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For Peer Review 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 : [email protected] 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).
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