Hei DJ, Clark DS (1994) Pressure Stabilization of Proteins from Extreme Thermophiles. Appl 25 16 Env Microbiol 60:932–939. 26 27 17 Huber J, Butterfield D, Baross J (2003) Bacterial diversity in a subseafloor habitat following a 28 29 18 deep sea volcanic eruption. FEMS Microbiol Ecol 43:393–409. 30 31 19 Huber R, Kurr M, Jannasch K, Stetter K (1989) A novel group of abyssal methanogenic 32 20 archaebacteria ( Methanopyrus ) growing at 110°C. Nature 342:833–834. 33 34 21 Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep sea hydrothermal vents. Science 35 22 (80 ) 229:717–725. doi: 10.1126/science.229.4715.717 36 37 23 Jarrell HC, Zukotynski KA, Sprott GD (1998) Lateral diffusion of the total polar lipids from 38 39 24 Thermoplasma acidophilum in multilamellar liposomes. Biochim Biophys Acta 40 25 Biomembranes 1369:259–266. 41 42 26 Johnson K, Beehler C, Sakamoto Arnold C, Childress J (1986) In situ measurements of 43 27 chemical distributions in a deep sea hydrothermal vent field. Science (80 ) 231:1139– 44 28 1141. 45 46 29 Jun X, Lupeng L, Minjuan X, et al. (2011) Complete genome sequence of the obligate 47 48 30 piezophilic hyperthermophilic archaeon Pyrococcus yayanosii CH1. J Bacteriol 49 31 193:4297–4298. doi: 10.1128/JB.05345 11 50 51 32 Kallmeyer J, Pockalny R, Adhikari RR, et al. (2012) Global distribution of microbial 52 33 abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109:16213– 53 34 16216. doi: 10.1073/pnas.1203849109 54 55 35 Kasai R, Kitajima Y, Martin CE, et al. (1976) Molecular control of membrane properties 56 36 during temperature acclimatation Membrane fluidity regulation of fatty acid desaturase 57 58 37 action. Biochemistry 15:5228–5233. 59 60 27 Extremophiles Page 28 of 82
1 2 3 1 Kawano H, Nakasone K, Matsumoto M, et al. (2004) Differential pressure resistance in the 4 2 activity of RNA polymerase isolated from Shewanella violacea and Escherichia coli . 5 3 Extremophiles 8:367–375. doi: 10.1007/s00792 004 0397 0 6 7 4 Khelaifia S, Fardeau M L, Pradel N, et al. (2011) Desulfovibrio piezophilus sp. nov., a 8 5 piezophilic, sulfate reducing bacterium isolated from wood falls in the Mediterranean 9 10 6 Sea. Int J Syst Evol Microbiol 61:2706–11. doi: 10.1099/ijs.0.028670 0 11 12 7 Koga Y (2011) Early evolution of membrane lipids: How did the lipid divide occur? J Mol 13 8 Evol 72:274–282. 14 15 9 Koga Y, Morii H (2007) Biosynthesis of ether type polar lipids in archaea and evolutionary 16 10 considerations. Microbiol Mol Biol Rev 71:97–120. 17 18 For Peer Review 19 11 Koga Y, Morii H (2005) Recent advances in structural research on ether lipids from archaea 20 12 including comparative and physiological aspects. Biosci Biotechnol Biochem 69:2019– 21 13 2034. 22 23 14 Koutsopoulos S, van der Oost J, Norde W (2005) Temperature dependent structural and 24 15 functional features of a hyperthermostable enzyme using elastic neutron scattering. 25 16 Proteins 61:377–384. 26 27 17 Lai D, Springstead JR, Monbouquette HG (2008) Effect of growth temperature on ether lipid 28 29 18 biochemistry in Archaeoglobus fulgidus. Extremophiles 12:271–278. 30 31 19 Lamosa P, Martins LO, Da Costa MS, Santos H (1998) Effects of temperature, salinity, and 32 20 medium composition on compatible solute accumulation by Thermococcus spp. Appl 33 21 Env Microbiol 64:3591–3598. 34 35 22 Lamosa P, Rodrigues M V, Gonçalves LG, et al. (2013) Organic solutes in the deepest 36 23 phylogenetic branches of the Bacteria: identification of α(1 6)glucosyl α(1 37 24 2)glucosylglycerate in Persephonella marina . Extremophiles 17:137–46. doi: 38 39 25 10.1007/s00792 012 0500 x 40 41 26 Lamosa P, Turner DL, Ventura R, et al. (2003) Protein stabilization by compatible solutes. 42 27 Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin 43 28 studied by NMR. Eur J Biochem 270:4606–4614. 44 45 29 Lauro F, Chastain R, Ferriera S, et al. (2013) Draft Genome Sequence of the Deep Sea 46 30 Bacterium Shewanella benthica Strain KT99. Genome Announc 1:pii: e00210–13. doi: 47 48 31 10.1128/genomeA.00210 13.Copyright 49 50 32 Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. 51 33 Biochim Biophys Acta 1612:1–40. 52 53 34 Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim 54 35 Biophys Acta Biomembranes 1666:62–87. 55 56 36 Li H, Yamada H, Akasaka K (1998) Effect of Pressure on Individual Hydrogen Bonds in 57 58 37 Proteins . Basic Pancreatic trypsin inhibitor. Biochemistry 37:1167–1173. 59 60 28 Page 29 of 82 Extremophiles
1 2 3 1 Lu B, Li Q, Liu W, Ruan K (1997) Effects of hydrostatic pressure on the activity of rat 4 2 ribosome and cell free translation system. Biochem Mol Biol Int 43:499–506. 5 6 3 Lucas S, Han J, Lapidus A, et al. (2012) Complete genome sequence of the thermophilic, 7 4 piezophilic, heterotrophic bacterium Marinitoga piezophila KA3. J Bacteriol 194:5974– 8 5 5975. doi: 10.1128/JB.01430 12 9 10 11 6 Luke KA, Higgins CL, Wittung Stafshede P (2007) Thermodynamic stability and folding of 12 7 proteins from hyperthermophilic organisms. FEBS J 274:4023–4033. doi: 13 8 10.1111/j.1742 4658.2007.05955.x 14 15 9 Macario AJL, Lange M, Ahring BK, et al. (1999) Stress genes and proteins in the archaea. 16 10 Microbiol Mol Biol Rev 63:923–67, table of contents. 17 18 For Peer Review 19 11 Macdonald AG, Martinac B (2005) Effect of high hydrostatic pressure on the bacterial 20 12 mechanosensitive channel MscS. Eur Biophys J 34:434–41. doi: 10.1007/s00249 005 21 13 0478 8 22 23 14 Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91– 24 15 98. 25 26 16 Mangelsdorf K, Zink KG, Birrien JL, Toffin L (2005) A quantitative assessment of pressure 27 17 dependent adaptive changes in the membrane lipids of piezosensitive deep sub seafloor 28 29 18 bacterium. Org Geochem 36:1459–1479. 30 31 19 Marassio G, Prangé T, David HN, et al. (2011) Pressure response analysis of anesthetic gases 32 20 xenon and nitrous oxide on urate oxidase: a crystallographic study. FASEB J 25:2266– 33 21 75. doi: 10.1096/fj.11 183046 34 35 22 Marchi M, Akasaka K (2001) Simulation of hydrated BPTI at high pressure : changes in 36 23 hydrogen bonding and its relation with NMR experiments. J Phys Chem B 105:711–714. 37 38 39 24 Marr AG, Ingraham JL (1962) Effect of temperature on the composition of fatty acids in 40 25 Escherichia coli .. J Bacteriol 84:1260–1267. 41 42 26 Marteinsson VT, Birrien JL, Reysenbach AL, et al. (1999) Thermococcus barophilus sp. nov., 43 27 a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic 44 28 pressure from a deep sea hydrothermal vent. Int J Syst Bacteriol 49 Pt 2:351–359. 45 46 29 Martin DD, Bartlett DH, Roberts MF (2002) Solute accumulation in the deep sea bacterium 47 48 30 Photobacterium profundum . Extremophiles 6:507–14. doi: 10.1007/s00792 002 0288 1 49 50 31 Martins LO, Carreto LS, DaCosta MS, Santos H (1996) New compatible solutes related to di 51 32 myo inositol phosphate in members of the order Thermotogales. J Bacteriol 178:5644– 52 33 5651. 53 54 34 Martins LO, Huber R, Huber H, et al. (1997) Organic solutes in hyperthermophilic Archaea. 55 35 Appl Environ Microbiol 63:896–902. 56 57 58 59 60 29 Extremophiles Page 30 of 82
1 2 3 1 Martins LO, Santos H (1995) Accumulation of mannosylglycerate and di myo inosytol 4 2 phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl Environ 5 3 Microbiol 61:3299–3303. 6 7 4 Masson P, Bec N, Froment M T, et al. (2004) Rate determining step of butyrylcholinesterase 8 5 catalyzed hydrolysis of benzoylcholine and benzoylthiocholine. Volumetric study of 9 10 6 wild type and D70G mutant behavior. Eur J Biochem 271:1980–90. doi: 10.1111/j.1432 11 7 1033.2004.04110.x 12 13 8 Mathai JC, Sprott GD, Zeidel ML (2001) Molecular mechanisms of water and solute transport 14 9 across archaebacterial lipid membranes. J Biol Chem 276:27266–27271. 15 16 10 Matsumi R, Atomi H, Driessen AJM, van der Oost J (2011) Isoprenoid biosynthesis in 17 11 Archaea Biochemical and evolutionary implications. Res Microbiol 162:39–52. 18 For Peer Review 19 20 12 Matsuno Y, Sugai A, Higashibata H, et al. (2009) Effect of growth temperature and growth 21 13 phase on the lipid composition of the archaeal membrane from Thermococcus 22 14 kodakaraensis . Biosci Biotechnol Biochem 73:104–108. doi: 10.1271/bbb.80520 23 24 15 McElhaney RN (1984a) The structure and function of the Acholeplasma laidlawii plasma 25 16 membrane. Biochim Biophys Acta 779:1–42. 26 27 17 McElhaney RN (1984b) The relationship between membrane fluidity and phase state and the 28 29 18 ability of bacteria and mycoplasma to grow and survive at various temperatures. In: 30 19 Kates M, Manson LA (eds) Membr. fluidity. Plenum Press, New York, pp 249–276 31 32 20 Mombelli E, Shehi E, Fusi P, Tortora P (2002) Exploring hyperthermophilic proteins under 33 21 pressure: theoretical aspects and experimental findings. Biochim Biophys Acta 25:392– 34 22 396. 35 36 23 Morita T (2003) Structure based analysis of high pressure adaptation of alpha actin. J Biol 37 24 Chem 278:28060–28066. doi: 10.1074/jbc.M302328200 38 39 40 25 Nagae T, Kato C, Watanabe N (2012) Structural analysis of 3 isopropylmalate dehydrogenase 41 26 from the obligate piezophile Shewanella benthica DB21MT 2 and the nonpiezophile 42 27 Shewanella oneidensis MR 1. Acta Crystallogr Sect F Struct Biol Cryst Commun 43 28 68:265–8. doi: 10.1107/S1744309112001443 44 45 29 Neves C, da Costa MS, Santos H (2005) Compatible solutes of the hyperthermophile 46 30 Palaeococcus ferrophilus : osmoadaptation and thermoadaptation in the order 47 48 31 thermococcales. Appl Env Microbiol 71:8091–8098. doi: 10.1128/AEM.71.12.8091 49 32 8098.2005 50 51 33 Nichols DS, Miller MR, Davies NW, et al. (2004) Cold adaptation in the antarctic archaeon 52 34 Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186:8508– 53 35 8515. 54 55 36 Nishiguchi Y, Miwa T, Abe F (2008) Pressure adaptive differences in lactate dehydrogenases 56 37 of three hagfishes: Eptatretus burgeri , Paramyxine atami and Eptatretus okinoseanus . 57 58 38 Extremophiles 12:477–480. doi: 10.1007/s00792 008 0140 3 59 60 30 Page 31 of 82 Extremophiles
1 2 3 1 Nisius L, Grzesiek S (2012) Key stabilizing elements of protein structure identified through 4 2 pressure and temperature perturbation of its hydrogen bond network. Nat Chem 4:711–7. 5 3 doi: 10.1038/nchem.1396 6 7 4 Nunes OC, Manaia CM, Dacosta MS, Santos H (1995) Compatible solutes in the thermophilic 8 5 bacteria Rhodothermus marinus and Thermus thermophilus . Appl Environ Microbiol 9 10 6 61:2351–2357. 11 12 7 Nunoura T, Oida H, Nakaseama M, et al. (2010) Archaeal diversity and distribution along 13 8 thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV 14 9 hydrothermal field in the Southern Okinawa trough. Appl Env Microbiol 76:1198–1211. 15 10 doi: 10.1128/AEM.00924 09 16 17 11 Occhipinti E, Bec N, Gambirasio B, et al. (2006) Pressure and temperature as tools for 18 For Peer Review 19 12 investigating the role of individual non covalent interactions in enzymatic reactions 20 13 Sulfolobus solfataricus carboxypeptidase as a model enzyme. Biochim Biophys Acta 21 14 1764:563–72. doi: 10.1016/j.bbapap.2005.12.007 22 23 15 Oger PM, Cario A (2013) Adaptation of the membrane in Archaea. Biophys Chem. doi: 24 16 10.1016/j.bpc.2013.06.020 25 26 17 Oger PM, Jebbar M (2010) The many ways of coping with pressure. Res Microbiol 161:799– 27 18 809. doi: 10.1016/j.resmic.2010.09.017 28 29 30 19 Ohmae E, Murakami C, Tate S, et al. (2012) Pressure dependence of activity and stability of 31 20 dihydrofolate reductases of the deep sea bacterium Moritella profunda and Escherichia 32 21 coli . Biochim Biophys Acta 1824:511–519. doi: 10.1016/j.bbapap.2012.01.001 33 34 22 Ohmae E, Tatsuta M, Abe F, et al. (2008) Effects of pressure on enzyme function of 35 23 Escherichia coli dihydrofolate reductase. Biochim Biophys Acta 1784:1115–21. doi: 36 24 10.1016/j.bbapap.2008.04.005 37 38 39 25 Orcutt BN, Bach W, Becker K, et al. (2011) Colonization of subsurface microbial 40 26 observatories deployed in young ocean crust. ISME J 5:692–703. doi: 41 27 10.1038/ismej.2010.157 42 43 28 Page A, Juniper S, Olagnon M, et al. (2004) Microbial diversity associated with a 44 29 Paralvinella sulfincola tube and the adjacent substratum on an active deep sea vent 45 30 chimney. Geobiology 2:225–238. 46 47 48 31 Ramos A, Raven NDH, Sharp RJ, et al. (1997) Stabilization of enzymes against thermal stress 49 32 and freeze drying by mannosylglycerate. Appl Environ Microbiol 63:4020–4025. 50 51 33 Refaee M, Tezuka T, Akasaka K, Williamson MP (2003) Pressure dependent Changes in the 52 34 Solution Structure of Hen Egg white Lysozyme. J Mol Biol 327:857–865. doi: 53 35 10.1016/S0022 2836(03)00209 2 54 55 36 Reysenbach AL, Gotz D, Banta A, et al. (2002) Expanding the distribution of the Aquificales 56 37 to the deep sea vents on Mid Atlantic ridge and central Indian Ocean ridge. Cah Biol 57 58 38 Mar 43:425–428. 59 60 31 Extremophiles Page 32 of 82
1 2 3 1 Reysenbach AL, Longnecker K, Kirshtein J (2000) Novel bacterial and archaeal lineages 4 2 from an in situ growth chamber deployed at a Mid Atlantic Ridge hydrothermal vent. 5 3 Appl Env Microbiol 66:3798–3806. 6 7 4 Robb FT, Clark DS (1999) Adaptation of proteins from hyperthermophiles to high pressure 8 5 and high temperature. J Mol Microbiol Biotechnol 1:101–105. 9 10 11 6 Roche J, Caro J a, Norberto DR, et al. (2012) Cavities determine the pressure unfolding of 12 7 proteins. Proc Natl Acad Sci U S A 109:6945–50. doi: 10.1073/pnas.1200915109 13 14 8 De Rosa M, Esposito E, Gambacorta A, et al. (1980a) Complex lipids of Caldariella 15 9 acidophila , a thermoacidophile archaebacterium. Phytochemistry 19:821–826. 16 17 10 De Rosa M, Esposito E, Gambacorta A, et al. (1980b) Effects of temperature on ether lipid 18 For Peer Review 19 11 composition of Caldariella acidophila . Phytochemistry 19:827–831. 20 21 12 Rosenbaum E, Gabel F, Durá MA, et al. (2012) Effects of hydrostatic pressure on the 22 13 quaternary structure and enzymatic activity of a large peptidase complex from 23 14 Pyrococcus horikoshii . Arch Biochem Biophys 517:104–10. doi: 24 15 10.1016/j.abb.2011.07.017 25 26 16 Rouget J B, Aksel T, Roche J, et al. (2011) Size and Sequence and the Volume Change of 27 17 Protein Folding. J Am Chem Soc 133:6020–6027. doi: 10.1021/ja200228w.Size 28 29 30 18 Roussel EG, Konn C, Charlou JL, et al. (2011) Comparison of microbial communities 31 19 associated with three Atlantic ultramafic hydrothermal systems. FEMS Microbiol Ecol 32 20 77:647–665. doi: 10.1111/j.1574 6941.2011.01161.x 33 34 21 Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria a dogma 35 22 rewritten. Microbiology 145 ( Pt 4:767–779. 36 37 23 Santos H, da Costa MS (2001) Organic solutes from thermophiles and hyperthermophiles. 38 39 24 Methods Enzym 334:302–315. 40 41 25 Santos H, da Costa MS (2002) Compatible solutes of organisms that live in hot saline 42 26 environments. Env Microbiol 4:501–509. 43 44 27 Sawle L, Ghosh K (2011) How do thermophilic proteins and proteomes withstand high 45 28 temperature? Biophys J 101:217–227. 46 47 48 29 Schrenk M, Kelley D, Bolton S, Baross J (2004) Low archaeal diversity linked to subseafloor 49 30 geochemical processes at the Lost City Hydrothermal Field, Mid Atlantic Ridge. Env 50 31 Microbiol 6:1086–1095. 51 52 32 Shimada H, Nemoto N, Shida Y, et al. (2008) Effects of pH and temperature on the 53 33 composition of polar lipids in Thermoplasma acidophilum HO 62. J Bacteriol 190:5404– 54 34 5411. 55 56 35 Sinensky M (1971) Temperature control of phospholipid biosynthesis in Escherichia coli. J 57 58 36 Bacteriol 106:449–455. 59 60 32 Page 33 of 82 Extremophiles
