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Recent Advances in Halophilic and Thermophilic Extremophiles Research in Microbiology 161 (2010) 506e514 www.elsevier.com/locate/resmic Exploring research frontiers in microbiology: recent advances in halophilic and thermophilic extremophiles Beate Averhoff, Volker Mu¨ller* Molecular Microbiology & Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt, Max-von-Laue-Str. 9, 60438, Frankfurt am Main, Germany Received 25 March 2010; accepted 11 May 2010 Available online 31 May 2010 Abstract Extremophilic prokaryotes inhabit ecosystems that are, from a human perspective, extreme, and life in these environments requires far- reaching cellular adaptations. Here, we will describe, for two examples (Thermus thermophilus, Halobacillus halophilus), how thermophilic or halophilic bacteria adapt to their environment; we will describe the molecular basis of sensing and responding to hypersalinity and we will analyze the impact and basis of natural competence for survival in hot environments. Ó 2010 Elsevier Masson SAS. All rights reserved. Keywords: Compatible solutes; DNA transport; Extremophiles; Halophiles; Natural competence; Thermophiles 1. Introduction from thermal springs in Yellowstone National Park (Brock and Freeze, 1969). This enzyme has made the polymerase chain Extremophilic prokaryotes are characterized by inhabiting reaction possible on a large, automated scale. With this enzyme, ecosystems that are, from a human perspective, extreme. Such sequencing genomes was made possible and it gave rise to the environments may have extremely high or low pH, high or low thousands of genomes that we have today, ranging from nano- temperatures, high salinity, high pressure and various combi- archaea to humans. nations thereof. Extremophilic microorganisms include The community of extremophilic researchers is rather large. members of all three domains of life, the Archaea, Bacteria and There are conferences that deal only with extremophiles; there Eukarya. Often, these microbes are not only challenged by one is an “International Society for Extremophiles”, and there is extreme, but multiple, and thus they are “polyextremophile” even a journal named “Extremophiles”, founded by Koki (Mesbah and Wiegel, 2008). Examples would be life at hot Horikoshi and now led by Garabed Antranikian. Research on alkaline springs or hypersaline and alkaline lakes or hot and extremophiles has been plentiful over the last few decades and acidic springs. Ever since extremophiles were discovered, their is as diverse as the organisms. It started with the isolation of physiology and their adaptation to the unhostile environment extremophiles and continued on by exploring their biochem- have attracted much interest. This was not only because of the istry, then into their genetics and regulation of their metabo- interest in their lifestyle, but also for exploring their biotech- lism. A couple of recent excellent books cover the entire nological potential. The enzyme Taq polymerase is a prime spectrum of extremophiles and describe their lifestyle (Gerday example of an enzyme from an extremophile, Thermus aqua- and Glansdorff, 2007; Garrett and Klenk, 2007; Oren, 2002). ticus, isolated in 1969 by Thomas D. Brock and Hudson Freeze Considering the wealth of information on extremophiles, on the one hand, and the limitation in space for this review, on the * Corresponding author. Tel.: þ49 69 79829509/507; fax: þ49 69 79829306. other, we will restrict ourselves to two examples and apologize E-mail addresses: [email protected] (B. Averhoff), vmueller@ to the readers and the community for not being able to cover bio.uni-frankfurt.de (V. Mu¨ller). the entire spectrum. 0923-2508/$ - see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2010.05.006 B. Averhoff, V. Mu¨ller / Research in Microbiology 161 (2010) 506e514 507 2. The molecular basis of salt adaptation in halophiles a genome-wide scale (Pflu¨ger et al., 2007). 84 genes of different functional categories, such as solute transport and þ Every living cell is challenged by changing water activities biosynthesis, Na export, stress response, ion, protein and in its ecosystem; thus, constant monitoring and adapting to phosphate transport, metabolic enzymes, regulatory proteins, changing water activities is a prerequisite for life. This is of DNA modification systems and cell surface modulators were particular importance for (moderate) halophiles. The biggest found to be more strongly expressed at high salinities. challenge is to adjust the turgor and living cells have devel- Moreover, 10 genes encoding different metabolic functions oped two principal strategies to re-establish turgor pressure including potassium uptake and ATP synthesis were reduced and to circumvent the detrimental consequences of water loss