Thermodynamic limits to microbial life at high salt concentrations.
TL;DR: New data is reviewed, both from field observations and from the characterization of cultures of new types of prokaryotes growing at high salt concentrations, to evaluate to what extent the theories formulated 12 years ago are still valid, need to be refined, or should be refuted.
Abstract: Summary
Life at high salt concentrations is energetically expensive. The upper salt concentration limit at which different dissimilatory processes occur in nature appears to be determined to a large extent by bioenergetic constraints. The main factors that determine whether a certain type of microorganism can make a living at high salt are the amount of energy generated during its dissimilatory metabolism and the mode of osmotic adaptation used. I here review new data, both from field observations and from the characterization of cultures of new types of prokaryotes growing at high salt concentrations, to evaluate to what extent the theories formulated 12 years ago are still valid, need to be refined, or should be refuted on the basis of the novel information collected. Most data agree well with the earlier theories. Some new observations, however, are not easily explained: the properties of Natranaerobius and other haloalkaliphilic thermophilic fermentative anaerobes, growth of the sulfate-reducing Desulfosalsimonas propionicica with complete oxidation of propionate and Desulfovermiculus halophilus with complete oxidation of butyrate, growth of lactate-oxidizing sulfate reducers related to Desulfonatronovibrio at 346 g l−1 salts at pH 9.8, and occurrence of methane oxidation in the anaerobic layers of Big Soda Lake and Mono Lake.
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TL;DR: The current state of knowledge for the biospace in which life operates on Earth is reviewed and discussed in a planetary context, highlighting knowledge gaps and areas of opportunity.
Abstract: Prokaryotic life has dominated most of the evolutionary history of our planet, evolving to occupy virtually all available environmental niches. Extremophiles, especially those thriving under multiple extremes, represent a key area of research for multiple disciplines, spanning from the study of adaptations to harsh conditions, to the biogeochemical cycling of elements. Extremophile research also has implications for origin of life studies and the search for life on other planetary and celestial bodies. In this article, we will review the current state of knowledge for the biospace in which life operates on Earth and will discuss it in a planetary context, highlighting knowledge gaps and areas of opportunity.
298 citations
Cites background from "Thermodynamic limits to microbial l..."
...The necessary energy needed to maintain osmosis, and the thermodynamics of surviving under saline conditions have been thoroughly discussed by Oren (2011)....
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...In contrast, many microorganisms that utilize the salt exclusion strategy can tolerate a wider range of salt concentrations due to the production of organic solutes to counter the concentration of salts (Oren, 2011)....
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TL;DR: The mechanisms of osmotic adaptation in a number of model organisms, including the KCl accumulating Halobacterium salinarum and Salinibacter ruber, and additional halophilic microorganisms presented are compared to obtain an integrative picture of the adaptations to life at high salt concentrations in the microbial world.
Abstract: Hypersaline environments with salt concentrations up to NaCl saturation are inhabited by a great diversity of microorganisms belonging to the three domains of life. They all must cope with the low water activity of their environment, but different strategies exist to provide osmotic balance of the cells' cytoplasm with the salinity of the medium. One option used by many halophilic Archaea and a few representatives of the Bacteria is to accumulate salts, mainly KCl and to adapt the entire intracellular machinery to function in the presence of molar concentrations of salts. A more widespread option is the synthesis or accumulation of organic osmotic, so-called compatible solutes. Here, we review the mechanisms of osmotic adaptation in a number of model organisms, including the KCl accumulating Halobacterium salinarum (Archaea) and Salinibacter ruber (Bacteria), Halomonas elongata as a representative of the Bacteria that synthesize organic osmotic solutes, eukaryotic microorganisms including the unicellular green alga Dunaliella salina and the black yeasts Hortaea werneckii and the basidiomycetous Wallemia ichthyophaga, which use glycerol and other compatible solutes. The strategies used by these model organisms and by additional halophilic microorganisms presented are then compared to obtain an integrative picture of the adaptations to life at high salt concentrations in the microbial world.
254 citations
TL;DR: There was a reduction in microbial richness and diversity after fracturing, with the lowest diversity at 49 days, and Thirty-one taxa dominated injected, flowback, and produced water communities, which took on distinct signatures as injected carbon and electron acceptors were attenuated within the shale.
Abstract: Microorganisms play several important roles in unconventional gas recovery, from biodegradation of hydrocarbons to souring of wells and corrosion of equipment. During and after the hydraulic fracturing process, microorganisms are subjected to harsh physicochemical conditions within the kilometer-deep hydrocarbon-bearing shale, including high pressures, elevated temperatures, exposure to chemical additives and biocides, and brine-level salinities. A portion of the injected fluid returns to the surface and may be reused in other fracturing operations, a process that can enrich for certain taxa. This study tracked microbial community dynamics using pyrotag sequencing of 16S rRNA genes in water samples from three hydraulically fractured Marcellus shale wells in Pennsylvania, USA over a 328-day period. There was a reduction in microbial richness and diversity after fracturing, with the lowest diversity at 49 days. Thirty-one taxa dominated injected, flowback, and produced water communities, which took on disti...