1 2 3 1 Sinensky M (1974) Homeoviscous adaptation Homerostatic process that regulates viscosity 4 2 of membrane lipids in Escherichia coli . Proc Natl Acad Sci U S A 71:522–525. 5 6 3 Sprott GD, Meloche M, Richards JC (1991) Proportions of diether, macrocyclic diether, and 7 4 tetraether lipids in Methanococcus jannaschii grown at different temperatures. J 8 5 Bacteriol 173:3907–3910. 9 10 11 6 Stewart LC, Kates M, Ekiel IH, Smith ICP (1990) Molecular order and dynnamics of 12 7 diphytanylglycerol phospholipids A 2H NMR and 31P NMR study. Chem Phys Lipids 13 8 54:115–129. 14 15 9 Sun MM, Tolliday N, Vetriani C, et al. (1999) Pressure induced thermostabilization of 16 10 glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus . Protein Sci 17 11 8:1056–63. doi: 10.1110/ps.8.5.1056 18 For Peer Review 19 20 12 Suzuki Y, Sasaki T, Suzuki M, et al. (2005) Novel chemoautotrophic endosymbiosis between 21 13 a member of the Epsilonproteobacteria and the hydrothermal vent gastropod 22 14 Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Env 23 15 Microbiol 71:5440–5450. doi: 10.1128/AEM.71.9.5440 5450.2005 24 25 16 Sylvan JB, Pyenson BC, Rouxel O, et al. (2012) Time series analysis of two hydrothermal 26 17 plumes at 9°50’N East Pacific Rise reveals distinct, heterogeneous bacterial populations. 27 18 Geobiology 10:178–192. doi: 10.1111/j.1472 4669.2011.00315.x 28 29 30 19 Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep sea hydrothermal vent 31 20 environments. Genetics 152:1285–1297. 32 33 21 Takai, K., Horikoshi, K., 2000. Thermosipho japonicus sp. nov., an extremely thermophilic 34 22 bacterium isolated from a deep sea hydrothermal vent in Japan. Extremophiles 4:9 17 35 36 23 Takai K, Komatsu T, Inagaki F, Horikoshi K (2001) Distribution of archaea in a black smoker 37 24 chimney structure. Appl Env Microbiol 67:3618–3629. doi: 10.1128/AEM.67.8.3618 38 39 25 3629.2001 40 41 26 Takai K, Miyazaki M, Hirayama H, et al. (2009) Isolation and physiological characterization 42 27 of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep sea 43 28 hydrothermal vent chimney. Env Microbiol 11:1983–1997. doi: 10.1111/j.1462 44 29 2920.2009.01921.x 45 46 30 Takai K, Nakamura K (2011) Archaeal diversity and community development in deep sea 47 48 31 hydrothermal vents. Curr Opin Microbiol 14:282–291. doi: 10.1016/j.mib.2011.04.013 49 50 32 Takai K, Nakamura K, Toki T, et al. (2008) Cell proliferation at 122 degrees C and 51 33 isotopically heavy CH4 production by a hyperthermophilic methanogen under high 52 34 pressure cultivation. Proc Natl Acad Sci U S A 105:10949–10954. doi: 53 35 10.1073/pnas.0712334105 54 55 36 Takai K, Sugai A, Itoh T, Horikoshi K (2000) Palaeococcus ferrophilus gen. nov., sp. nov., a 56 37 barophilic, hyperthermophilic archaeon from a deep sea hydrothermal vent chimney. Int 57 58 38 J Syst Evol Microbiol 50 Pt 2:489–500. 59 60 33 Extremophiles Page 34 of 82
1 2 3 1 Tehei M, Franzetti B, Madern D, et al. (2004) Adaptation to extreme environments: 4 2 macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO 5 3 Rep 5:66–70. doi: 10.1038/sj.embor.7400049 6 7 4 Tehei M, Madern D, Franzetti B, Zaccai G (2005) Neutron scattering reveals the dynamic 8 5 basis of protein adaptation to extreme temperature. J Biol Chem 280:40974–40979. doi: 9 10 6 10.1074/jbc.M508417200 11 12 7 Teske A, Hinrichs K, Edgcomb V, et al. (2002) Microbial Diversity of Hydrothermal 13 8 Sediments in the Guaymas Basin : Evidence for Anaerobic Methanotrophic Communities 14 9 †. 68:1994–2007. doi: 10.1128/AEM.68.4.1994 15 16 10 Uda I, Sugai A, Itoh YH, Itoh T (2001) Variation in molecular species of polar lipids from 17 11 Thermoplasma acidophilum depends on growth temperature. Lipids 36:103–105. 18 For Peer Review 19 20 12 Uda Y, Sugai A, Itoh YH, Itoh T (2004) Variation in molecular species of core lipids from the 21 13 order Thermoplasmales strains depends on the growth temperature. J Oleo Sci 53:399– 22 14 404. 23 24 15 Vannier P, Marteinsson VT, Fridjonsson OH, et al. (2011) Complete genome sequence of the 25 16 hyperthermophilic, piezophilic, heterotrophic, and carboxydotrophic archaeon 26 17 Thermococcus barophilus MP. J Bacteriol 193:1481–1482. doi: 10.1128/JB.01490 10 27 28 29 18 Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. 30 19 Microbiol Mol Biol Rev 62:504–544. 31 32 20 Van de Vossenberg J, Driessen AJM, da Costa MS, Konings WN (1999) Homeostasis of the 33 21 membrane proton permeability in Bacillus subtilis grown at different temperatures. 34 22 Biochim Biophys Acta Biomembranes 1419:97–104. 35 36 23 Vreeland RH (1987) Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol 37 24 14:311–356. doi: 10.3109/10408418709104443 38 39 40 25 Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl 41 26 Acad Sci U S A 95:6578–6583. 42 43 27 Winter R (2002) Effect of lipid chain length, temperature, pressure and composition on the 44 28 lateral organisation and phase behavior of lipid bilayer/gramicidin mixtures. Biophys J 45 29 82:153A–153A. 46 47 48 30 Winter R, Jeworrek C (2009) Effect of pressure on membranes. Soft Matter 5:3157–3173. 49 50 31 Yamauchi K, Doi K, Yoshida Y, Kinoshita M (1993) Archaebacterial lipids: highly proton 51 32 impermeable membranes from 1,2 diphytanyl sn glycero 3 phosphocholine. 52 33 BiochimBiophysActa 1146:178–182. 53 54 34 Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting 55 35 cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830. doi: 56 36 10.1242/jeb.01730 57 58 59 60 34 Page 35 of 82 Extremophiles
1 2 3 1 Yano Y, Nakayama A, Ishihara K, Saito H (1998) Adaptive changes in membrane lipids of 4 2 barophilic bacteria in response to changes in growth pressure. Appl Env Microbiol 5 3 64:479–485. 6 7 4 Yayanos AA, Dietz AS, Van Boxtel R (1981) Obligately barophilic bacterium from the 8 5 Mariana trench. Proc Natl Acad Sci U S A 78:5212–5215. 9 10 11 6 Zaccai G (2013) The ecology of protein dynamics. Curr Phys Chem 3:9–16. 12 13 7 Zeng X, Birrien JL, Fouquet Y, et al. (2009) Pyrococcus CH1, an obligate piezophilic 14 8 hyperthermophile: extending the upper pressure temperature limits for life. ISME J 15 9 3:873–876. doi: 10.1038/ismej.2009.21 16 17 10 Zeng X, Zhang X, Jiang L, et al. (2012) Palaeococcus pacificus sp. nov., a novel archaeon 18 For Peer Review 19 11 from a deep sea hydrothermal sediment. Int J Syst Evol Microbiol 63:2155 2159 . doi: 20 12 10.1099/ijs.0.044487 0 21 22 13 Zeng X, Zhang Z, Li X, et al. (2015) . Anoxybacter fermentans gen. nov., sp. nov., a 23 14 piezophilic, thermophilic, anaerobic, fermentative bacterium isolated from a deep sea 24 15 hydrothermal vent. Int J Syst Evol Microbiol 65:710 715 25 26 16 Zhao W, Zeng X, Xiao X (2015) Thermococcus eurythermalis sp. nov., a conditional 27 17 piezophilic, hyperthermophilic archaeon with a wide temperature range for growth, 28 29 18 isolated from an oil immersed chimney in the Guaymas Basin. Int J Syst Evol Microbiol 30 19 65:30 35 31 32 20 Zobell CE, Johnson FH (1949) the Influence of Hydrostatic Pressure on the Growth and 33 21 Viability of Terrestrial and Marine Bacteria. J Bacteriol 57:179–89. 34 35 22 36 37 23 38 39 40 24 41 42 25 43 44 26 45 46 27 47 48 49 28 50 51 29 52 53 30 54 55 31 56 57 58 32 59 60 35 Extremophiles Page 36 of 82
1 2 3 1 4 5 2 6 7 3 8 9 10 4 11 12 5 Figure legends 13 14 6 Figure 1. Global map of hydrothermal vents identified so far according to data compiled in 15 16 7 Interridge vents database ( http://vents data.interridge.org/maps ) (Beaulieu, S.E., 2013, 17 18 8 InterRidge Global For Database ofPeer Active Submarine Review Hydrothermal Vent Fields: prepared for 19 20 21 9 InterRidge, Version 3.1. World Wide Web electronic publication. Version 3.2 accessed 2015 22 23 10 02 11, http://vents data.interridge.org ") 24 25 11 26 27 12 Figure 2 : illustration showing mixing between the hot hydrothermal fluid enriched in 28 29 30 13 dissolved reduced gas as H 2, CH 4 H2S, CO, CO 2 and metals etc (electron donors) and cold 31 2 32 14 seawater that contains O2, SO 4 and NO 3 (electron acceptors) that constitutes the basis of 33 34 15 “bacterial chemosynthesis” occurring in deep sea vents. Photograph of a chimney from 35 36 16 Rainbow location (Mid Atlantic Ridge) reproduced with the permission from Ifremer ©. 37 38 17 39 40 18 41 42 19 43 44 20 Figure 3 : Homeoviscous adaptation in Archaea . (A) In its functional state the membrane is 45 46 21 in the liquid crystalline state. Upon an increase in temperature or a decrease in hydrostatic 47 48 22 pressure, the lipid motion increases and the membrane enters the fluid phase. Conversely, 49 50 51 23 when temperature drops or hydrostatic pressure increase, the lipid molecules pack more 52 53 24 tightly and enter a gel phase. Membranes in both gel phase and fluid phase, have impaired 54 55 25 membrane function. (B) Known membrane lipid composition adaptive mechanisms in 56 57 26 Archaea. 58 59 60 36 Page 37 of 82 Extremophiles
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 For Peer Review 19 20 21 22 23 24 25 26 27 28 29 30 Figure 1. Global map of hydrothermal vents identified so far according to data compiled in Interridge vents database (http://vents-data.interridge.org/maps) (Beaulieu, S.E., 2013, InterRidge Global Database of 31 Active Submarine Hydrothermal Vent Fields: prepared for InterRidge, Version 3.1. World Wide Web 32 electronic publication. Version 3.2 accessed 2015-02-11, http://vents-data.interridge.org") 33 223x149mm (300 x 300 DPI) 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Extremophiles Page 38 of 82
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 For Peer Review 19 20 21 22 23 24 25 26 27 28 29 30 31 32 Figure 2 : illustration showing mixing between the hot hydrothermal fluid enriched in dissolved reduced gas 33 as H2, CH4 H2S, CO, CO2 and metals etc (electron donors) and cold seawater that contains O2, SO4-2 and 34 NO3- (electron acceptors) that constitutes the basis of “bacterial chemosynthesis” occurring in deep sea 35 vents. Photograph of a chimney from Rainbow location (Mid Atlantic Ridge) reproduced with the permission 36 from Ifremer©. 37 254x190mm (96 x 96 DPI) 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Page 39 of 82 Extremophiles
1 2 3 4 5 6 7 8 9 10 11 A 12 T T 13 P P 14 15 16 17 18 gel phase Liquid crystalline state Fluid phase 19 functional phase 20 compact lipid layer For Peer Review disordered membrane 21 increased rigidity increased uidity 22 reduced permeability increased permeability 23 reduced lipid motion increased lipid motion 24 25 26 B 27 28 T or pH T or P 29 R O 2 30 O O O 31 O O O O 32 P O R1 P 33 R 1 Increased packing Cross-linking of 34 Incorporation of Decreased permeability Increased stability isoprenoid chains 35 cyclopentane rings Decreased permeability 36 O O 37 R2 O O 38 O O O O 39 P P R O 40 1 R1 41 42 T T or pH P
43 R1
P O
44 O O O O
45 O O P 46 O R1 O 47 P Decreased packing R1 Increased packing Incorporation of 48 Increase of the proportion Increased uidity Increased stability unsaturation of tetra ether lipids Increased permeability 49 Decreased permeability
50 R 2 O O 51 O O O 52 O O O 53 O P P R1 54 R1 55 56 57 58 59 60 Extremophiles Page 40 of 82
1 2 3 4 5 6 Table 1. List of known cultured piezotolerant and piezophilic prokaryotes Maximal T P Pressure GenBank genome sequence 7 Isolate opt opt growth rate Isolation source (depth [m]) Metabolism Reference(s) (°C) (MPa) range (MPa) accession number 8 (h−1 ) Domain: Bacteria 9 Phylum : Actinobacteria Class Actinobacteria 10 Order Actinomycetales 11 Family Dermacoccaceae Dermacoccus abyssi MT1.1T 28 40 nd nd Mariana Trench, sediment (10,898) chemoorganoheterotroph Pathom aree et al., 2006 12 Phylum : Firmicutes 13 Class : Bacilli Order Lactobacillales For Peer Review 14 Family Carnobacteriaceae Carnobacterium sp. strain AT12 2 20 0.1 60 Alaska, Aleoutiennes Trench (2550) chemoorganoheterotroph Lauro et al, 2007 15 Carnobacterium sp. strain AT7 20 20 0.75 0.1 60 Central Indian Ridge, black smoker fluid (2,415–2,460) ABHH01000000 chemoorganoheterotroph Lauro et al, 2007 Class : Clostridia 16 Order to be established 17 Novel family to be established Anoxybacter fermentans DY22613T 60 62 20 2.22 0.1 60 deep sea hydrothermal sulfide deposit at the East Pacific Rise (2,891) chemoorganoheterotroph Zeng et al., 2015 18 Phylum : Proteobacteria Class: Alphaproteobacteria 19 Alphaproteobacterium without standing nomenclature 20 Piezobacter thermophilus 108 50 35 0.46 0.1 65 Mid Atlantic Ridge, black smoker chimney (3,626) facultative chemoautotroph Takai et al., 2009 Order Rhodobacterales 21 Family Rhodobacteraceae Rhodobacterales bacterium PRT1 10 80 0.019 20 100 Puerto Rico Trench, seawater (8,350) chemooligoorganotroph Eloe et al., 2011 22 Class: Deltaproteobacteria 23 Order Desulfovibrionales Family Desulfovibrionaceae 24 Desulfovibrio profundus 500 1T 25 10 40 nd 0.1 40 Japan Sea, sediment core 518 mbsfb (900) chemoorganoheterotroph Bale et al., 1997 25 Desulfovibrio hydrothermalis AM13T 35 26 0.05 nd East Pacific Rise, hydrothermal vent chimney (2,600) FO203522 chemoorganoheterotroph Alazard et al., 2003 Desulfovibrio piezophilus C1TLV30T 30 10 0.01 0.1 30 Wood falls in the Mediterranean Sea (1,693) FO203427 chemoorganoheterotroph Khelaifia et al., 2011 26 Class: Gammaproteobacteria 27 Order Alteromonadales Family Colwelliaceae 28 Colwellia piezophila Y223GT 10 60 0.14 0.1 80 Japan Trench, sediment (6,278) NZ_ARKQ00000000 chemoorganoheterotroph Nogi et al., 2004 29 Colwellia piezophila Y251ET 10 60 nd 0.1 80 Japan Trench, sediment (6,278) chemoorganoheterotroph Nogi et al., 2004 Colwellia hadaliensis BNL 1T 10 90 0.12 37 102 Puerto Rico Trench (7,410) chemoorganoheterotroph Deming et al., 1988 30 Colwellia sp. strain MT41 8 69 0.07 38 103 Mariana Trench, decaying amphipod (10,476) GCA_000712155.1 chemoorganoheterotroph Yayanos et al., 1981 31 Family Psychromonadaceae Psychromonas profunda 2825T 10 25 0.15 0.1 50 Atlantic Ocean sediment (2,770) chemoorganoheterotroph Xu et al., 2003 32 Psychromonas kaikoae JT7304T 10 50 0.15 0.1 70 Japan Trench, cold seep sediment (7,434) chemoorganoheterotroph Nogi et al., 2002 33 Psychromonas sp. strain CNPT3 12 52 0.19 0.1 85 Central North Pacific, decaying amphipod (5,800) CP004404 chemoorganoheterotroph Yayanos et al., 1979 Psychromonas hadalis K41GT 6 60 0.14 0.1 90 Japan Trench, sediment (7,542) NZ_ATUO00000000 chemoorganoheterotroph Nogi et al, 2007 34 Family Moritellaceae 35 Moritella profunda 2674T 6 30 0.17 0.1 50 Atlantic Ocean, sediment (2,815) chemoorganoheterotroph Xu et al, 2003 Moritella abyssi 2693T 10 30 0.20 0.1 50 Atlantic Ocean, sediment (2,815) chemoorganoheterotroph Xu et al, 2003 36 Moritella sp. strain PE36 10 41 0.28 0.1 70 Pacific Ocean, amphipod trap water (3,584) ABCQ00000000 chemoorganoheterotroph Yayanos et al., 1986 Moritella japonica DSK1 15 50 0.4 0.1 70 Japan Trench, sediment (6,356) chemoorganoheterotroph Kato et al., 1995 37 Moritella yayanosii DB21MT 5 10 80 0.2 60 100 Mariana Trench, sediment (10,898) chemoorganoheterotroph Nogi et Kato, 1999 38 Family Shewanellaceae Shewanella piezotolerans WP2 15 20 15 0.5 0.1 50 West Pacific, sediment (1,914) NC_011566 chemoorganoheterotroph Xiao et al., 2007 39 Shewanella piezotolerans WP3 15 20 20 0.5 0.1 50 West Pacific, sediment (1,914) NC_011566 chemoorganoheterotroph Xiao et al., 2007 40 Shewanella profunda LT13a 25 30 10 1.33 0.1 50 Pacific Ocean Nankai Trough, sediment (4,790 ) chemoorganoheterotroph Toffin et al., 2004 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Page 41 of 82 Extremophiles
1 2 3 4