in expression under high salt. The overall expression profiles when exposed to increasing osmolality. On the one hand, there suggest that M. mazei is able to adapt to high salinities by is the “salt-in-cytoplasm”-strategy, which means that inorganic multiple upregulation of many different cellular functions, ions, mainly Kþ and ClÀ, accumulate in the cytoplasm until including protective pathways such as solute transport and the internal salt concentration is similar to the extracellular biosynthesis, import of phosphate, export of Naþ, and upre- one. This strategy is found in extremely halophilic Halobac- gulation of pathways for modification of DNA and cell surface teria (Archaea) and halophilic, anaerobic Haloanaerobiales architecture. Taking this (and other studies) into account, it is (Bacteria)(Galinski and Tru¨per, 1994; Ventosa et al., 1998). obvious that a fine-tuned response to changing salinities On the other hand, the vast majority of prokaryotes cope with requires an elaborate regulatory network that, in addition, also increasing osmolarity by uptake or synthesis of compatible has to talk to other networks. Again, analyses of these solutes, which are defined as small, highly soluble, organic networks have only begun recently and we will describe one molecules which do not interfere with the central metabolism, that we discovered in the moderately halophilic bacterium even if they accumulate at high concentrations (Brown, 1976). Halobacillus halophilus. This strategy is widespread and evolutionarily well conserved in all three domains of life (Bohnert, 1995; Kempf and 2.1. The chloride regulon in the moderate halophile Bremer, 1998; Roeßler and Mu¨ller, 2001b; Saum and H. halophilus Mu¨ller, 2008a). However, the spectrum of compatible solutes used comprises only a limited number of compounds and these The moderately halophilic bacteria are a specialized group can be divided into 2 major groups: 1) sugars and polyols; and of organisms that require NaCl for growth (Ventosa et al., 2) a- and b-amino acids and their derivatives, including 1998). They grow at nearly the same rate over a rather wide methylamines. This limitation to a rather small number of range of external salt concentrations (0.5e2.5 M) which is compounds reflects the fundamental constraints on solutes evidence for effective mechanisms to cope with changing which are compatible with macromolecular and cellular external salinities. The aerobic, endospore-forming, Gram- functions (Le Rudulier et al., 1984). Most archaeal compatible positive bacterium H. halophilus has become a model system solutes resemble in structure their bacterial counterpart, with to study salt adaptation at various cellular levels (Mu¨ller and the difference that the majority of them carry a negative charge Saum, 2005). (Martin et al., 1999; Roeßler and Mu¨ller, 2001b). H. halophilus is the first organism for which a strict chlo- The uptake and biosynthesis of compatible solutes is ride dependence of growth was described (Claus et al., 1983; À induced by high salinity or high osmolarity on both the DNA Roeßler and Mu¨ller, 1998). No growth was observed at a Cl and protein level. The pathways for the biosynthesis of various concentration of 0.2 M, but addition of chloride (to a medium solutes have been identified in different bacteria and archaea, with constant osmolarity) restored growth in a concentration- À but how the environmental signal “salinity” is sensed and how dependent manner. Optimal growth occurs at 0.8e1.0 M Cl . this signal is transmitted to various output modules at the level Moreover, not only growth rates but also cell yields (final of gene, enzyme or transporter activation is completely optical densities) were strictly chloride-dependent (Roeßler obscure (Wood et al., 2001). This is even more important if and Mu¨ller, 1998). one considers that the overall cellular response of cells to What looked like an exotic phenotype at a first glance was hypersalinity is not only the accumulation of solutes but analyzed in more detail. To understand the function of chloride a reprogramming of cellular metabolism and structure in it was important to figure out physiological processes that are general. The first step towards unraveling the complexity of chloride-dependent. In addition to growth, germination of regulation could be by genome-wide expression profiling endospores as well as flagella production and motility were studies, but unfortunately, these have not been done with identified to be chloride-dependent (Dohrmann and Mu¨ller, (moderate) halophiles. However, there are a few studies 1999; Roeßler et al., 2000) and the very different functions of available on halotolerant organisms that actually demonstrate ClÀ (motility, flagellation, spore germination,
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