233 citations
TL;DR: Coupling the biogeochemical C, N, and S cycles and identifying where each process takes place on a spatial and temporal scale could unravel the interspecies relationships and thereby reveal more about the ecosystem dynamics of these enigmatic extreme environments.
Abstract: Soda lakes contain high concentrations of sodium carbonates resulting in a stable elevated pH, which provide a unique habitat to a rich diversity of haloalkaliphilic bacteria and archaea. Both cultivation-dependent and -independent methods have aided the identification of key processes and genes in the microbially mediated carbon, nitrogen, and sulfur biogeochemical cycles in soda lakes. In order to survive in this extreme environment, haloalkaliphiles have developed various bioenergetic and structural adaptations to maintain pH homeostasis and intracellular osmotic pressure. The cultivation of a handful of strains has led to the isolation of a number of extremozymes, which allow the cell to perform enzymatic reactions at these extreme conditions. These enzymes potentially contribute to biotechnological applications. In addition, microbial species active in the sulfur cycle can be used for sulfur remediation purposes. Future research should combine both innovative culture methods and state-of-the-art ‘meta-omic’ techniques to gain a comprehensive understanding of the microbes that flourish in these extreme environments and the processes they mediate. Coupling the biogeochemical C, N, and S cycles and identifying where each process takes place on a spatial and temporal scale could unravel the interspecies relationships and thereby reveal more about the ecosystem dynamics of these enigmatic extreme environments.
228 citations
Cites background from "Thermodynamic limits to microbial l..."
...Although the ‘‘salt out’’ strategy of osmotic regulation is energeti- cally more expensive than the ‘‘salt in’’ strategy, it allows microorganisms with a highly efficient energy metabolism to survive over larger salinity gradients (Oren 2011)....
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...Although the ‘‘salt out’’ strategy of osmotic regulation is energetically more expensive than the ‘‘salt in’’ strategy, it allows microorganisms with a highly efficient energy metabolism to survive over larger salinity gradients (Oren 2011)....
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...Extremely halo(alkali)philic Euryarchaeota predominantly utilize K? as an osmotic regulator (Oren 1999, 2011)....
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...…cell and sulfate reduction rates encountered even in soda lakes with more than 475 g/L, Foti et al. (2007) challenged an earlier hypothesis, specifically for the case of soda lakes, that complete carbon oxidizers could only grow at salt concentrations below 150 g/L (Oren, 1999 and Oren 2011)....
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TL;DR: In this paper, the progress of efforts to stimulate microbial methane generation in coal beds, and key remaining knowledge gaps are reviewed, and several key knowledge gaps remain that need to be addressed before MECoM strategies can be implemented commercially.
224 citations
Cites background from "Thermodynamic limits to microbial l..."
...Reduction in salinity is key for promoting methanogenesis in basins with high salinities because these organisms prefer Cl- concentrations b3 M (Doerfert et al., 2009; Hoehler et al, 2010; Oren, 2011; Osborn and McIntosh, 2010; Schlegel et al., 2011; Waldron et al., 2007)....
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References
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TL;DR: Examinination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities.
Abstract: Examinination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities. Examples are methanogenesis for H2 + CO2 or from acetate, dissimilatory sulfate reduction with oxidation of acetate, and autotrophic nitrification. Occurrence of the different metabolic types is correlated with the free-energy change associated with the dissimilatory reactions. Life at high salt concentrations is energetically expensive. Most bacteria and also the methanogenic archaea produce high intracellular concentrations of organic osmotic solutes at a high energetic cost. All halophilic microorganisms expend large amounts of energy to maintain steep gradients of NA+ and K+ concentrations across their cytoplasmic membrane. The energetic cost of salt adaptation probably dictates what types of metabolism can support life at the highest salt concentrations. Use of KCl as an intracellular solute, while requiring far-reaching adaptations of the intracellular machinery, is energetically more favorable than production of organic-compatible solutes. This may explain why the anaerobic halophilic fermentative bacteria (order Haloanaerobiales) use this strategy and also why halophilic homoacetogenic bacteria that produce acetate from H2 + CO2 exist whereas methanogens that use the same substrates in a reaction with a similar free-energy yield do not.
955 citations
TL;DR: The hypothesis that chronic energy stress is the primary selective pressure governing the evolution of the Archaea is proposed and proposed, and biochemical mechanisms that enable archaea to cope with chronicEnergy stress include low-permeability membranes and specific catabolic pathways.
Abstract: The three domains of life on Earth include the two prokaryotic groups, Archaea and Bacteria. The Archaea are distinguished from Bacteriabased on phylogenetic and biochemical differences, but currently there is no unifying ecological principle to differentiate these groups. The ecology of the Archaea is reviewed here in terms of cellular bioenergetics. Adaptation to chronic energy stress is hypothesized to be the crucial factor that distinguishes the Archaea from Bacteria. The biochemical mechanisms that enable archaea to cope with chronic energy stress include low-permeability membranes and specific catabolic pathways. Based on the ecological unity and biochemical adaptations among archaea, I propose the hypothesis that chronic energy stress is the primary selective pressure governing the evolution of the Archaea.