5 Shewanella violacea DSS12 10 30 0.28 0.1 70 Ryukyu Trench, sediment (5,110) NC_014012 chemoorganoheterotroph Kato et al., 1995 6 Shewanella benthica F1A 8 30 0.15 0.1 70 Atlantic Ocean, water column (4,900) chemoorganoheterotroph Wirsen et al., 1986 Shewanella benthica DB6101 10 50 0.35 0.1 70 Ryukyu Trench sediment (5,110) chemoorganoheterotroph Kato et al, 1995 7 Shewanella benthica DB5501 15 60 0.35 0.1 70 Suruga Bay, sediment (2,485) chemoorganoheterotroph Kato et al., 1995 Shewanella benthica DB6705 15 60 0.4 0.1 70 Japan Trench, sediment (6,356) chemoorganoheterotroph Kato et al., 1995 8 Shewanella benthica DB6906 15 60 0.35 0.1 70 Japan Trench, sediment (6,269) chemoorganoheterotroph Kato et al., 1995 9 Shewanella benthica DB172R 10 60 0.45 0.1 70 Izu Bonin Trench, sediment (6,499) chemoorganoheterotroph Kato et al., 1996 Shewanella benthica DB172F 10 70 0.41 50 100 Izu Bonin Trench, sediment (6,499) chemoorganoheterotroph Kato et al., 1996 10 Shewanella benthica DB21MT 2 10 70 0.17 60 100 Mariana Trench sediment (10,898) chemoorganoheterotroph Kato et al., 1998 Shewanella benthica KT99 2 98 40 140 Kermadec Trench, amphipod homogenate (9,856) ABIC00000000 chemoorganoheterotroph Lauro et al., 2007 11 Order Chromatiales Family Thioalkalispiraceae 12 Thioprofundum lithotrophica 106 50 15 0.3 0.1 50 Mid Atlantic Ridge, black smoker chimney (3,626) chemolithoautotrophic Takai et al., 2009 13 Order Oceanospirillales Family Oceanospirillaceae For Peer Review 14 Profundimonas piezophila YC 1 8 50 0.017 20 70 Puerto Rico Trench, water column (6,000) chemoorganoheterotroph Cao et al., 2014 Order "Vibrionales" 15 Family Vibrionaceae Nogi et al., 1998 16 Photobacterium profundum DSJ4 10 10 0.45 0.1 70 Ryukyu Trench, sediment (5,110) chemoorganoheterotroph De Long et al., 1998 Photobacterium profundum SS9 15 28 0.5 0.1 70 Sulu Trough, amphipod homogenate (2,551) NC_006370, NC_006371 chemoorganoheterotroph 17 Phylum : Thermotogae Class Thermotogae 18 Order Thermotogales 19 Family Thermotogaceae Thermosipho japonicus IHB1T 72 20 1.33 0.1 60 Okinawa, Iheya (972) chemoorganoheterotroph Takai and Horikoshi, 2000 20 Marinitoga piezophila KA3T 65 40 1.9 0.1 60 East Pacific Rise, hydrothermal vent (2,630) CP003257 chemoorganoheterotroph Alain et al., 2002 21 Domain : Archaea Phylum : Euryarchaeota 22 Class Methanococci 23 Order Methanococcales Family Methanocaldococcaceae 24 Methanocaldococcus jannaschii JAL 1T 86 75 2.36 0.1 75 East Pacific Rise, hydrothermal vent (2,610) NC_000909 methanogenesis Jones et al., 1983 Family Methanococcaceae 25 Methanococcus thermolithotrophicus 65 50 0.58 0.1 100 Italy, geothermally heated sediments (0.5) NZ_AQXV01000000 methanogenesis Bernhardt et al., 2007 26 Class Methanopyri Order Methanopyrales 27 Family Methanopyraceae Methanopyrus kandleri 116 105 20 0.73 0.1 50 Aleutian Trench, water column (2,500) NC_003551 methanogenesis Takai et al., 2008 28 Class Thermococci 29 Order Thermococcales Family Thermococcaceae 30 Palaeococcus ferrophilus DMJT 83 30 0.5 0.1 60 The Myojin Knoll in the Ogasawara Bonin Arc, Japan (1,338) Ongoing chemoorganoheterotroph Takai et al., 2000 31 Palaeococcus pacificus DY20341T 80 30 0.91 0.1 80 East Pacific Ocean hydrothermal field (2,737) CP006019 chemoorganoheterotroph Zeng et al., 2013 Pyrococcus abyssi GE5 96 20 0.98 0.1 50 Fiji Basin, hydrothermal vent (2,000) NC_000868 chemoorganoheterotroph Erauso et al., 1993 32 Pyrococcus yayanosii CH1T 98 52 1.2 20 120 Mid Atlantic Ridge, hydrothermal vent (4,100) NC_015680 chemoorganoheterotroph Zeng et al, 2009 33 Thermococcus aggregans TYT 75 20 0.1 30 Guaymas bassin (2,000) chemoorganoheterotroph Canganella et al., 2000 Thermococcus guaymasensis TYST 85 20 35 0.1 50 Guaymas bassin (2,000) chemoorganoheterotroph Canganella et al., 1998 34 Thermococcus peptonophilus DSM 10343T 90 45 0.1 60 Back arc Bonin, Izu (1,380) chemoorganoheterotroph Canganella et al., 1997 35 Thermococcus eurythermalis A501T 85 0.1 30 1.25 0.1 70 an oil immersed hydrothermal chimney, Guaymas Basin (2,000) CP008887, CP008888 chemoorganoheterotroph Zhao et al., 2015 Thermococcus barophilus MPT 85 40 1.5 0.1 80 Mid Atlantic Ridge, hydrothermal vent chimney (3,550) CP002372, CP002373 chemoorganoheterotroph Marteinsson et al., 1999 36 n.d. not determined 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Extremophiles Page 42 of 82
1 2 Rapport sur la compatibilité concernant Classeur1list 3 piezophiles.xls 4 Exécuté le 30/07/2014 18:26 5 6 Les fonctionnalités suivantes de ce classeur ne sont pas 7 prises en charge dans les versions antérieures d’Excel. Ces 8 fonctionnalités seront peut-être perdues ou dégradées si vous 9 ouvrez le classeur dans une version antérieure du 10 programme ou si vous l’enregistrez dans un format de fichier 11 antérieur. 12 13 Perte mineure de fidélité Nb Version 14 15 d'occurrence 16 s 17 18 Certaines cellules ou certainsFor styles de cePeer classeur Review4 Excel 97-2003 19 contiennent une mise en forme qui n'est pas prise en charge 20 par le format de fichier sélectionné. Ces formats seront 21 convertis au format le plus proche disponible. 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Page 43 of 82 Extremophiles
1 2 3 Subject: Manuscript ID EXT-15-Feb-0030 revised version 4 5 Dear Editor, 6 7 We would first like to thank you and the two reviewers for the time you spent reviewing this review 8 article, your comments, criticisms and suggestions are all relevant and we have taken into account to 9 improve the quality and the message of this review and we have prepared a new version of the 10 11 manuscript that we hope will be now desirable for publication in Extremophiles Journal. 12 13 Reviewer(s)' Comments to Author: 14 15 Reviewer: 1 16 17 Comments to the Author 18 For Peer Review 19 This paper is almost good enough for publication in extremophiles, no detail revition are needed this 20 moment. But adding following work would be beneficial before formal publication 21 22 Thank you for your positive comments! 23 24 1 This paper lookes like two seperated parts,The first part is about isolates from hydrothermal vent 25 aera, the second part is about high pressure adaptation,These two parts need a better connection. 26 27 Thank you for this appropriate remark! we have made our best to meet your expectation, to answer 28 29 to your inquiries and to provide new information that was added in the revised version of the 30 manuscript (see p. 9, lines 12-25 and p. 10, lines 1-10) 31 32 2 Recent publication about Thermococcus eurythermalis A501 could be list. 33 34 This information was included in the text (p. 9, line 23) and in the table 1 35 36 3 The authors mentioned that Prokaryotes inhabiting in the deep sea vent ecosystem will thus 37 experience waves of temperature, pH, salinity or high hydrostatic pressure (HHP) stress, how these 38 39 strains adapted to multiple stresses could be discuss in more detail, 40 41 This point is well documented in many other reviews on some bacterial and archaeal models and 42 some mechanisms were commonly evolved by prokaryotes to face multiple stress situations like the 43 accumulation of compatible solutes, the scavenging of reactive species (ROS) or the modulation of 44 unsaturation or cyclic lipids in membrane to adapt membrane fluidity, etc… 45 46 especially why hyperthermophilic piezophilic archaea have optimal growth pressure higher than their 47 48 sampling sites depth? 49 50 For hyperthermophiles piezophiles, their optimal growth pressure is obviously higher than the 51 pressure occurring in their sampling sites; this is might be an indication of their origin from deeper 52 sites than where they were sampled as was published by Deming and Baross, 1993 where they 53 proposed that hydrothermal vents are considered as windows on a deeper biosphere. 54 55 56 Is obligate piezophile really exist or just because they were cultivated under 57 "unconfortable"conditions? for example a piezosentive bacterium could adapted also to HHP 58 59 60 Extremophiles Page 44 of 82
1 2 3 Obligate piezophiles are real and the whole cell machinery was fine-tuned during the evolution to 4 function optimally under HHP. In some studies adaptive laboratory evolution (ALE) experiments were 5 conducted on piezosensitive bacterium E. coli and a derivative strain was isolated that acquired the 6 7 ability to grow at high pressure (pressure non-permissive for the parental strain) (Marietou A. et al., 8 2015). The new strain displayed growth properties and changes in the proportion and regulation of 9 unsaturated fatty acids that indicated the acquisition of multiple piezotolerant properties (Marietou 10 A. et al., 2015). This was also the case for P. yayanosii the only known hyperthermophile obligate 11 12 piezophile, for which a facultatively piezophilic derivative strain was isolated, this means that P. 13 yayanosii has acquired during adaptive laboratory evolution, some properties allowing its 14 metabolism and cell cycle to function properly at atmospheric pressure (Li X. et al., 2015). 15 16 Reviewer: 2 17 18 Comments to the AuthorFor Peer Review 19 20 Good review on pressure induced changes in microorganisms inhabiting hydrothermal vents. 21 22 Thank you for your positive comments! 23 24 The abstract is concise, although the first sentence needs to be re-written. I doubt that there are 25 26 "waves" of pressure, and since the focus is on pressure, this needs to be fixed. 27 28 The correction was done accordingly 29 30 Few grammatical things or missing words etc: 31 32 p 1, l. 12: change reinforce to reinforces 33 34 OK 35 36 p. 1, l. 15: add are before ..still needs to be... 37 38 OK 39 40 p. 3, l. 7-12: vague, could mention that average temperature in the deep ocean is 2-3 degree C, 41 except for hydrothermal vents 42 43 OK 44 45 p. 4, l. 24: revise sentence ...some of which are able to grow at more than 46 47 OK 48 49 p. 5, l. 23: exchange ...recorded and... for ..recorded in 50 51 OK 52 53 p. 6, l. 5-7: revise sentence, hardly understandable 54 55 The correction and modification were done accordingly 56 57 p. 6, l. 18: sulur reduction, sulfate reduction and thiosulfate reduction? 58 59 60 Page 45 of 82 Extremophiles
1 2 3 The correction and modification were done accordingly 4 5 p. 7, l. 1: exchange specific for specifically 6 7 OK 8 9 p. 8. l. 7: Prof. or Professor Yayanos 10 11 OK 12 13 p. 8, l. 24" ultramafic rock in Ashadze? 14 15 Yes, please see the publication by Ondréas H et al., 2012, vol 13, n 1, doi:10.1029/2012GC004433, in 16 Geochemistry Geophysics Geosystems (G 3) “Geological context and vents morphology of the 17 18 ultramafic-hosted AshadzeFor hydrothermal Peer areas (Mid-A Reviewtlantic Ridge 13N)” 19 20 After this the manuscript is a lot more fluid. 21 22 I like te figures showing transitions membranes in different phases. 23 24 Thank you for your kind comment! 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Extremophiles Page 46 of 82
1 2 3 4 5 6 7 1 Microbial diversity and adaptation to high hydrostatic pressure in deep sea 8 9 2 hydrothermal vents prokaryotes 10 3 Mohamed Jebbar 1,2, 3*, Bruno Franzetti 4,5,6, Eric Girard 4,5,6, and Philippe Oger 7 11 12 4 13 14 5 1 Université de Bretagne Occidentale, UMR 6197 Laboratoire de Microbiologie des 15 16 6 Environnements Extrêmes (LM2E), Institut Universitaire Européen de la Mer (IUEM), 17 18 7 rue Dumont d’Urville, 29For 280 Plouzané, Peer France Review 19 20 8 2 CNRS, UMR 6197 Laboratoire de Microbiologie des Environnements Extrêmes 21 22 9 (LM2E), Institut Universitaire Européen de la Mer (IUEM), rue Dumont d’Urville, 29 23 24 10 280 Plouzané, France 25 26 11 3 Ifremer, UMR 6197 Laboratoire de Microbiologie des Environnements Extrêmes 27 28 12 (LM2E), Technopôle Brest Iroise, BP70, 29 280 Plouzané, France 29 4 30 13 Centre National de la Recherche Scientifique, IBS, F 38027 Grenoble, France
31 5 32 14 Université Grenoble Alpes, Institut de Biologie Structurale (IBS), F 38027 Grenoble, 33 34 15 France 35 16 6Commissariat à l'Energie Atomique et aux Energies Alternatives, Direction des 36 37 17 Sciences du Vivant, IBS, F 38027 Grenoble, France 38 39 18 7 CNRS, UMR 5276, Ecole Normale Supérieure de Lyon, Lyon, France 40 41 19 42 43 20 44 45 21 *Corresponding author: 46 22 Prof. Mohamed Jebbar 47 23 Institut Universitaire Européen de la Mer (IUEM) 48 24 Laboratoire de Microbiologie des Environnements Extrêmes (UMR 6197) 49 25 Technopole Brest Iroise 50 26 Rue Dumont d’Urville 51 27 29280 Plouzané 52 28 Phone : +33 298 498 817 53 29 Fax : +33 298 498 705 54 30 e mail : mohamed.jebbar@univ brest.fr 55 31 56 57 1 58 59 60 Page 47 of 82 Extremophiles
1 2 3 4 5 6 7 1 Abstract 8 2 Prokaryotes inhabiting in the deep sea vent ecosystem will thus experience waves harsh 9 10 3 conditions of temperature, pH, salinity or high hydrostatic pressure (HHP) stress. Among the 11 12 4 fifty two piezophilic and piezotolerant prokaryotes isolated so far from different deep sea 13 14 5 environments, only fifteen (four Bacteria and eleven Archaea) that are true 15 16 6 hyper/thermophiles and piezophiles have been isolated from deep sea hydrothermal vents, 17 18 7 these belong mainly to theFor Thermococcales Peer order. Different Review strategies are used by 19 20 8 microorganisms to thrive in deep sea hydrothermal vents in which "extreme" physico 21 22 9 chemical conditions prevail and where non adapted organisms cannot live, or even survive. 23 24 10 HHP is known to impact the structure of several cellular components and functions, such as 25 26 11 membrane fluidity, protein activity and structure. Physically the impact of pressure resembles 27 28 12 aresembles a lowering of temperature, since it reinforce s the structure of certain molecules, 29 30 13 such as membrane lipids, and an increase in temperature, since it will also destabilize other 31 32 14 structures, such as proteins. However, universal molecular signatures of HHP adaptation are 33 34 15 not yet known and are still to be deciphered. 35 16 36 37 17 Key words : deep biosphere, diversity, high hydrostatic pressure, enzymatic function, 38 39 18 molecular adaptation 40 41 19 42 43 20 44 45 21 46 47 22 48 49 23 50 51 24 52 53 25 54 55 56 57 2 58 59 60 Extremophiles Page 48 of 82
1 2 3 4 5 6 7 1 Introduction 8 2 Hydrostatic pressure increases with depth at an approximate rate of 10 MPa (~100 9 10 3 atmospheres/bars) per km in the water column and 30 MPa per km underground (Oger and 11 12 4 Jebbar 2010). The definition of the deep biosphere is conveniently and arbitrarily defined as 13 14 5 applying to water depths of 1000 m or more. Consequently, all environments above 10 MPa 15 16 6 qualify as high hydrostatic pressure (HHP) biotopes. HHP waters account for 88% of the 17 18 7 volume of the oceans, whichFor have an averagePeer depth of 3800Review m, and thus an average 19 20 8 hydrostatic pressure ca. 38 MPa, but reach 110 MPa in the trenches. The average temperature 21 22 9 in the deep ocean is 2 3 degree, except for hydrothermal vents. In contrast, the average 23 24 10 geothermal gradient in the continental system is ca. 25°C km 1. The currently known 25 26 11 temperature limit for life, 122°C (Takai et al. 2008), would thus place the "deep" limit for the 27 28 12 putative continental biosphere at ca. 5 km below ground on average, under maximal pressures 29 30 13 of 150 MPa (Zeng et al. 2009; Oger and Jebbar 2010). 31 32 14 HHP affects chemical equilibria and reaction rates, depending on the reaction ( V) 33 34 15 and activation ( V≠) volumes involved. The behavior of all systems under HHP is governed 35 36 16 by Le Châtelier’s principle, which states that the application of pressure shifts equilibrium 37 38 17 towards the state that occupies the smallest volume. It accelerates a process whose transition 39 40 18 state has a smaller volume than that of the ground state. For example, if the volume of a 41 42 19 protein is smaller in its unfolded form, then this protein will be denatured by the application 43 20 of HHP. Several cellular processes such as RNA synthesis, membrane fluidity, motility, cell 44 45 21 division, nutrient uptake, membrane protein function, protein synthesis and replication are 46 47 22 also impaired by HHP. HHP greater than 200 MPa can kill most microorganisms and is used 48 49 23 as a means to preserve foodstuffs. 50 51 24 52 53 25 54 55 56 57 3 58 59 60 Page 49 of 82 Extremophiles
1 2 3 4 5 6 7 1 The discovery of deep sea hydrothermal vent ecosystems is rather recent in the history 8 2 of biological sciences (Corliss, J. B. and Ballard 1977; Paull et al. 1984; Jannasch and Mottl 9 10 3 1985; Eder et al. 1999). The most significant microbial process taking place at these sites is 11 12 4 "bacterial chemosynthesis", which contrasts with the well known process of photosynthesis. 13 14 5 Both processes involve the biosynthesis of organic carbon compounds from CO 2, with the 15 16 6 source of energy being either chemical oxidations or light, respectively (Jannasch and Mottl 17 18 7 1985). Chemoautotrophic prokaryotesFor will assimilatePeer CO 2 and isReview coupled in some prokaryotes 19 20 8 with chemolithotrophy, which enables them to reduce some inorganic compounds as energy 21 22 9 sources. Due to the mixture between the hot reduced hydrothermal fluids enriched in 23 24 10 dissolved gas (H 2S, H 2, CH 4, CO/CO 2) and metals (Fe, Mn) and the cold oxidized sea water 25 26 11 containing sulfates and nitrates, a wide variety of electron donors and acceptors are available 27 28 12 to supply different microbial metabolisms. 29 30 13 Most of the Earth’s prokaryotes live in deep biosphere environments under HHP.
