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      Desulfohalophilus alkaliarsenatis gen. nov., sp. nov., an extremely halophilic sulfate- and arsenate-respiring bacterium from Searles Lake, California

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          Abstract

          A haloalkaliphilic sulfate-respiring bacterium, strain SLSR-1, was isolated from a lactate-fed stable enrichment culture originally obtained from the extreme environment of Searles Lake, California. The isolate proved capable of growth via sulfate-reduction over a broad range of salinities (125–330 g/L), although growth was slowest at salt-saturation. Strain SLSR-1 was also capable of growth via dissimilatory arsenate-reduction and displayed an even broader range of salinity tolerance (50–330 g/L) when grown under these conditions. Strain SLSR-1 could also grow via dissimilatory nitrate reduction to ammonia. Growth experiments in the presence of high borate concentrations indicated a greater sensitivity of sulfate-reduction than arsenate-respiration to this naturally abundant anion in Searles Lake. Strain SLSR-1 contained genes involved in both sulfate-reduction ( dsrAB) and arsenate respiration ( arrA). Amplicons of 16S rRNA gene sequences obtained from DNA extracted from Searles Lake sediment revealed the presence of close relatives of strain SLSR-1 as part of the flora of this ecosystem despite the fact that sulfate-reduction activity could not be detected in situ. We conclude that strain SLSR-1 can only achieve growth via arsenate-reduction under the current chemical conditions prevalent at Searles Lake. Strain SLSR-1 is a deltaproteobacterium in the family Desulfohalobiacea of anaerobic, haloalkaliphilic bacteria, for which we propose the name Desulfohalophilus alkaliarsenatis gen. nov., sp. nov.

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          Most cited references32

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          Bioenergetic aspects of halophilism.

          Examination 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.
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            Thermodynamic limits to microbial life at high salt concentrations.

            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. © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd.
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              Genetic identification of a respiratory arsenate reductase.

              For more than a decade, it has been recognized that arsenate [H2AsO41-; As(V)] can be used by microorganisms as a terminal electron acceptor in anaerobic respiration. Given the toxicity of arsenic, the mechanistic basis of this process is intriguing, as is its evolutionary origin. Here we show that a two-gene cluster (arrAB; arsenate respiratory reduction) in the bacterium Shewanella sp. strain ANA-3 specifically confers respiratory As(V) reductase activity. Mutants with in-frame deletions of either arrA or arrB are incapable of growing on As(V), yet both are able to grow on a wide variety of other electron acceptors as efficiently as the wild-type. Complementation by the wild-type sequence rescues the mutants' ability to respire As(V). arrA is predicted to encode a 95.2-kDa protein with sequence motifs similar to the molybdenum containing enzymes of the dimethyl sulfoxide reductase family. arrB is predicted to encode a 25.7-kDa iron-sulfur protein. arrA and arrB comprise an operon that contains a twin arginine translocation (Tat) motif in ArrA (but not in ArrB) as well as a putative anaerobic transcription factor binding site upstream of arrA, suggesting that the respiratory As(V) reductase is exported to the periplasm via the Tat pathway and under anaerobic transcriptional control. These genes appear to define a new class of reductases that are specific for respiratory As(V) reduction.
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                Author and article information

                Contributors
                roremlan@usgs.gov
                Journal
                Extremophiles
                Extremophiles
                Extremophiles
                Springer Japan (Japan )
                1431-0651
                1433-4909
                29 June 2012
                29 June 2012
                September 2012
                : 16
                : 5
                : 727-742
                Affiliations
                [1 ]US Geological Survey, Menlo Park, CA 94025 USA
                [2 ]Department of Geological Sciences and Environmental Studies, Binghamton University, Binghamton, NY 13902 USA
                [3 ]Department of Biological Sciences, University of Alberta, Edmonton, AB Canada
                [4 ]Department of Microbiology and Toxicology, University of California, Santa Cruz, CA 95064 USA
                [5 ]Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282 USA
                Author notes

                Communicated by A. Oren.

                Article
                468
                10.1007/s00792-012-0468-6
                3432211
                22744231
                96b7557e-6e21-4d00-84d6-112e33c6bd6e
                © The Author(s) 2012
                History
                : 8 February 2012
                : 14 June 2012
                Categories
                Original Paper
                Custom metadata
                © Springer 2012

                Microbiology & Virology
                phylogeny,genetics,anaerobic bacteria,alkaliphile ecology,systematics,ecology,halophiles,taxonomy,enzymes,biotechnology,metaloxidation and reduction

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