656 citations
TL;DR: Isolation of a bacterium from the natural environment that, although being a major component of the community, was previously known by its phylotype only is succeeded, allowing formal description of a novel genus and species.
Abstract: Five brightly red-pigmented, motile, rod-shaped, extremely halophilic bacteria were isolated from saltern crystallizer ponds in Alicante (two strains) and Mallorca (three strains), Spain. They grew optimally at salt concentrations between 20 and 30% and did not grow below 15% salts. Thus, these isolates are among the most halophilic organisms known within the domain Bacteria. The temperature optimum was 37-47 degrees C. A single, yet to be identified pigment was present, with an absorption maximum at 482 nm and a shoulder at 506-510 nm. The G+C content of the DNA was 66.3-67.7 mol% and, together, they formed a homogeneous genomic group with DNA-DNA similarities above 70%. The 16S rRNA gene sequences were almost identical to sequences recovered earlier from the saltern biomass by amplification of bacterial small-subunit rRNA genes from DNA extracted from the environment. This phylotype, earlier described as 'Candidatus Salinibacter', was shown by fluorescence in situ hybridization to contribute between 5 and 25% of the prokaryote community of the saltern crystallizers. We have therefore succeeded in isolating a bacterium from the natural environment that, although being a major component of the community, was previously known by its phylotype only. Isolation of the organism now allows formal description of a novel genus and species, for which we propose the name Salinibacter ruber gen. nov., sp. nov. The type strain is strain M31T (= DSM 13855T = CECT 5946T).
399 citations
TL;DR: Three pure culture-strains from different sulfide-containing sea water sources were characterized in detail and are described as a new genus and species Desulfuromonas acetoxidans, a new type of strictly anaerobic, rod-shaped, laterally flagellated, Gram-negative bacterium.
Abstract: Anaerobic sea or fresh water media with acetate and elemental sulfur yielded enrichments of a new type of strictly anaerobic, rod-shaped, laterally flagellated, Gram-negative bacterium. Three pure culture-strains from different sulfide-containing sea water sources were characterized in detail and are described as a new genus and species Desulfuromonas acetoxidans. The new bacterium is unable to ferment organic substances; it obtains energy for growth by anaerobic sulfur respiration. Acetate, ethanol or propanol can serve as carbon and energy source for growth; their oxidation to CO2 is stoichiometrically linked to the reduction of elemental sulfur to sulfide. Organic disulfide compounds, malate or fumarate are the only other electron acceptors used. Butanol and pyruvate are used in the presence of malate only; no other organic compounds are utilized. Biotin is required as a growth factor. The following dry weight yields per mole of substrate are obtained: in the presence of sulfur: 4.21 g on acetate, 9.77 g on ethanol; in the presence of malate: 16.5 g on acetate, 34.2 g on ethanol and 46.2 g on pyruvate. Accumulations of cells are pink; cell suspensions exhibit absorption spectra resembling those of c-type cytochromes (abs. max. at 419, 523 and 553 nm). Malate-ethanol grown cells contain a b-type cytochrome in addition. In the presence of acetate, ethanol or propanol, Desulfuromonas strains form robust growing syntrophic mixed cultures with phototrophic green sulfur bacteria.
360 citations
TL;DR: The ecological niches of methanotrophic Archaea seem to be mainly defined by the availability of methane and sulfate, but it remains open which additional factors lead to the dominance of ANME-I or -II in the environment.
Abstract: The anaerobic oxidation of methane (AOM) is one of the major sinks for methane on earth and is known to be mediated by at least two phylogenetically different groups of anaerobic methanotrophic Archaea (ANME-I and ANME-II) We present the first comparative in vitro study of the environmental regulation and physiology of these two methane-oxidizing communities, which occur naturally enriched in the anoxic Black Sea (ANME-I) and at Hydrate Ridge (ANME-II) Both types of methanotrophic communities are associated with sulfate-reducing-bacteria (SRB) and oxidize methane anaerobically in a 1:1 ratio to sulfate reduction (SR) They responded sensitively to elevated methane partial pressures with increased substrate turnover The ANME-II-dominated community showed significantly higher cell-specific AOM rates Besides sulfate, no other electron acceptor was used for AOM The processes of AOM and SR could not be uncoupled by feeding the SRB with electron donors such as acetate, formate or molecular hydrogen AOM was completely inhibited by the addition of bromoethanesulfonate in both communities, indicating the participation of methanogenic enzymes in the process Temperature influenced the intensity of AOM, with ANME-II being more adapted to cold temperatures than ANME-I The variation of other environmental parameters, such as sulfate concentration, pH and salinity, did not influence the activity of both communities In conclusion, the ecological niches of methanotrophic Archaea seem to be mainly defined by the availability of methane and sulfate, but it remains open which additional factors lead to the dominance of ANME-I or -II in the environment
315 citations