31 28 32 14 From global estimates of volume, the upper 200 m of the ocean contains a total of 3.6 10
33 27 34 15 prokaryotic cells of which 2.9 10 cells are autotrophs; whereas the ocean water below 200 m 35 16 contains 6.5 10 28 prokaryotic cells (Whitman et al. 1998). A recent study has estimated the 36 37 17 total cell abundance in subseafloor sediment at 2.9 10 29 , which is 92% lower than the previous 38 39 18 standard estimate (35.5 ×10 29 ) (Whitman et al. 1998; Kallmeyer et al. 2012). Thus, even 40 41 19 though the maximal productivity of the high pressure continental or marine biosphere is 42 43 20 orders of magnitude lower than that of surface biotopes due to their extremely large volume, 44 45 21 these high pressure biotopes contribute significantly to the production and recycling of 46 47 22 organic carbon. 48 49 23 In less than 30 years, microbiologists have isolated and described many new microbial 50 51 24 species involved in most major biogeochemical cycles and some of which are able for some 52 53 25 to grow at more than 110°C and 150 MPa. Psychrophiles, mesophiles, hyper/thermophiles, 54 55 56 57 4 58 59 60 Extremophiles Page 50 of 82
1 2 3 4 5 6 7 1 acidophiles, piezophiles and even moderate halophiles were isolated from samples originating 8 2 from deep sea hydrothermal vents constituting cultivable representatives of at least 20 phyla, 9 10 3 89 genus and 175 species. This represents a little more than 1% of ∼12,391 prokaryotic 11 12 4 cultured type species (451 Archaea and 11,940 Bacteria) (http://www.bacterio.net/ 13 14 5 number.html#notea) whose taxonomy has been well described (Euzéby 2013). These species 15 16 6 belong to 35 different phyla (30 bacterial phyla and 5 archaeal phyla). The latest molecular 17 18 7 biology techniques allow us toFor see that the Peer cultured and described Review species represent only 19 20 8 ∼1‒2% of the Earth’s Bacteria and Archaea according to the SILVA database 21 22 9 (http://www.arb silva.de), which contains 534,968 of non redundant 16S rRNA sequences 23 24 10 distributed as follows: Bacteria (86.9%), Archaea (3.5%) and Eukarya (9.6%). 25 26 11 This review aims to provide an overview of the diversity of microorganisms thriving 27 28 12 in deep sea hydrothermal vents, their metabolic characteristics and the adaptive mechanisms 29 30 13 they have evolved to cope with HHP. 31 32 14 33 34 15 Deep sea hydrothermal vent ecosystems 35 36 16 Hydrothermalism 37 17 Deep sea hydrothermal vent sites (700 to 5000 m below the ocean surface) are located 38 39 18 in areas of high tectonic activity (Figure 1) such as areas of accretion along mid ocean ridges 40 41 19 (e.g. the mid Atlantic Ridge [MAR] or East Pacific Rise [EPR]), subduction zones, the back 42 43 20 arc basins (e.g. the North Fiji or Lau Basins) and finally hot spot volcanism (e.g. Loihi 44 45 21 Seamount near Hawaii) (Van Dover et al. 2002). According to the InterRidge Global 46 47 22 Database, about 600 active or ancient Submarine Hydrothermal Vent Fields have been 48 49 23 recorded and in more than 200 locations throughout the Pacific, Atlantic, and Indian Oceans 50 51 24 confirmed or inferred (Figure 1), including 46 locations in Indian Ocean (depth from 1500 to 52 53 25 4200 m), 64 locations in the Atlantic Ocean (depth from 800 to 4530 m) and 100 locations in 54 55 56 57 5 58 59 60 Page 51 of 82 Extremophiles
1 2 3 4 5 6 7 1 Pacific Ocean (depth from 850 to 5000 m). The activity of the tectonic plates generates 8 2 seafloor spreading centers (rifts), regions where hot basalt and magma near the sea floor cause 9 10 3 the floor to slowly drift apart. Seawater seeping into these cracked regions mixes with hot 11 12 4 minerals (Edmond et al. 1982) and, under the effect of high pressure, is emitted from the 13 14 5 springs; these underwater hot springs are known as hydrothermal vents. Tthe mineral rich hot 15 16 6 water (270 460°C) forms a cloud of precipitated material upon mixing with will rise to the 17 18 7 surface of the seafloor and canFor reach over 20 Peer m in height, chimneys Review "black smokers" are built 19 20 8 when dissolved minerals and drawn by the groundwater flow in rush back in contact with 21 22 9 oxygenated cold seawater (2‒3°C) , these hydrothermal vents are called black smokers. 23 24 10 Interactions between deep basaltic or ultramafic rocks and sea water brought to high 25 26 11 temperature and high pressure, which therefore has a high solvent power, will produce 27 28 12 hydrothermal fluids. These fluids may reach a temperature as high as 4 600°C, with an acidic 29 30 13 pH. They are anoxic and contain high concentrations of dissolved gases (H 2S, CH 4, CO, CO 2,
31 2+ 2+ + 2+ 32 14 and H 2) and minerals (Mn , Fe , Si , Zn , etc.) (Figure 2) (Jannasch and Mottl 1985; 33 34 15 Johnson et al. 1986; Von Damm 2000; Charlou et al. 2002; Charlou et al. 2010). In contact 35 16 with sea water (cold, oxic with alkaline pH), minerals precipitate and form black smokers. 36 37 17 38 39 18 Metabolic and phylogenetic diversity of deep sea hydrothermal vents 40
41 19 Many Bacteria and Archaea can usereduce sul fph ur, sulfates, thiosulfate, and Iron Formatted: Font: Italic 42 Formatted: Font: Italic 43 20 (III) oxide as electron acceptors in anaerobic respiration and drive metabolisms like sulf ur 44 45 21 respirationoreduction , sulfato respiration and thiosulfat e respirationoreduction , iron 46 47 22 respiration and Anaerobic Oxidation of Methane (AOM) and iron reduction . Fermentative 48 49 23 metabolism is also a principal feature of many archaeal and bacterial species isolated from 50 51 24 deep sea hydrothermal vents (Takai and Nakamura 2011). 52 53 54 55 56 57 6 58 59 60 Extremophiles Page 52 of 82
1 2 3 4 5 6 7 1 Except for some Thaumarchaeota that perform nitrification, oxygen and nitrate are 8 2 used as electrons acceptors by almost all bacteria that specific ally drive metabolisms such as 9 10 3 aerobic respiration, hydrogen oxidation, nitrification, methanotrophy and methylotrophy, 11 12 4 sulfur compound oxidation, iron oxidation, manganese oxidation, denitrification and 13 14 5 Annamox. Some metabolisms like methanogenesis and ammonia oxidation are specifically to 15 16 6 Archaea. The culture independent approach was used to describe the microbial phylogenetic 17 18 7 diversity in active deep sea hydrothermalFor vents Peer from chimney fluidReview sediments and macrofauna 19 20 8 samples. Archaea are associated with hydrothermal edifices, fluids and sediments and 21 22 9 encompass archaeal groups like Thermococcales , Archaeoglobales , Desulfurococcales , 23 24 10 Ignicoccales , Methanococcales and Methanopyrales (Huber et al. 1989; Takai and Horikoshi 25 26 11 1999; Takai et al. 2001; Teske et al. 2002; Schrenk et al. 2004; Nunoura et al. 2010; Roussel 27 28 12 et al. 2011; Takai and Nakamura 2011). Other groups like Halobacteriales , Thaumarchaeota , 29 30 13 DHVE2 and MCG divisions were also detected in these ecosystems (Takai et al. 2001; 31 32 14 Roussel et al. 2011; Orcutt et al. 2011; Flores et al. 2012). 33 34 15 The Bacteria domain is dominated by Epsilonproteobacteria detected in hydrothermal 35 16 fluids, in sea water, hydrothermal sediments, microbial mats and in association with 36 37 17 macrofauna (Reysenbach et al. 2000; Alain et al. 2002b; Reysenbach et al. 2002; Teske et al. 38 39 18 2002; Huber et al. 2003; Page et al. 2004; Suzuki et al. 2005; Campbell et al. 2006; 40 41 19 Gerasimchuk et al. 2010; Crépeau et al. 2011; Sylvan et al. 2012); other bacterial groups were 42 43 20 also detected, such as Alpha , Beta , Delta and Gammaproteobacteria , Aquificales , 44 45 21 Desulfobacteriales , Thermotogales , Deinococcus-Thermus , Deferribacteres , Firmicutes , CFB 46 47 22 (Cytophaga-Flavobacteria-Bacteroidetes ), Acidobacteria , Verrumicrobia and 48 49 23 Planctomycetes (Alain et al. 2002a; Reysenbach et al. 2002; Teske et al. 2002; Huber et al. 50 51 24 2003; Page et al. 2004; Crépeau et al. 2011; Orcutt et al. 2011; Sylvan et al. 2012). More than 52 53 25 one hundred species of Bacteria (17 phyla, 72 genera, 113 species) and Archaea (3 phyla, 17 54 55 56 57 7 58 59 60 Page 53 of 82 Extremophiles
1 2 3 4 5 6 7 1 genera and 62 species) were isolated and cultured from deep sea hydrothermal vents, mainly 8 2 from the Pacific ocean (69‒77% of species) and, in lesser numbers, from the Atlantic 9 10 3 (19‒28% of species) and Indian (2‒4% of species) Oceans. 11 12 4 13 14 5 15 16 6 Knowledge on piezophiles vs other extremophiles from deep sea hydrothermal 17 18 7 vents For Peer Review 19 20 8 The field of piezomicrobiology has been held back by requirements for expensive 21 22 9 high pressure laboratory equipment for sample containment and culture. The first HHP 23 24 10 adapted prokaryotes were bacteria isolated from deep sea sediments in 1949 by ZoBell and 25 26 11 Johnson (Zobell and Johnson 1949). In 1979, the group of Pr ofessor. Yayanos reported the 27 28 12 isolation of the first piezophilic bacterium from the cold deep ocean and two years later 29 30 13 (Yayanos et al. 1981) isolated the first obligate piezophile microorganism, a psychrophilic 31 32 14 bacterium isolated from a decaying amphipod fished from the bottom of the Mariana Trench. 33 34 15 However, although deep sea hydrothermal vent fields were explored at depths ranging 35 16 from 800 to 5000 m, rather few attempts to enrich isolates under in situ pressures have been 36 37 17 carried out. Almost all hyper/thermophilic vent prokaryotes have been isolated under 38 39 18 atmospheric pressure, and few of them have been exposed to HHP. To our knowledge, only a 40 41 19 few microorganisms have been described that are both piezotolerant and piezophilic, these 42 43 20 include representatives from across both Archaea and Bacteria domains: Pyrococcus abyssi Formatted: Font: Italic 44 Formatted: Font: Italic 45 21 (Erauso et al. 1993) Thermococcus barophilus (Marteinsson et al. 1999), Thermococcus 46 47 22 aggregans (Canganella et al., 2000), Thermococcus guaymasensis (Canganella et al., 1998), 48 49 23 Thermococcus peptonophilus (Canganella et al. 1997), Thermococcus eurythermalis (Zhao et Formatted: Font: Italic 50 51 24 al., 2015), Palaeococcus ferrophilus (Takai et al. 2000), Palaeococcus pacificus (Zeng et al. 52 53 25 2012), Methanopyrus kandleri (Takai et al. 2008), Marinitoga piezophila (Alain et al. 2002a), 54 55 56 57 8 58 59 60 Extremophiles Page 54 of 82
1 2 3 4 5 6 7 1 Thermosipho japonicus (Takai and Horikoshi, 2000), Thioprofundum lithotrophica , 8 2 Piezobacter thermophilus (Takai et al. 2009) and Desulfovibrio hydrothermalis (Alazard 9 10 3 2003). The first obligate piezophilic anaerobic hyperthermophilic archaeon discovered was 11 12 4 Pyrococcus yayanosii , isolated from ultramafic a deep sea hydrothermal vent field named 13 14 5 “Ashadze” located on the Mid Atlantic Ridge at 4100 m depth (Zeng et al. 2009; Birrien et al. 15 16 6 2011). P. yayanosii , T. barophilus and M. piezophila were isolated after enrichment cultures 17 18 7 performed under both high temperaturesFor andPeer HHP; they showed Review the highest growth rates 19 20 8 when grown under hydrostatic pressures and their genomes were entirely sequenced and 21 22 9 annotated (Jun et al. 2011; Vannier et al. 2011; Lucas et al. 2012). However, when T. 23 24 10 barophilus and M. piezophila grew under atmospheric pressure, their growth rates were 25 26 11 lower. 27 28 12 Microbes in the deep sea hydrothermal environment face contrasted and fluctuating 29 30 13 environmental conditions, to which they need to adapt or die. Hydrothermal vents are 31 32 14 characterized by large fluctuations in salinity and temperature, from 0.1 to twice the salinity 33 34 15 of seawater (Jannasch and Mottl 1985), and from fluid temperatures as high as 460°C at the 35 16 heart of the vent, to 2°C, the average temperature of the surrounding deep ocean waters (Oger 36 37 17 and Jebbar, 2010). Prokaryotes residing in the vent ecosystem will thus experience situations 38 39 18 of heat, cold, acidic, or salinity stresses. In addition in the deepest parts of the oceans, 40 41 19 hydrothermal vent ecosystems are also submitted to extremely HHP, which is known to 42 43 20 impact the structure of several cellular components and functions, such as membrane fluidity, 44 45 21 protein activity and structure (Oger and Jebbar 2010). Physically the impact of pressure bears 46 47 22 resemblance to both a lowering of temperature, since it will reinforce the structure of certain 48 49 23 molecules, such as membrane lipids, and an increase in temperature, since it will as well 50 51 24 destabilize other structures, such as proteins. These environmental stressors will affect the cell 52 53 25 structure and metabolism. 54 55 56 57 9 58 59 60 Page 55 of 82 Extremophiles
1 2 3 4 5 6 7 1 The hyper/thermophiles piezophiles prokaryotes may have evolved a combination of 8 2 several adaptive mechanisms (compatible solutes accumulation, efficient expression and 9 10 3 activity of prefoldins, membrane fluidity maintaining, robust biocatalysts, etc) to face harsh 11 12 4 and fluctuating conditions prevailing in deep sea hydrothermal vents, thus their cellular 13 14 5 processes such as motility, cell division, nutrient uptake, membrane protein function, protein 15 16 6 synthesis and replication are not or less impaired by HHP such as it was observed in 17 18 7 piezosensitive species E. coli orFor S. cerevisiae .Peer Review Formatted: Font: 12 pt 19 20 8 In the following two sections we will, respectively, address a quick overview of the 21 22 9 main physiological adaptive strategies of vent prokaryotes and molecular adaptations in the 23 24 10 structure of proteins. 25 26 11 27 28 12 Physiology and adaptation 29 30 13 Due to the environmental fluctuations, microorganisms from hydrothermal vents are 31 32 14 expected to show strong osmotic adaptation. In a simplistic way, the effect of salinity and heat 33 34 15 stresses may be reduced to one factor, e.g. the reduced activity of water within or in the 35 16 vicinity of the cells, with a number of consequences, e.g. for the inward or outward fluxes of 36 37 17 cellular salts and the destabilization of the function and structure of cellular components. 38 39 18 Under reduced water activity, proteins fold incorrectly, which reduces or stops protein 40 41 19 activity. We know two strategies of osmoadaptation to high temperature or salinity in hyper 42 43 20 thermophilic prokaryotes isolated from shallow or deep sea hydrothermal vents (da Costa et 44 45 21 al. 1998). Extremely halophilic Archaea and a few halophilic bacteria accumulate K +, Na + 46 47 22 and Cl in response to changes in extracellular salinity (Vreeland 1987; Csonka and Hanson 48 49 23 1991; Galinski and Truper 1994), while a common strategy among microorganisms to cope 50 51 24 with osmotic stress is the accumulation of low molecular mass organic compounds, also 52 53 25 known as compatible solutes because they do not interfere with cellular metabolism (Brown 54 55 56 57 10 58 59 60 Extremophiles Page 56 of 82
1 2 3 4 5 6 7 1 1976; Galinski 1995; Ventosa et al. 1998). Compatible solutes of hyperthermophiles are 8 2 similar to those used by mesophiles, i.e. sugars, amino acids, polyols. In addition, 9 10 3 hyperthermophiles also accumulate solutes little or never encountered in mesophiles such as 11 12 4 mannosylglycerate (MG) (Martins et al. 1997), di myo 1,1' inositol phosphate (DIP) (Martins 13 14 5 et al. 1996), diglycerol phosphate and derivatives of these compounds (da Costa et al. 1998; 15 16 6 Santos and da Costa 2001). These two solutes are essentially restricted to thermophiles 17 18 7 (Santos and da Costa 2002). MGFor is accumulated Peer mostly in response Review to salt stress in Archaea 19 20 8 such as Pyrococcus furiosus , Pyrococcus horikoshii , Thermococcus celer , Thermococcus 21 22 9 stetteri or Thermococcus litoralis and Bacteria such as Thermus thermophilus (Martins and 23 24 10 Santos 1995; Nunes et al. 1995; Lamosa et al. 1998; Empadinhas et al. 2001). In the same 25 26 11 Archaea , DIP is accumulated in response to supra optimal temperature of growth. In the 27 28 12 family Thermococcales , there are three noticeable exceptions to this shared osmolyte 29 30 13 accumulation pattern. First, Thermococcus kodakarensis , which does not seem to accumulate 31 32 14 MG under heat or salt stress; second, Pyrolobus fumarii , which only accumulates DIP as a 33 34 15 response to both stresses (Goncalves et al. 2008); and finally P. ferrophilus , which lacks the 35 16 DIP synthesis genes and accumulates only MG as a response to both stresses. MG is mostly 36 37 17 accumulated in response to high salinity, in amounts above 0.6 µmol/mg protein, in the 38 39 18 genera Palaeococcus (Neves et al. 2005), Pyrococcus (Martins and Santos 1995; Empadinhas 40 41 19 et al. 2001) or Thermococcus (Lamosa et al. 1998). DIP is usually accumulated in response to 42 43 20 high temperatures in amounts above 1 µmol/mg of protein in T. celer (Lamosa et al. 1998) 44 45 21 and P. furiosus (Martins and Santos 1995). Osmolytes, such as MG or DIP, create a protective 46 47 22 shell surrounding the proteins, which helps maintain proper folding and protein functions 48 49 23 (Lamosa et al. 2003). Natural osmolytes increase protein thermal stability in vitro (Santos and 50 51 24 da Costa 2002). In hyperthermophiles, MG has been shown to preserve protein folding 52 53 25 through an increase of protein rigidity (Borges et al. 2002). 54 55 56 57 11 58 59 60 Page 57 of 82 Extremophiles
1 2 3 4 5 6 7 1 In piezophiles, studies devoted to characterizing the role of compatible solutes in 8 9 2 response to HHP have been very limited. Interestingly, P. profundum accumulates β 10 11 3 hydroxybutyrate (both monomers and oligomers) in response to hydrostatic pressure (Martin 12 13 4 et al. 2002), M. piezophila accumulates only amino acids ( α glutamate, proline and alanine) 14 15 5 under atmospheric pressure, but the role of these compatible solutes in adaptation to HHP has 16 6 not been investigated (Lamosa et al. 2013). 17 18 7 As the first and ultimateFor barrier between Peer the intracellular Review space and the outside world, 19 20 8 biological membranes play a fundamental role in the adaptation of microbes to their 21 22 9 environment. The function of the membrane is threefold: 1) to act as a physical barrier to 23 24 10 regulate inward and outward trafficking, 2) to play a central role in energy storage and 25 26 11 processing via ion gradients, and 3) to provide a matrix for environmental sensing, 27 28 12 multicomponent metabolic and signaling pathways and motility. Thus, maintaining optimal 29 30 13 membrane biological function is crucial for any organism. Temperature , pH , salinity or 31 32 14 hydrostatic pressure induced perturbations in membrane organization pose a serious challenge 33 34 15 for the cell. Archaeal and bacterial membranes are very dissimilar in structure, although they 35 36 16 perform identical functions. However, as will be demonstrated below, the mechanisms 37 38 17 employed to adapt to extreme conditions and fluctuating environments are essentially similar. 39 40 18 Bacterial polar lipids, apart from a few rare exceptions, are based on straight chain 41 42 19 hydrocarbons linked by ester bonds on the sn 1 and sn 2 positions of glycerol. Archaeal polar 43 20 lipids are composed of isoprenoid hydrocarbon chains bound by ether bonds to the sn 2 and 44 45 21 sn 3 positions of glycerol (Figure 3). Polar headgroups consist of phosphodiester linked polar 46 47 22 groups or sugar moieties on the sn 1 ( Archaea ) or sn 3 ( Bacteria ) positions of the glycerol 48 49 23 backbone ( sn glycerol 1 phosphate, or G 1 P, structure and sn glycerol 3 phosphate, or G 3 50 51 24 P, structure). 52 53 54 55 56 57 12 58 59 60 Extremophiles Page 58 of 82
1 2 3 4 5 6 7 1 Based on the observation that the membrane lipids of E. coli cells grown under the 8 2 contrasting temperatures of 43°C and 15°C were different (Marr and Ingraham 1962; 9 10 3 Sinensky 1971) while the respective membranes displayed similar physical properties at their 11 12 4 respective growth temperatures, Sinensky modeled the basis of homeoviscous adaptation 13 14 5 (Sinensky 1974; Oger and Cario 2013). This theory states that organisms adapt their 15 16 6 membrane lipid composition to favor the maintenance of the appropriate membrane fluidity 17 18 7 for it to function optimally. ThisFor concept isPeer now understood Review in a broader sense to include 19 20 8 adaptation to proton/water permeability and the dynamic nature of the plasmic membranes 21 22 9 (McElhaney 1984a; McElhaney 1984b; van de Vossenberg et al. 1999; Oger and Cario 2013). 23 24 10 Homeoviscous adaptation must also be understood as a means to rapidly adapt the 25 26 11 composition, and thus the functionality, of the membrane to brutal environmental fluctuations, 27 28 12 or aggressions, including those of heat and cold, salinity, osmotic stress, pressure and pH. 29 30 13 Under normal physiological conditions, membranes are relatively fluid, disordered 31 32 14 liquid crystalline phases. When the temperature drops, or hydrostatic pressure increases, the 33 34 15 membrane lipids may undergo the fluid to gel phase transition. When the temperature 35 16 increases above the physiological conditions, or the pressure decreases from these, the rate of 36 37 17 motion of lipids in the membrane will be increased, this may impact membrane stability and 38 39 18 intrinsic permeability. As can be expected, perturbation in lipid phase state has profound 40 41 19 consequences on membrane structure and function (Lee 2003; Lee 2004). Transition to the gel 42 43 20 phase may induce the clustering of membrane proteins, which appear de facto, excluded from 44 45 21 the zones in the gel phase, reducing the diffusion and the activity of proteins in the membrane 46 47 22 and slowing the flux of transported solutes, but increasing the permeability to cations and 48 49 23 water. 50 51 24 Adaptation of bacterial membrane properties follows four major routes. 1) The 52 53 25 variation of acyl chain length: an increase of the chain length by two carbons increases the 54 55 56 57 13 58 59 60 Page 59 of 82 Extremophiles
1 2 3 4 5 6 7 1 phase transition temperature of the lipid by 10 to 20°C, and decreases membrane permeability 8 2 to proton and water (Winter 2002). 2) The accumulation of unsaturated fatty acids: the 9 10 3 incorporation of a single unsaturation can shift the fluid/gel phase transition by 10 to 20°C 11 12 4 (Russell and Nichols 1999; Winter 2002). 3) The accumulation of specific polar headgroups 13 14 5 such as phosphatidylcholine (PC) or phosphatidylglycerol (PG) in place of 15 16 6 phosphatidylethanolamine (PE). The presence of PC as a polar headgroup results in a drastic 17 18 7 shift of the fluid/gel transition Fortemperature (YanoPeer et al. 1998; WinterReview 2002; Mangelsdorf et al. 19 20 8 2005; Winter and Jeworrek 2009). This is due in part to the reduced hydration and stearic 21 22 9 bulk of the ethanolamine compared to choline, and the capacity of PE, and incapacity of PC, 23 24 10 groups to form hydrogen bonds. 4) The accumulation of branched fatty acid. 25 26 11 Archaeal lipid membranes generally have much lower phase transition temperature 27 28 12 than fatty acyl ester lipids (Yamauchi et al. 1993). Part of the adaptation of the archaeal 29 30 13 membrane to extreme environments may originate from the original structure of its lipids. 31 32 14 While membranes made of fatty acyl ester lipids are in the gel phase or in the liquid 33 34 15 crystalline phase depending mostly on their fatty acid composition, archaeol and 35 16 caldarchaeol based polar lipid membranes of Archaea are assumed to be in the liquid 36 37 17 crystalline phase at a wide temperature range of 0–100°C (Stewart et al. 1990; Dannenmuller 38 39 18 et al. 2000). In addition, most if not all Archaea from the hydrothermal environments 40 41 19 synthesize membrane spanning bipolar tetraether lipids that form monolayers. The monolayer 42 43 20 organization provides extreme rigidity to these membranes. Lateral mobility studies 44 45 21 demonstrate that the lateral diffusion rate at 80°C is comparable between Sulfolobus 46 47 22 acidocaldarius or T. acidphilum and E. coli at 37°C. However, in contrast to bacterial lipids, 48 49 23 which exhibit similar lateral diffusion rates for temperatures close to the phase transition 50 51 24 temperature, in T. acidphilum these values are observed approximately 65°C above the 52 53 25 nominal lipid phase transition temperature (Jarrell et al. 1998). 54 55 56 57 14 58 59 60 Extremophiles Page 60 of 82
1 2 3 4 5 6 7 1 The adaptation of archaeal membrane properties is very similar in its physics to that of 8 2 bacteria, although it takes slightly different routes to converge to the same effects. There exist 9 10 3 several different routes, as follows. 1) The incorporation of cyclopentane rings along the 11 12 4 isoprenoid chain as a function of fluctuating temperature (De Rosa et al. 1980a; De Rosa et al. 13 14 5 1980b; Ernst et al. 1998; Uda et al. 2001; Uda et al. 2004) or pH (Shimada et al. 2008) 15 16 6 increases the packing efficiency of the membrane lipids (Gliozzi et al. 1983), which increases 17 18 7 membrane stability as a functionFor of increasing Peer temperature or salinityReview and decreasing pressure 19 20 8 or pH, and consequently lowers the permeability (Chong et al. 2012). 2) The regulation of the 21 22 9 tetraether to diether lipid ratio (Sprott et al. 1991; Lai et al. 2008; Matsuno et al. 2009): 23 24 10 increase in tetraether lipids will stabilize the membranes by forming monolayer type 25 26 11 membranes or domains in the membrane, helping to regulate the flux of solutes and protons 27 28 12 across the membrane. 3) The crosslinking of the two acyl chains of the lipids to yield 29 30 13 macrocyclic archaeol or caldarchaeol derivatives by a covalent bond between the isoprenoid 31 32 14 chains reduces the motion of the molecule creating a more closely packed structure and 33 34 15 increasing the membrane stability, creating an efficient barrier against water, proton and 35 16 solute leakage (Dannenmuller et al. 2000; Mathai et al. 2001). 4) The increase in unsaturation 36 37 17 along the isoprenoid chains of the lipids as a function of temperature (Nichols et al. 2004) or 38 39 18 salinity (Dawson et al. 2012) has to date only been described in the psychrophilic methanogen 40 41 19 Methanococcoides burtonii (Franzmann et al. 1992; Nichols et al. 2004), but unsaturated 42 43 20 lipids have been characterized in several species of hyperthermophiles (Hafenbradl et al. 44 45 21 1993; Gonthier et al. 2001), which might indicate the occurrence of a similar adaptive strategy 46 47 22 in hydrothermal vent organisms. 48 49 23 Adaptation of bacterial and archaeal membranes to the harsh environment of the 50 51 24 hydrothermal system is clearly visible in the lipids most commonly present. However, 52 53 25 responding to the variations of environmental stressors might only involve a fraction of the 54 55 56 57 15 58 59 60 Page 61 of 82 Extremophiles
1 2 3 4 5 6 7 1 adaptive traits mentioned above. Indeed, in order to be efficient, the membrane composition 8 2 adaptation response needs to be very quick. The routes described require different timeframes. 9 10 3 Thus, certain adaptive mechanisms will prevail over others. For example, the increasing 11 12 4 unsaturation of membrane lipids will decrease the gel/fluid transition temperature to the same 13 14 5 extent as the shortening of one of the acyl chains, or the substitution of a phosphatidylcholine 15 16 6 by a phosphatidylethanolamine polar head, but will be quicker because it is performed inside 17 18 7 the cytoplasmic membrane onFor existing lipids Peer by a membrane Review protein (Kasai et al. 1976; 19 20 8 Cybulski et al. 2002; Aguilar and de Mendoza 2006; Beranova et al. 2008), while the other 21 22 9 actions would need de novo lipid synthesis. 23 24 10 25 26 11 Molecular adaptation of deep sea enzymes 27 28 12 While extremophilic adaptation has been extensively studied for temperature and salt 29 30 13 adapted enzymes, very little is known about pressure adaptation. Pressure induced 31 32 14 modifications of the protein volume may arise from a global elastic compression within 33 34 15 closely related conformational sub states or from promotion of conformational sub states 35 16 presenting lower specific volumes, up to complete unfolding of the protein (Fourme et al. 36 37 17 2006; Akasaka 2006; Akasaka et al. 2013). These modifications originate from changes in the 38 39 18 various interactions between amino acids (hydrogen bond, ionic, van der Waals and 40 41 19 hydrophobic interactions), from changes in the internal voids and cavities found in proteins, 42 43 20 and from changes in the hydration properties (Li et al. 1998; Marchi and Akasaka 2001; 44 45 21 Boonyaratanakornkit et al. 2002; Refaee et al. 2003; Girard et al. 2005; Nisius and Grzesiek 46 47 22 2012). As protein folding, substrate recognition, protein protein interactions and protein 48 49 23 hydration rely upon a combination of these various interactions, pressure may affect all 50 51 24 protein mechanisms through its influence on them (Masson et al. 2004; Occhipinti et al. 2006; 52 53 25 Ohmae et al. 2008; Rosenbaum et al. 2012). 54 55 56 57 16 58 59 60 Extremophiles Page 62 of 82
1 2 3 4 5 6 7 1 Studies that link pressure induced structural modifications to alterations or 8 2 stimulations of biological functions are rare. However, it was shown that, for example, 9 10 3 pressure induces minor changes in the orientation of a chromophore in the protein citrine, 11 12 4 leading to a pressure induced continuous shift of the fluorescence peak (Barstow et al. 2008). 13 14 5 The effect of pressure on the internal solvent excluded void volume has been proposed as a 15 16 6 major contribution to protein activity (Fourme et al. 2006; Girard et al. 2010), but mainly in 17 18 7 protein pressure induced unfoldingFor (Collins Peer et al. 2005; Rouget Review et al. 2011; Roche et al. 19 20 8 2012). Indeed, the role of a hydrophobic cavity, positioned close to the active site pocket, has 21 22 9 been proposed to play a major role in urate oxidase (Girard et al. 2010). Pressure induced an 23 24 10 expansion of the active site pocket correlated with a volume reduction of the hydrophobic 25 26 11 cavity, leading to an inactivation of the protein. It was proposed (Girard et al. 2010) and 27 28 12 confirmed (Marassio et al. 2011) that this particular cavity acts as ballast, providing the 29 30 13 required plasticity of the active site pocket during the urate oxidase catalytic process. A recent 31 32 14 study (Roche et al. 2012) provided evidence that cavities that are present in the folded state 33 34 15 and absent in the unfolded state make a large contribution to the volume difference between 35 16 folded and unfolded states that govern pressure induced unfolding of proteins. Such internal 36 37 17 cavities might also play a role in the pressure dissociation of protein oligomers and aggregates 38 39 18 (Foguel et al. 2003; Girard et al. 2010). 40 41 19 In general, monomeric proteins are quite resistant to high pressure and do not undergo 42 43 20 denaturation under a pressure of 300 MPa (Robb and Clark 1999; Sun et al. 1999), but in 44 45 21 some cases unfolding has been observed at moderate pressure (Gorovits et al. 1995). 46 47 22 Oligomeric proteins can be dissociated by lower pressure than monomeric proteins; 48 49 23 for example, in the GroEl chaperonin complex (14 subunits) from E. coli , dissociation 50 51 24 occurred at 130 MPa (Gorovits et al. 1995), while the RuBisCO from Rhodospirillum rubrum 52 53 25 already started to dissociate at 40 MPa (Erijman et al. 1993). Interestingly, these pressure 54 55 56 57 17 58 59 60 Page 63 of 82 Extremophiles
1 2 3 4 5 6 7 1 values lie within the physiological range of many deep sea organisms. However, the picture is 8 2 more complex than this would make it appear because some oligomeric assemblies have been 9 10 3 described to withstand pressure up to 1 GPa for the dimeric protein, bovine erythrocyte Cu, 11 12 4 Zn superoxide dismutase (Ascone et al. 2010), up to 400 MPa for the cowpea mosaic virus 13 14 5 capsid (Fourme et al. 2002) or up to 300 MPa and 90°C for the 12 subunit TET 15 16 6 aminopeptidase from the archaeon P. horikoshii (Rosenbaum et al. 2012). 17 18 7 The existence of a specificFor molecular Peer adaptation to prolongedReview exposure to pressure 19 20 8 such as the one encountered in the deep sea or in the sediments is suggested by the recent 21 22 9 discovery of obligate piezophilic microbes such as P. yayanosii (Zeng et al. 2009; Birrien et 23 24 10 al. 2011) or Shewanella benthica (Lauro et al. 2013). Moreover, as already mentioned above, 25 26 11 piezophilic strains display a typical cellular stress response when they are grown at 27 28 12 atmospheric pressure. This suggests that a significant part of the proteome is adapted at the 29 30 13 molecular level and, conversely, that the stabilization and enzymatic processes of many 31 32 14 proteins must be adapted to colonize the deeper part of the biosphere. As said before, each 33 34 15 protein will experience pressure differently depending on its specific 3D structure and the 35 16 pressure sensitivity of an organism may be controlled by a limited number of proteins. 36 37 17 Most deep sea organisms are exposed to hydrostatic pressures of 20 to 110 MPa. Due 38 39 18 to the prominent effects of pressure on intermolecular surfaces, it is commonly believed that 40 41 19 large molecular systems are significantly affected in this pressure range. It is apparently the 42 43 20 case, for instance, for the translational activity that is entirely lost when the pressure was up to 44 45 21 90 MPa (Lu et al. 1997). Pressure induced dissociation of ribosomes has been considered a 46 47 22 major cause of the inhibition of bacterial growth in the deep sea. Cell free assays showed that 48 49 23 the post translocational complex represents the most pressure sensitive intermediate of the 50 51 24 elongation cycle and is possibly the limiting factor for the pressure induced block of protein 52 53 25 biosynthesis (Gross et al. 1993). High hydrostatic pressure (HHP) has also been suggested to 54 55 56 57 18 58 59 60 Extremophiles Page 64 of 82
1 2 3 4 5 6 7 1 influence the structure and function of membrane proteins. The effect of hydrostatic pressure 8 2 on mitochondrial H + ATPase revealed that the complex was inactivated in the pressure range 9 10 3 of 60‒180 MPa (Dreyfus et al. 1988). The effect of high hydrostatic pressure was also studied 11 12 4 on the bacterial mechanosensitive channel. In this case, pressure significantly affected channel 13 14 5 kinetics between 0 and 90 MPa. The reduced activity was attributed to a shortening of the 15 16 6 channel openings due to lateral compression of the bilayer under high hydrostatic pressure 17 18 7 (Macdonald and Martinac 2005).For Dimer dissociationPeer of Vibrio Review cholerae ToxR membrane 19 20 8 protein was observed at 20 to 50 MPa in vivo in E. coli reporter strains (Macdonald and 21 22 9 Martinac 2005). These observations indicated that piezophilic adaptation principally targeted 23 24 10 large molecular machines and membrane systems. Accordingly, the volume change upon 25 26 11 Actin polymerization was found to be smaller in the case of a deep sea fish than commonly 27 28 12 measured in surface organisms (Morita 2003). The transcriptional activities and the subunit 29 30 13 dissociations of the RNA polymerases from the piezophile Shewanella violacea and the one 31 32 14 of E. coli were compared and revealed a better resistance of the deep sea machinery after 33 34 15 pressure treatment (Kawano et al. 2004). All these observations suggest that important 35 16 structural modifications occur in large supramolecular assemblies that make it possible to 36 37 17 adapt to a high pressure environment. However, the structure determination of such large 38 39 18 protein complexes is a technical challenge in structural biology that hampers the comparative 40 41 19 structural and biophysical studies of large molecular systems arising from different pressure 42 43 20 environments. 44 45 21 Compared to complex cellular machines, the metabolic enzymes represent tractable 46 47 22 systems to reveal the structural determinants of piezophilicity. For many enzymes, the 48 49 23 biochemistry involves simple substrates and cofactors, and kinetics parameters can be 50 51 24 extracted straightforwardly to assess whether or not the reaction is favoured by high pressure. 52 53 25 It also exists a consistent knowledge for their structure function relationships and, in some 54 55 56 57 19 58 59 60 Page 65 of 82 Extremophiles
1 2 3 4 5 6 7 1 cases, such as the Lactate Malate deshydrogenase family, the molecular determinants for 8 2 thermal or halophilic adaptations have already been explored (Madern et al. 2000; Luke et al. 9 10 3 2007; Sawle and Ghosh 2011). Considering that the stability and the enzymatic properties of 11 12 4 most studied mesophilic proteins do not show important alterations in the pressure range that 13 14 5 is encountered in the deep sea; the existence of a piezophilic adaptation at the enzyme level 15 16 6 remains controversial. However, comparative biochemical studies on enzymes arising from 17 18 7 surfaces and deep sea organismsFor revealed differencePeers indicating Review that catalytic reactions are 19 20 8 more efficient under high pressure for deep sea enzymes. The study of tetrameric lactate 21 22 9 dehydrogenases (LDH) from hagfish living at different depth showed that pressure 23 24 10 inactivation was less pronounced for the abyssal species (Nishiguchi et al. 2008). Several 25 26 11 studies were performed on thermophilic enzymes. They revealed an increase in half life at 27 28 12 high temperature with increasing pressure, thus suggesting that high pressure should be taken 29 30 13 into account in temperature adaptation (Hei and Clark 1994; Sun et al. 1999; Mombelli et al. 31 32 14 2002). However, these studies focused on residual activities and do not allow us to conclude 33 34 15 whether pressure inactivation and thermal stabilization are due to differences in oligomers 35 16 (Hei and Clark 1994) dissociation, unfolding or subtle structural changes, for example at the 36 37 17 active site level. A study on a large aminopeptidase tetrahedral complex (TET) from the deep 38 39 18 sea archaeon P. horikoshii , in which small angle X ray scattering (SAXS) and activity 40 41 19 measurements were performed under high pressure and high temperature, showed that the 12 42 43 20 subunits molecular edifice maintains its quaternary structure up to 300 MPa (Rosenbaum et 44 45 21 al. 2012). This study suggested that large molecular complexes could maintain high pressure 46 47 22 stability far beyond the pressure that the organisms could encounter in the deepest part of the 48 49 23 oceans. Interestingly, the catalytic behaviour of the system was enhanced by pressure. The 50 51 24 determination of the volume changes associated with catalysis indicated a change in the 52 53 25 reaction rate limiting step at 180 MPa. This suggested that pressure adaptation could occur at 54 55 56 57 20 58 59 60 Extremophiles Page 66 of 82
1 2 3 4 5 6 7 1 the active site level in this peptidase family. However, comparative studies on different TET 8 2 peptidases arising from surface and deep sea organisms are essential to draw a conclusion on 9 10 3 this matter. Such comparative studies have been performed on dihydrofolate reductases 11 12 4 (DHFR) from Shewanella species living in deep sea and atmospheric pressure environments 13 14 5 (Ohmae et al. 2012). The stabilities of these enzymes were found to be similar and the 15 16 6 pressure effects did not indicate that the catalytic processes of deep sea DHFR enzymes are 17 18 7 better adapted to high pressureFor environments. Peer However, 3 isopropylmalate Review dehydrogenase 19 20 8 from the obligate piezophile Shewanella benthica DB21MT 2 (SbIPMDH) remains active in 21 22 9 extreme conditions whereas that isolated from the land bacterium S. oneidensis MR 1 23 24 10 (SoIPMDH) becomes inactivated. Comparison of the structures of the two enzymes shows 25 26 11 that SbIPMDH has a larger internal cavity volume than SoIPMDH. This loosely packed 27 28 12 structure of SbIPMDH may limit pressure induced modification of the native structure, 29 30 13 keeping it active at higher pressures compared to SoIPMDH (Nagae et al. 2012). This study 31 32 14 highlighted the potential role of internal cavity in high pressure adaptation. 33 34 15 35 16 Conclusions 36 37 17 Based on the studies described above, a number of mechanisms explaining pressure 38 39 18 resistance and possible adaptation to HHP can be proposed. However, comparative 40 41 19 experimental studies combining enzymology, biophysics, structure and microbiology 42 43 20 approaches performed under high pressure are still essential to make a decisive statement on 44 45 21 the existence of a specific kind of pressure adaptation in deep sea organisms. As already 46 47 22 underlined, proteins are dynamic entities. High pressure adaptive traits might therefore only 48 49 23 be revealed by molecular dynamics studies such as high pressure crystallography or neutron 50 51 24 spectroscopy. Finally, transcriptomic and proteomic studies are vital for revealing the identity 52 53 54 55 56 57 21 58 59 60 Page 67 of 82 Extremophiles
1 2 3 4 5 6 7 1 of the proteins that are mostly impacted by high or low pressure, either to compensate for 8 2 losses of cellular functions or as bona fide key players in pressure adaptation. 9 10 3 At this time it is not yet clear if HHP adaptations require just a change of one or a few 11 12 4 genes in a few pathways, an overall alteration of many genes in a genome, or mainly 13 14 5 regulatory modulations. Several reasons may explain our present inability to identify specific 15 16 6 signatures associated with HHP. First, thus far, only piezosensitive ( E. coli , S. cerevisiae ) or 17 18 7 moderately piezophile strains For( P. profundum Peer strain SS9, Popt Review= 28 MPa) have been studied 19 20 8 extensively. As a consequence, HHP adaptation, if it exists, might not be sufficient to be 21 22 9 demonstrated. Secondly, all results converge to demonstrate a large overlap between cold and 23 24 10 HHP regulation. 25 26 11 The diversity of piezophiles isolated so far from deep sea hydrothermal vents is Formatted: Indent: First line: 0.49" 27 28 12 narrow and consists of prokaryotes driving metabolisms such as sulfatoreduction, 29 30 13 sulforeduction, methanogenesis and fermentation, which does not represent the large 31 32 14 metabolic diversity encountered in these ecosystems. Autochthonous microorganisms of the 33 34 15 deep sea hydrothermal vents are inherently adapted to the extreme conditions of their 35 16 environment, i.e. to the high pressure, low to high temperature, low to high pH, anaerobiosis 36 37 17 to aerobiosis conditions found throughout the deep sea hydrothermal vents. Much more effort 38 39 18 should be put into isolating new and varied piezophiles from deep sea hydrothermal vents, 40 41 19 including i) development of adapted and specialized high pressure equipment to maintain 42 43 20 samples at in situ pressure and temperature once onboard ship, ii) improvement of knowledge 44 45 21 and imagination about geochemistry of their ambient environment, extracellular milieu and 46 47 22 try to recreate viable laboratory conditions, and iii) patience, which has sometimes been 48 49 23 rewarded by very long term incubation of cultures. 50 51 24 52 53 54 55 56 57 22 58 59 60 Extremophiles Page 68 of 82
1 2 3 4 5 6 7 1 Acknowledgments This work was supported by the Agence Nationale de la Recherche 8 2 (ANR 10 BLAN 1725 01 Living deep). We are indebted to Helen McCombie [Bureau de 9 10 3 Traduction de l’Université (BTU), Université de Bretagne Occidentale Brest] for helpful 11 12 4 language improvement. 13 14 5 15 16 6 17 18 7 References For Peer Review 19 20 21 8 Aguilar PS, de Mendoza D (2006) Control of fatty acid desaturation: a mechanism conserved 22 9 from bacteria to humans. Mol Microbiol 62:1507–1514. 23 24 10 Akasaka K (2006) Probing conformational fluctuation of proteins by pressure perturbation. 25 11 Chem Rev 106:1814–35. doi: 10.1021/cr040440z 26 27 12 Akasaka K, Kitahara R, Kamatari YO (2013) Exploring the folding energy landscape with 28 13 pressure. Arch Biochem Biophys 531:110–5. doi: 10.1016/j.abb.2012.11.016 29 30 14 Alain K, Marteinsson VT, Miroshnichenko ML, et al. (2002a) Marinitoga piezophila sp. nov., 31 15 a rod shaped, thermo piezophilic bacterium isolated under high hydrostatic pressure 32 16 from a deep sea hydrothermal vent. Int J Syst Evol Microbiol 52:1331–1339. 33 34 17 Alain K, Olagnon M, Desbruyères D, et al. (2002b) Phylogenetic characterization of the 35 18 bacterial assemblage associated with mucous secretions of the hydrothermal vent 36 19 polychaete Paralvinella palmiformis . FEMS Microbiol Ecol 42:463–476. 37 20 Alazard D (2003) Desulfovibrio hydrothermalis sp. nov., a novel sulfate reducing bacterium 38 21 isolated from hydrothermal vents. Int J Syst Evol Microbiol 53:173–178. doi: 39 22 10.1099/ijs.0.02323 0 40 41 23 Ascone I, Savino C, Kahn R, Fourme R (2010) Flexibility of the Cu,Zn superoxide dismutase 42 24 structure investigated at 0.57 GPa. Acta Crystallogr D Biol Crystallogr 66:654–63. doi: 43 25 10.1107/S0907444910012321 44 45 26 Bale SJ, Goodman K, Rochelle P a, et al. (1997) Desulfovibrio profundus sp. nov., a novel 46 27 barophilic sulfate reducing bacterium from deep sediment layers in the Japan Sea. Int J 47 28 Syst Bacteriol 47:515–21. 48 49 29 Barstow B, Ando N, Kim CU, Gruner SM (2008) Alteration of citrine structure by hydrostatic 50 30 pressure explains the accompanying spectral shift. Proc Natl Acad Sci U S A 51 31 105:13362–6. doi: 10.1073/pnas.0802252105 52 53 54 55 56 57 23 58 59 60 Page 69 of 82 Extremophiles
1 2 3 4 5 6 7 1 Beranova J, Jemiola Rzeminska M, Elhottova D, et al. (2008) Metabolic control of the 8 2 membrane fluidity in Bacillus subtilis during cold adaptation. Biochim Biophys Acta 3 Biomembranes 1778:445–453. 9 10 4 Birrien JL, Zeng X, Jebbar M, et al. (2011) Pyrococcus yayanosii sp. nov., an obligate 11 5 piezophilic hyperthermophilic archaeon isolated from a deep sea hydrothermal vent. Int 12 6 J Syst Evol Microbiol 61:2827–2831. doi: 10.1099/ijs.0.024653 0 13 14 7 Boonyaratanakornkit BB, Park CB, Clark DS (2002) Pressure effects on intra and 15 8 intermolecular interactions within proteins. Biochim Biophys Acta 1595:235–249. 16 17 9 Borges N, Ramos A, Raven NDH, et al. (2002) Comparative study of the thermostabilizing 18 10 properties of mannosylglycerateFor and Peer other compatibl e Review solutes on model enzymes. 19 11 Extremophiles 6:209–216. 20 21 12 Brown AD (1976) Microbial water stress. Bacteriol Rev 40:803–846. 22 23 13 Campbell B, Engel A, Porter M, Takai K (2006) The versatile epsilon proteobacteria: key 24 14 players in sulphidic habitats. Nat Rev Microbio 4:458–468. 25 26 15 Canganella, F., Gambacorta, A., Kato, C., Horikoshi, K., 2000. Effects of hydrostatic pressure 27 16 and temperature on physiological traits of Thermococcus guaymasensis and 28 17 Thermococcus aggregans growing on starch. Microbiological Research 154:297 306 29 30 18 Canganella, F., Gonzalez, J.M., Yanagibayashi, M., Kato, C., Horikoshi, K., 1997. Pressure 31 19 and temperature effects on growth and viability of the hyperthermophilic archaeon 32 20 Thermococcus peptonophilus . Arch. Microbiol. 168:1 7 33 34 21 Canganella, F., Jones, W.J., Gambacorta, A., Antranikian, G., 1998. Thermococcus 35 22 guaymasensis sp. nov. and Thermococcus aggregans sp. nov., two novel thermophilic 36 23 archaea isolated from the Guaymas Basin hydrothermal vent site. International Journal of 37 24 Systematic Bacteriology 48:1181 1185 38 25 Chamieh H, Marty V, Guetta D, et al. (2012) Stress regulation of the PAN proteasome system 39 26 in the extreme halophilic archaeon Halobacterium . Extremophiles 16:215–225. doi: 40 27 10.1007/s00792 011 0421 0 41 42 28 Charlou JL, Donval JP, Fouquet Y, et al. (2002) Geochemistry of high H(2) and CH(4) vent 43 29 fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36 degrees 14 ’ 44 30 N, MAR). Chem Geol 191:345–359. doi: 10.1016/s0009 2541(02)00134 1 45 46 31 Charlou JL, Donval JP, Konn C, et al. (2010) High production of H 2 and CH4 and abiotic 47 32 hydrocarbons in ultramafic hosted hydrothermal systems on the Mid Atlantic Ridge. 48 33 Geochim Cosmochim Acta 74:A163–A163. 49 50 34 Chong PL, Ayesa U, Daswani VP, Hur EC (2012) On physical properties of tetraether lipid 51 35 membranes: effects of cyclopentane rings. Archaea 2012:138439. doi: 52 36 10.1155/2012/138439 53 54 55 56 57 24 58 59 60 Extremophiles Page 70 of 82
1 2 3 4 5 6 7 1 Colletier J P, Aleksandrov A, Coquelle N, et al. (2012) Sampling the conformational energy 8 2 landscape of a hyperthermophilic protein by engineering key substitutions. Mol Biol 3 Evol 29:1683–94. doi: 10.1093/molbev/mss015 9 10 4 Collins MD, Hummer G, Quillin ML, et al. (2005) Cooperative water filling of a nonpolar 11 5 protein cavity observed by high pressure crystallography and simulation. Proc Natl Acad 12 6 Sci U S A 102:16668–71. doi: 10.1073/pnas.0508224102 13 14 7 Coquelle N, Fioravanti E, Weik M, et al. (2007) Activity, stability and structural studies of 15 8 lactate dehydrogenases adapted to extreme thermal environments. J Mol Biol 374:547– 16 9 562. doi: 10.1016/j.jmb.2007.09.049 17 18 10 Coquelle N, Talon R, Juers DH,For et al. (2010) Peer Gradual adaptive Review changes of a protein facing 19 11 high salt concentrations. J Mol Biol 404:493–505. doi: 10.1016/j.jmb.2010.09.055 20 21 12 Da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of 22 13 compatible solutes in Bacteria and Archaea. Adv Biochem Eng Biotechnol 61:117–153. 23 24 14 Crépeau V, Cambon Bonavita, MA Lesongeur F, Randrianalivelo H, et al. (2011) Diversity 25 15 and function in microbial mats from the Lucky Strike hydrothermal vent field. FEBS 26 16 Lett 76:524–540. 27 28 17 Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation Genetics and physiology. Annu 29 18 Rev Microbiol 45:569–606. 30 31 19 Cybulski LE, Albanesi D, Mansilla MC, et al. (2002) Mechanism of membrane fluidity 32 20 optimization: isothermal control of the Bacillus subtilis acyl lipid desaturase. Mol 33 21 Microbiol 45:1379–1388. 34 35 22 Von Damm KL (2000) Chemistry of hydrothermal vent fluids from 9 degrees 10 degrees N, 36 23 East Pacific Rise: “Time zero,” the immediate posteruptive period. J Geophys Res Earth 37 24 105:11203–11222. doi: 10.1029/1999jb900414 38 25 Dannenmuller O, Arakawa K, Eguchi T, et al. (2000) Membrane properties of archaeal 39 26 macrocyclic diether phospholipids. Chemistry (Easton) 6:645–654. 40 41 27 Dawson KS, Freeman KH, Macalady JL (2012) Molecular characterization of core lipids 42 28 from halophilic archaea grown under different salinity conditions. Org Geochem 48:1–8. 43 44 29 Dobson CM (2003) Protein folding and misfolding. Nature 426:884–890. doi: 45 30 10.1038/nature02261 46 47 31 Van Dover CL, German CR, Speer KG, et al. (2002) Evolution and biogeography of deep sea 48 32 vent and seep invertebrates. Science (80 ) 295:1253–1257. doi: 49 33 10.1126/science.1067361 50 51 34 Dreyfus G, Guimaraes Motta H, Silva J (1988) Effect of hydrostatic pressure on the 52 35 mitochondrial ATP synthase. Biochemistry 27:6704–6710. 53 54 55 56 57 25 58 59 60 Page 71 of 82 Extremophiles
1 2 3 4 5 6 7 1 Ebel C, Costenaro L, Pascu M, et al. (2002) Solvent interactions of halophilic malate 8 2 dehydrogenase. Biochemistry 41:13234–13244. 9 3 Edmond JM, Vondamm KL, McDuff RE, Measures CI (1982) Chemistry of hot springs on 10 4 the east pacific rise and their effluent dispersal.. Nature 297:187–191. doi: 11 5 10.1038/297187a0 12 13 6 Empadinhas N, Marugg JD, Borges N, et al. (2001) Pathway for the synthesis of 14 7 mannosylglycerate in the hyperthermophilic archaeon Pyrococcus horikoshii 15 8 Biochemical and genetic characterization of key enzymes. J Biol Chem 276:43580– 16 9 43588. 17 18 10 Erauso G, Reysenbach AL, GodfroyFor A, etPeer al. (1993) Pyrococcus Review abyssi sp nov, a new 19 11 hyperthermophilic archaeon isolated from a deep sea hydrothermal vent. Arch Microbiol 20 12 160:338–349. 21 22 13 Erijman L, Lorimer G, Weber G (1993) Reversible dissociation and conformational stability 23 14 of dimeric ribulose bisphosphate carboxylase. Biochemistry 32:5187–5195. 24 25 15 Ernst M, Freisleben HJ, Antonopoulos E, et al. (1998) Calorimetry of archaeal tetraether lipid 26 16 indication of a novel metastable thermotropic phase in the main phospholipid from 27 17 Thermoplasma acidophilum cultured at 59 degrees C. Chem Phys Lipids 94:1–12. 28 29 18 Euzéby J (2013) List of prokaryotic names with standing in nomenclature. 30 19 http://www.bacterio.net/number.html . Accessed 26 July 2013. 31 32 20 Flores GE, Wagner ID, Liu Y, Reysenbach A L (2012) Distribution, abundance, and diversity 33 21 patterns of the thermoacidophilic “deep sea hydrothermal vent euryarchaeota 2”. Front 34 22 Microbiol 3:47. doi: 10.3389/fmicb.2012.00047 35 36 23 Foguel D, Suarez MC, Ferrão Gonzales AD, et al. (2003) Dissociation of amyloid fibrils of 37 24 alpha synuclein and transthyretin by pressure reveals their reversible nature and the 38 25 formation of water excluded cavities. Proc Natl Acad Sci U S A 100:9831–6. doi: 26 10.1073/pnas.1734009100 39 40 27 Fourme R, Ascone I, Kahn R, et al. (2002) Opening the High Pressure Domain beyond 2 kbar 41 28 to Protein and Virus Crystallography. Structure 10:1409–1414. 42 43 29 Fourme R, Girard E, Kahn R, et al. (2006) High pressure macromolecular crystallography 44 30 (HPMX): status and prospects. Biochim Biophys Acta 1764:384–90. doi: 45 31 10.1016/j.bbapap.2006.01.008 46 47 32 Franzmann PD, Springer N, Ludwig W, et al. (1992) A methanogenic archaeon from Ace 48 33 Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15:573–581. 49 50 34 Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:272–328. 51 52 35 Galinski EA, Truper HG (1994) Microbial behavior in salt stressed ecosystems. FEMS 53 36 Microbiol Rev 15:95–108. 54 55 56 57 26 58 59 60 Extremophiles Page 72 of 82
1 2 3 4 5 6 7 1 Gerasimchuk a. L, Shatalov a. a., Novikov a. L, et al. (2010) The search for sulfate reducing 8 2 bacteria in mat samples from the lost city hydrothermal field by molecular cloning. 3 Microbiology 79:96–105. doi: 10.1134/S0026261710010133 9 10 4 Girard E, Kahn R, Mezouar M, et al. (2005) The first crystal structure of a macromolecular 11 5 assembly under high pressure: CpMV at 330 MPa. Biophys J 88:3562–71. doi: 12 6 10.1529/biophysj.104.058636 13 14 7 Girard E, Marchal S, Perez J, et al. (2010) Structure function perturbation and dissociation of 15 8 tetrameric urate oxidase by high hydrostatic pressure. Biophys J 98:2365–73. doi: 16 9 10.1016/j.bpj.2010.01.058 17 18 10 Gliozzi A, Rolandi R, De RosaFor M, Gambacorta Peer A (1983) Monolayer Review black membranes from 19 11 bipolar lipids of archaebacteria and their temperature induced structural changes. J 20 12 Membr Biol 75:45–56. 21 22 13 Goncalves LG, Lamosa P, Huber R, Santos H (2008) Di myo inositol phosphate and novel 23 14 UDP sugars accumulate in the extreme hyperthermophile Pyrolobus fumarii . 24 15 Extremophiles 12:383–389. doi: 10.1007/s00792 008 0143 0 25 26 16 Gonthier I, Rager MN, Metzger P, et al. (2001) A di O dihydrogeranylgeranyl glycerol from 27 17 Thermococcus S557, a novel ether lipid, and likely intermediate in the biosynthesis of 28 18 diethers in Archaea. Tetrahedron Lett 42:2795–2797. 29 30 19 Gorovits B, Raman C, Horowitz P (1995) High hydrostatic pressure induces the dissociation 31 20 of cpn60 tetradecamers and reveals a plasticity of the monomers. J Biol Chem 270:2061– 32 21 2066. 33 34 22 Gross M, Auerbach G, Jaenicke R (1993) The catalytic activities of monomeric enzymes 35 23 show complex pressure dependence. FEBS Lett 321:256–260. 36 37 24 Hafenbradl D, Keller M, Thiericke R, Stetter KO (1993) A novel unsaturated archael ether 38 25 core lipid from the hyperthermophile Methanopyrus kandleri . Syst Appl Microbiol 26 16:165–169. 39 40 27 Hei DJ, Clark DS (1994) Pressure Stabilization of Proteins from Extreme Thermophiles. Appl 41 28 Env Microbiol 60:932–939. 42 43 29 Huber J, Butterfield D, Baross J (2003) Bacterial diversity in a subseafloor habitat following a 44 30 deep sea volcanic eruption. FEMS Microbiol Ecol 43:393–409. 45 46 31 Huber R, Kurr M, Jannasch K, Stetter K (1989) A novel group of abyssal methanogenic 47 32 archaebacteria ( Methanopyrus ) growing at 110°C. Nature 342:833–834. 48 49 33 Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep sea hydrothermal vents. Science 50 34 (80 ) 229:717–725. doi: 10.1126/science.229.4715.717 51 52 35 Jarrell HC, Zukotynski KA, Sprott GD (1998) Lateral diffusion of the total polar lipids from 53 36 Thermoplasma acidophilum in multilamellar liposomes. Biochim Biophys Acta 54 37 Biomembranes 1369:259–266. 55 56 57 27 58 59 60 Page 73 of 82 Extremophiles
1 2 3 4 5 6 7 1 Johnson K, Beehler C, Sakamoto Arnold C, Childress J (1986) In situ measurements of 8 2 chemical distributions in a deep sea hydrothermal vent field. Science (80 ) 231:1139– 3 1141. 9 10 4 Jun X, Lupeng L, Minjuan X, et al. (2011) Complete genome sequence of the obligate 11 5 piezophilic hyperthermophilic archaeon Pyrococcus yayanosii CH1. J Bacteriol 12 6 193:4297–4298. doi: 10.1128/JB.05345 11 13 14 7 Kallmeyer J, Pockalny R, Adhikari RR, et al. (2012) Global distribution of microbial 15 8 abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109:16213– 16 9 16216. doi: 10.1073/pnas.1203849109 17 18 10 Kasai R, Kitajima Y, Martin For CE, et al. (1976) Peer Molecular controlReview of membrane properties 19 11 during temperature acclimatation Membrane fluidity regulation of fatty acid desaturase 20 12 action. Biochemistry 15:5228–5233. 21 22 13 Kawano H, Nakasone K, Matsumoto M, et al. (2004) Differential pressure resistance in the 23 14 activity of RNA polymerase isolated from Shewanella violacea and Escherichia coli . 24 15 Extremophiles 8:367–375. doi: 10.1007/s00792 004 0397 0 25 26 16 Khelaifia S, Fardeau M L, Pradel N, et al. (2011) Desulfovibrio piezophilus sp. nov., a 27 17 piezophilic, sulfate reducing bacterium isolated from wood falls in the Mediterranean 28 18 Sea. Int J Syst Evol Microbiol 61:2706–11. doi: 10.1099/ijs.0.028670 0 29 30 19 Koga Y (2011) Early evolution of membrane lipids: How did the lipid divide occur? J Mol 31 20 Evol 72:274–282. 32 33 21 Koga Y, Morii H (2007) Biosynthesis of ether type polar lipids in archaea and evolutionary 34 22 considerations. Microbiol Mol Biol Rev 71:97–120. 35 36 23 Koga Y, Morii H (2005) Recent advances in structural research on ether lipids from archaea 37 24 including comparative and physiological aspects. Biosci Biotechnol Biochem 69:2019– 38 25 2034. 39 26 Koutsopoulos S, van der Oost J, Norde W (2005) Temperature dependent structural and 40 27 functional features of a hyperthermostable enzyme using elastic neutron scattering. 41 28 Proteins 61:377–384. 42 43 29 Lai D, Springstead JR, Monbouquette HG (2008) Effect of growth temperature on ether lipid 44 30 biochemistry in Archaeoglobus fulgidus. Extremophiles 12:271–278. 45 46 31 Lamosa P, Martins LO, Da Costa MS, Santos H (1998) Effects of temperature, salinity, and 47 32 medium composition on compatible solute accumulation by Thermococcus spp. Appl 48 33 Env Microbiol 64:3591–3598. 49 50 34 Lamosa P, Rodrigues M V, Gonçalves LG, et al. (2013) Organic solutes in the deepest 51 35 phylogenetic branches of the Bacteria: identification of α(1 6)glucosyl α(1 52 36 2)glucosylglycerate in Persephonella marina . Extremophiles 17:137–46. doi: 53 37 10.1007/s00792 012 0500 x 54 55 56 57 28 58 59 60 Extremophiles Page 74 of 82
1 2 3 4 5 6 7 1 Lamosa P, Turner DL, Ventura R, et al. (2003) Protein stabilization by compatible solutes. 8 2 Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin 3 studied by NMR. Eur J Biochem 270:4606–4614. 9 10 4 Lauro F, Chastain R, Ferriera S, et al. (2013) Draft Genome Sequence of the Deep Sea 11 5 Bacterium Shewanella benthica Strain KT99. Genome Announc 1:pii: e00210–13. doi: 12 6 10.1128/genomeA.00210 13.Copyright 13 14 7 Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. 15 8 Biochim Biophys Acta 1612:1–40. 16 17 9 Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim 18 10 Biophys Acta BiomembranesFor 1666:62–87. Peer Review 19 20 11 Li H, Yamada H, Akasaka K (1998) Effect of Pressure on Individual Hydrogen Bonds in 21 12 Proteins . Basic Pancreatic trypsin inhibitor. Biochemistry 37:1167–1173. 22 23 13 Lu B, Li Q, Liu W, Ruan K (1997) Effects of hydrostatic pressure on the activity of rat 24 14 ribosome and cell free translation system. Biochem Mol Biol Int 43:499–506. 25 26 15 Lucas S, Han J, Lapidus A, et al. (2012) Complete genome sequence of the thermophilic, 27 16 piezophilic, heterotrophic bacterium Marinitoga piezophila KA3. J Bacteriol 194:5974– 28 17 5975. doi: 10.1128/JB.01430 12 29 30 18 Luke KA, Higgins CL, Wittung Stafshede P (2007) Thermodynamic stability and folding of 31 19 proteins from hyperthermophilic organisms. FEBS J 274:4023–4033. doi: 32 20 10.1111/j.1742 4658.2007.05955.x 33 34 21 Macario AJL, Lange M, Ahring BK, et al. (1999) Stress genes and proteins in the archaea. 35 22 Microbiol Mol Biol Rev 63:923–67, table of contents. 36 37 23 Macdonald AG, Martinac B (2005) Effect of high hydrostatic pressure on the bacterial 38 24 mechanosensitive channel MscS. Eur Biophys J 34:434–41. doi: 10.1007/s00249 005 25 0478 8 39 40 26 Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91– 41 27 98. 42 43 28 Mangelsdorf K, Zink KG, Birrien JL, Toffin L (2005) A quantitative assessment of pressure 44 29 dependent adaptive changes in the membrane lipids of piezosensitive deep sub seafloor 45 30 bacterium. Org Geochem 36:1459–1479. 46 47 31 Marassio G, Prangé T, David HN, et al. (2011) Pressure response analysis of anesthetic gases 48 32 xenon and nitrous oxide on urate oxidase: a crystallographic study. FASEB J 25:2266– 49 33 75. doi: 10.1096/fj.11 183046 50 51 34 Marchi M, Akasaka K (2001) Simulation of hydrated BPTI at high pressure : changes in 52 35 hydrogen bonding and its relation with NMR experiments. J Phys Chem B 105:711–714. 53 54 55 56 57 29 58 59 60 Page 75 of 82 Extremophiles
1 2 3 4 5 6 7 1 Marr AG, Ingraham JL (1962) Effect of temperature on the composition of fatty acids in 8 2 Escherichia coli .. J Bacteriol 84:1260–1267. 9 3 Marteinsson VT, Birrien JL, Reysenbach AL, et al. (1999) Thermococcus barophilus sp. nov., 10 4 a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic 11 5 pressure from a deep sea hydrothermal vent. Int J Syst Bacteriol 49 Pt 2:351–359. 12 13 6 Martin DD, Bartlett DH, Roberts MF (2002) Solute accumulation in the deep sea bacterium 14 7 Photobacterium profundum . Extremophiles 6:507–14. doi: 10.1007/s00792 002 0288 1 15 16 8 Martins LO, Carreto LS, DaCosta MS, Santos H (1996) New compatible solutes related to di 17 9 myo inositol phosphate in members of the order Thermotogales. J Bacteriol 178:5644– 18 10 5651. For Peer Review 19 20 11 Martins LO, Huber R, Huber H, et al. (1997) Organic solutes in hyperthermophilic Archaea. 21 12 Appl Environ Microbiol 63:896–902. 22 23 13 Martins LO, Santos H (1995) Accumulation of mannosylglycerate and di myo inosytol 24 14 phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl Environ 25 15 Microbiol 61:3299–3303. 26 27 16 Masson P, Bec N, Froment M T, et al. (2004) Rate determining step of butyrylcholinesterase 28 17 catalyzed hydrolysis of benzoylcholine and benzoylthiocholine. Volumetric study of 29 18 wild type and D70G mutant behavior. Eur J Biochem 271:1980–90. doi: 10.1111/j.1432 30 19 1033.2004.04110.x 31 32 20 Mathai JC, Sprott GD, Zeidel ML (2001) Molecular mechanisms of water and solute transport 33 21 across archaebacterial lipid membranes. J Biol Chem 276:27266–27271. 34 35 22 Matsumi R, Atomi H, Driessen AJM, van der Oost J (2011) Isoprenoid biosynthesis in 36 23 Archaea Biochemical and evolutionary implications. Res Microbiol 162:39–52. 37 38 24 Matsuno Y, Sugai A, Higashibata H, et al. (2009) Effect of growth temperature and growth 25 phase on the lipid composition of the archaeal membrane from Thermococcus 39 26 kodakaraensis . Biosci Biotechnol Biochem 73:104–108. doi: 10.1271/bbb.80520 40 41 27 McElhaney RN (1984a) The structure and function of the Acholeplasma laidlawii plasma 42 28 membrane. Biochim Biophys Acta 779:1–42. 43 44 29 McElhaney RN (1984b) The relationship between membrane fluidity and phase state and the 45 30 ability of bacteria and mycoplasma to grow and survive at various temperatures. In: 46 31 Kates M, Manson LA (eds) Membr. fluidity. Plenum Press, New York, pp 249–276 47 48 32 Mombelli E, Shehi E, Fusi P, Tortora P (2002) Exploring hyperthermophilic proteins under 49 33 pressure: theoretical aspects and experimental findings. Biochim Biophys Acta 25:392– 50 34 396. 51 52 35 Morita T (2003) Structure based analysis of high pressure adaptation of alpha actin. J Biol 53 36 Chem 278:28060–28066. doi: 10.1074/jbc.M302328200 54 55 56 57 30 58 59 60 Extremophiles Page 76 of 82
1 2 3 4 5 6 7 1 Nagae T, Kato C, Watanabe N (2012) Structural analysis of 3 isopropylmalate dehydrogenase 8 2 from the obligate piezophile Shewanella benthica DB21MT 2 and the nonpiezophile 3 Shewanella oneidensis MR 1. Acta Crystallogr Sect F Struct Biol Cryst Commun 9 4 68:265–8. doi: 10.1107/S1744309112001443 10 11 5 Neves C, da Costa MS, Santos H (2005) Compatible solutes of the hyperthermophile 12 6 Palaeococcus ferrophilus : osmoadaptation and thermoadaptation in the order 13 7 thermococcales. Appl Env Microbiol 71:8091–8098. doi: 10.1128/AEM.71.12.8091 14 8 8098.2005 15 16 9 Nichols DS, Miller MR, Davies NW, et al. (2004) Cold adaptation in the antarctic archaeon 17 10 Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186:8508– 18 11 8515. For Peer Review 19 20 12 Nishiguchi Y, Miwa T, Abe F (2008) Pressure adaptive differences in lactate dehydrogenases 21 13 of three hagfishes: Eptatretus burgeri , Paramyxine atami and Eptatretus okinoseanus . 22 14 Extremophiles 12:477–480. doi: 10.1007/s00792 008 0140 3 23 24 15 Nisius L, Grzesiek S (2012) Key stabilizing elements of protein structure identified through 25 16 pressure and temperature perturbation of its hydrogen bond network. Nat Chem 4:711–7. 26 17 doi: 10.1038/nchem.1396 27 28 18 Nunes OC, Manaia CM, Dacosta MS, Santos H (1995) Compatible solutes in the thermophilic 29 19 bacteria Rhodothermus marinus and Thermus thermophilus . Appl Environ Microbiol 30 20 61:2351–2357. 31 32 21 Nunoura T, Oida H, Nakaseama M, et al. (2010) Archaeal diversity and distribution along 33 22 thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV 34 23 hydrothermal field in the Southern Okinawa trough. Appl Env Microbiol 76:1198–1211. 35 24 doi: 10.1128/AEM.00924 09 36 37 25 Occhipinti E, Bec N, Gambirasio B, et al. (2006) Pressure and temperature as tools for 38 26 investigating the role of individual non covalent interactions in enzymatic reactions 27 Sulfolobus solfataricus carboxypeptidase as a model enzyme. Biochim Biophys Acta 39 28 1764:563–72. doi: 10.1016/j.bbapap.2005.12.007 40 41 29 Oger PM, Cario A (2013) Adaptation of the membrane in Archaea. Biophys Chem. doi: 42 30 10.1016/j.bpc.2013.06.020 43 44 31 Oger PM, Jebbar M (2010) The many ways of coping with pressure. Res Microbiol 161:799– 45 32 809. doi: 10.1016/j.resmic.2010.09.017 46 47 33 Ohmae E, Murakami C, Tate S, et al. (2012) Pressure dependence of activity and stability of 48 34 dihydrofolate reductases of the deep sea bacterium Moritella profunda and Escherichia 49 35 coli . Biochim Biophys Acta 1824:511–519. doi: 10.1016/j.bbapap.2012.01.001 50 51 36 Ohmae E, Tatsuta M, Abe F, et al. (2008) Effects of pressure on enzyme function of 52 37 Escherichia coli dihydrofolate reductase. Biochim Biophys Acta 1784:1115–21. doi: 53 38 10.1016/j.bbapap.2008.04.005 54 55 56 57 31 58 59 60 Page 77 of 82 Extremophiles
1 2 3 4 5 6 7 1 Orcutt BN, Bach W, Becker K, et al. (2011) Colonization of subsurface microbial 8 2 observatories deployed in young ocean crust. ISME J 5:692–703. doi: 3 10.1038/ismej.2010.157 9 10 4 Page A, Juniper S, Olagnon M, et al. (2004) Microbial diversity associated with a 11 5 Paralvinella sulfincola tube and the adjacent substratum on an active deep sea vent 12 6 chimney. Geobiology 2:225–238. 13 14 7 Ramos A, Raven NDH, Sharp RJ, et al. (1997) Stabilization of enzymes against thermal stress 15 8 and freeze drying by mannosylglycerate. Appl Environ Microbiol 63:4020–4025. 16 17 9 Refaee M, Tezuka T, Akasaka K, Williamson MP (2003) Pressure dependent Changes in the 18 10 Solution Structure of HenFor Egg white Peer Lysozyme. J MolReview Biol 327:857–865. doi: 19 11 10.1016/S0022 2836(03)00209 2 20 21 12 Reysenbach AL, Gotz D, Banta A, et al. (2002) Expanding the distribution of the Aquificales 22 13 to the deep sea vents on Mid Atlantic ridge and central Indian Ocean ridge. Cah Biol 23 14 Mar 43:425–428. 24 25 15 Reysenbach AL, Longnecker K, Kirshtein J (2000) Novel bacterial and archaeal lineages 26 16 from an in situ growth chamber deployed at a Mid Atlantic Ridge hydrothermal vent. 27 17 Appl Env Microbiol 66:3798–3806. 28 29 18 Robb FT, Clark DS (1999) Adaptation of proteins from hyperthermophiles to high pressure 30 19 and high temperature. J Mol Microbiol Biotechnol 1:101–105. 31 32 20 Roche J, Caro J a, Norberto DR, et al. (2012) Cavities determine the pressure unfolding of 33 21 proteins. Proc Natl Acad Sci U S A 109:6945–50. doi: 10.1073/pnas.1200915109 34 35 22 De Rosa M, Esposito E, Gambacorta A, et al. (1980a) Complex lipids of Caldariella 36 23 acidophila , a thermoacidophile archaebacterium. Phytochemistry 19:821–826. 37 38 24 De Rosa M, Esposito E, Gambacorta A, et al. (1980b) Effects of temperature on ether lipid 25 composition of Caldariella acidophila . Phytochemistry 19:827–831. 39 40 26 Rosenbaum E, Gabel F, Durá MA, et al. (2012) Effects of hydrostatic pressure on the 41 27 quaternary structure and enzymatic activity of a large peptidase complex from 42 28 Pyrococcus horikoshii . Arch Biochem Biophys 517:104–10. doi: 43 29 10.1016/j.abb.2011.07.017 44 45 30 Rouget J B, Aksel T, Roche J, et al. (2011) Size and Sequence and the Volume Change of 46 31 Protein Folding. J Am Chem Soc 133:6020–6027. doi: 10.1021/ja200228w.Size 47 48 32 Roussel EG, Konn C, Charlou JL, et al. (2011) Comparison of microbial communities 49 33 associated with three Atlantic ultramafic hydrothermal systems. FEMS Microbiol Ecol 50 34 77:647–665. doi: 10.1111/j.1574 6941.2011.01161.x 51 52 35 Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria a dogma 53 36 rewritten. Microbiology 145 ( Pt 4:767–779. 54 55 56 57 32 58 59 60 Extremophiles Page 78 of 82
1 2 3 4 5 6 7 1 Santos H, da Costa MS (2001) Organic solutes from thermophiles and hyperthermophiles. 8 2 Methods Enzym 334:302–315. 9 3 Santos H, da Costa MS (2002) Compatible solutes of organisms that live in hot saline 10 4 environments. Env Microbiol 4:501–509. 11 12 5 Sawle L, Ghosh K (2011) How do thermophilic proteins and proteomes withstand high 13 6 temperature? Biophys J 101:217–227. 14 15 7 Schrenk M, Kelley D, Bolton S, Baross J (2004) Low archaeal diversity linked to subseafloor 16 8 geochemical processes at the Lost City Hydrothermal Field, Mid Atlantic Ridge. Env 17 9 Microbiol 6:1086–1095. 18 For Peer Review 19 10 Shimada H, Nemoto N, Shida Y, et al. (2008) Effects of pH and temperature on the 20 11 composition of polar lipids in Thermoplasma acidophilum HO 62. J Bacteriol 190:5404– 21 12 5411. 22 23 13 Sinensky M (1971) Temperature control of phospholipid biosynthesis in Escherichia coli. J 24 14 Bacteriol 106:449–455. 25 26 15 Sinensky M (1974) Homeoviscous adaptation Homerostatic process that regulates viscosity 27 16 of membrane lipids in Escherichia coli . Proc Natl Acad Sci U S A 71:522–525. 28 29 17 Sprott GD, Meloche M, Richards JC (1991) Proportions of diether, macrocyclic diether, and 30 18 tetraether lipids in Methanococcus jannaschii grown at different temperatures. J 31 19 Bacteriol 173:3907–3910. 32 33 20 Stewart LC, Kates M, Ekiel IH, Smith ICP (1990) Molecular order and dynnamics of 34 21 diphytanylglycerol phospholipids A 2H NMR and 31P NMR study. Chem Phys Lipids 35 22 54:115–129. 36 37 23 Sun MM, Tolliday N, Vetriani C, et al. (1999) Pressure induced thermostabilization of 38 24 glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus . Protein Sci 25 8:1056–63. doi: 10.1110/ps.8.5.1056 39 40 26 Suzuki Y, Sasaki T, Suzuki M, et al. (2005) Novel chemoautotrophic endosymbiosis between 41 27 a member of the Epsilonproteobacteria and the hydrothermal vent gastropod 42 28 Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Env 43 29 Microbiol 71:5440–5450. doi: 10.1128/AEM.71.9.5440 5450.2005 44 45 30 Sylvan JB, Pyenson BC, Rouxel O, et al. (2012) Time series analysis of two hydrothermal 46 31 plumes at 9°50’N East Pacific Rise reveals distinct, heterogeneous bacterial populations. 47 32 Geobiology 10:178–192. doi: 10.1111/j.1472 4669.2011.00315.x 48 49 33 Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep sea hydrothermal vent 50 34 environments. Genetics 152:1285–1297. 51 52 35 Takai, K., Horikoshi, K., 2000. Thermosipho japonicus sp. nov., an extremely thermophilic 53 36 bacterium isolated from a deep sea hydrothermal vent in Japan. Extremophiles 4:9 17 54 55 56 57 33 58 59 60 Page 79 of 82 Extremophiles
1 2 3 4 5 6 7 1 Takai K, Komatsu T, Inagaki F, Horikoshi K (2001) Distribution of archaea in a black smoker 8 2 chimney structure. Appl Env Microbiol 67:3618–3629. doi: 10.1128/AEM.67.8.3618 3 3629.2001 9 10 4 Takai K, Miyazaki M, Hirayama H, et al. (2009) Isolation and physiological characterization 11 5 of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep sea 12 6 hydrothermal vent chimney. Env Microbiol 11:1983–1997. doi: 10.1111/j.1462 13 7 2920.2009.01921.x 14 15 8 Takai K, Nakamura K (2011) Archaeal diversity and community development in deep sea 16 9 hydrothermal vents. Curr Opin Microbiol 14:282–291. doi: 10.1016/j.mib.2011.04.013 17 18 10 Takai K, Nakamura K, TokiFor T, et al. (2008)Peer Cell proliferation Review at 122 degrees C and 19 11 isotopically heavy CH4 production by a hyperthermophilic methanogen under high 20 12 pressure cultivation. Proc Natl Acad Sci U S A 105:10949–10954. doi: 21 13 10.1073/pnas.0712334105 22 23 14 Takai K, Sugai A, Itoh T, Horikoshi K (2000) Palaeococcus ferrophilus gen. nov., sp. nov., a 24 15 barophilic, hyperthermophilic archaeon from a deep sea hydrothermal vent chimney. Int 25 16 J Syst Evol Microbiol 50 Pt 2:489–500. 26 27 17 Tehei M, Franzetti B, Madern D, et al. (2004) Adaptation to extreme environments: 28 18 macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO 29 19 Rep 5:66–70. doi: 10.1038/sj.embor.7400049 30 31 20 Tehei M, Madern D, Franzetti B, Zaccai G (2005) Neutron scattering reveals the dynamic 32 21 basis of protein adaptation to extreme temperature. J Biol Chem 280:40974–40979. doi: 33 22 10.1074/jbc.M508417200 34 35 23 Teske A, Hinrichs K, Edgcomb V, et al. (2002) Microbial Diversity of Hydrothermal 36 24 Sediments in the Guaymas Basin : Evidence for Anaerobic Methanotrophic Communities 37 25 †. 68:1994–2007. doi: 10.1128/AEM.68.4.1994 38 26 Uda I, Sugai A, Itoh YH, Itoh T (2001) Variation in molecular species of polar lipids from 39 27 Thermoplasma acidophilum depends on growth temperature. Lipids 36:103–105. 40 41 28 Uda Y, Sugai A, Itoh YH, Itoh T (2004) Variation in molecular species of core lipids from the 42 29 order Thermoplasmales strains depends on the growth temperature. J Oleo Sci 53:399– 43 30 404. 44 45 31 Vannier P, Marteinsson VT, Fridjonsson OH, et al. (2011) Complete genome sequence of the 46 32 hyperthermophilic, piezophilic, heterotrophic, and carboxydotrophic archaeon 47 33 Thermococcus barophilus MP. J Bacteriol 193:1481–1482. doi: 10.1128/JB.01490 10 48 49 34 Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. 50 35 Microbiol Mol Biol Rev 62:504–544. 51 52 36 Van de Vossenberg J, Driessen AJM, da Costa MS, Konings WN (1999) Homeostasis of the 53 37 membrane proton permeability in Bacillus subtilis grown at different temperatures. 54 38 Biochim Biophys Acta Biomembranes 1419:97–104. 55 56 57 34 58 59 60 Extremophiles Page 80 of 82
1 2 3 4 5 6 7 1 Vreeland RH (1987) Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol 8 2 14:311–356. doi: 10.3109/10408418709104443 9 3 Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl 10 4 Acad Sci U S A 95:6578–6583. 11 12 5 Winter R (2002) Effect of lipid chain length, temperature, pressure and composition on the 13 6 lateral organisation and phase behavior of lipid bilayer/gramicidin mixtures. Biophys J 14 7 82:153A–153A. 15 16 8 Winter R, Jeworrek C (2009) Effect of pressure on membranes. Soft Matter 5:3157–3173. 17 18 9 Yamauchi K, Doi K, YoshidaFor Y, Kinoshita PeerM (1993) Archaebacterial Review lipids: highly proton 19 10 impermeable membranes from 1,2 diphytanyl sn glycero 3 phosphocholine. 20 11 BiochimBiophysActa 1146:178–182. 21 22 12 Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting 23 13 cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830. doi: 24 14 10.1242/jeb.01730 25 26 15 Yano Y, Nakayama A, Ishihara K, Saito H (1998) Adaptive changes in membrane lipids of 27 16 barophilic bacteria in response to changes in growth pressure. Appl Env Microbiol 28 17 64:479–485. 29 30 18 Yayanos AA, Dietz AS, Van Boxtel R (1981) Obligately barophilic bacterium from the 31 19 Mariana trench. Proc Natl Acad Sci U S A 78:5212–5215. 32 33 20 Zaccai G (2013) The ecology of protein dynamics. Curr Phys Chem 3:9–16. 34 35 21 Zeng X, Birrien JL, Fouquet Y, et al. (2009) Pyrococcus CH1, an obligate piezophilic 36 22 hyperthermophile: extending the upper pressure temperature limits for life. ISME J 37 23 3:873–876. doi: 10.1038/ismej.2009.21 38 39 24 Zeng X, Zhang X, Jiang L, et al. (2012) Palaeococcus pacificus sp. nov., a novel archaeon 25 from a deep sea hydrothermal sediment. Int J Syst Evol Microbiol 63:2155 2159 . doi: 40 26 10.1099/ijs.0.044487 0 41 42 27 Zeng X, Zhang Z, Li X, et al. (2015) . Anoxybacter fermentans gen. nov., sp. nov., a 43 28 piezophilic, thermophilic, anaerobic, fermentative bacterium isolated from a deep sea 44 29 hydrothermal vent. Int J Syst Evol Microbiol 65:710 715 Formatted: English (U.S.) 45 Formatted: English (U.S.) 46 30 Zhao W, Zeng X, Xiao X (2015) Thermococcus eurythermalis sp. nov., a conditional Field Code Changed 47 31 piezophilic, hyperthermophilic archaeon with a wide temperature range for growth, Formatted: English (U.S.) 48 32 isolated from an oil immersed chimney in the Guaymas Basin. Int J Syst Evol Microbiol Field Code Changed 49 33 65:30 35 Formatted: English (U.S.) 50 Formatted: English (U.S.) 51 34 Zobell CE, Johnson FH (1949) the Influence of Hydrostatic Pressure on the Growth and Formatted: English (U.S.) 52 35 Viability of Terrestrial and Marine Bacteria. J Bacteriol 57:179–89. 53 Formatted: Font: Italic, English (U.S.) 54 36 Formatted: English (U.S.) 55 Field Code Changed 56 57 35 58 59 60 Page 81 of 82 Extremophiles
1 2 3 4 5 6 7 1 8 2 9 10 3 11 12 4 13 14 5 15 16 6 17 18 7 For Peer Review 19 20 8 21 22 9 23 24 10 25 26 11 27 28 12 29 30 13 31 32 14 33 34 15 Figure legends 35 16 Figure 1. Global map of hydrothermal vents identified so far according to data compiled in 36 37 17 Interridge vents database ( http://vents data.interridge.org/maps ) (Beaulieu, S.E., 2013, 38 39 18 InterRidge Global Database of Active Submarine Hydrothermal Vent Fields: prepared for 40 41 19 InterRidge, Version 3.1. World Wide Web electronic publication. Version 3.2 accessed 2015 42 43 20 02 11, http://vents data.interridge.org ") 44 45 21 46 47 22 Figure 2 : illustration showing mixing between the hot hydrothermal fluid enriched in 48 49 23 dissolved reduced gas as H 2, CH 4 H2S, CO, CO 2 and metals etc (electron donors) and cold 50 2 51 24 seawater that contains O2, SO 4 and NO 3 (electron acceptors) that constitutes the basis of 52 53 54 55 56 57 36 58 59 60 Extremophiles Page 82 of 82
1 2 3 4 5 6 7 1 “bacterial chemosynthesis” occurring in deep sea vents. Photograph of a chimney from 8 2 Rainbow location (Mid Atlantic Ridge) reproduced with the permission from Ifremer ©. 9 10 3 11 4 12 13 5 14 15 6 Figure 3 : Homeoviscous adaptation in Archaea. (A) In its functional state the membrane is in 16 17 7 the liquid crystalline state. Upon an increase in temperature or a decrease in hydrostatic 18 For Peer Review 19 8 pressure, the lipid motion increases and the membrane enters the fluid phase. Conversely, 20 21 9 when temperature drops or hydrostatic pressure increase, the lipid molecules pack more 22 23 10 tightly and enter a gel phase. Membranes in both gel phase and fluid phase, have impaired 24 25 11 membrane function. (B) Known membrane lipid composition adaptive mechanisms in 26 27 12 Archaea. 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 37 58 59 60