1887

Abstract

So far, anaerobic sulfate-dependent acetate oxidation at high pH has only been demonstrated for a low-salt-tolerant syntrophic association of a clostridium ‘ Contubernalis alkalaceticum’ and its hydrogenotrophic sulfate-reducing partner . Anaerobic enrichments at pH 10 inoculated with sediments from hypersaline soda lakes of the Kulunda Steppe (Altai, Russia) demonstrated the possibility of sulfate-dependent acetate oxidation at much higher salt concentrations (up to 3.5 M total Na). The most salt-tolerant purified cultures contained two major components apparently working in syntrophy. The primary acetate-fermenting component was identified as a member of the order forming, together with ‘ Contubernalis alkalaceticum’, an independent branch within the family . A provisional name, ‘ Syntrophonatronum acetioxidans’, is suggested for the novel haloalkaliphilic clostridium. Two phylotypes of extremely haloalkaliphilic sulfate-reducing bacteria of the genus were identified as sulfate-reducing partners in the acetate-oxidizing cultures under extreme salinity. The dominant phylotype differed from the two species of described so far, whilst a minor component belonged to . The results proved that, contrary to previous beliefs, sulfate-dependent acetate oxidation is possible, albeit very slowly, in nearly saturated soda brines.

Funding
This study was supported by the:
  • Russian Foundation for Basic Research (Award 13-04-40405 comfi and 13-04-00049)
  • ERC
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2014-04-01
2024-04-24
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References

  1. Brown S. D., Begemann M. B., Mormile M. R., Wall J. D., Han C. S., Goodwin L. A., Pitluck S., Land M. L., Hauser L. J., Elias D. A. ( 2011). Complete genome sequence of the haloalkaliphilic, hydrogen-producing bacterium Halanaerobium hydrogenoformans. J Bacteriol 193:3682–3683 [View Article][PubMed]
    [Google Scholar]
  2. Geets J., Borremans B., Diels L., Springael D., Vangronsveld J., van der Lelie D., Vanbroekhoven K. ( 2006). DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J Microbiol Methods 66:194–205 [View Article][PubMed]
    [Google Scholar]
  3. Gorlenko V. M., Namsaraev B. B., Kulyrova A. V., Zavarzina D. G., Zhilina T. N. ( 1999) Activity of sulfate-reducing bacteria in the sediments of the soda lakes in south-east Transbaikal area. Microbiology (English translation of Mikrobiologiia) 68:580–586
    [Google Scholar]
  4. Kevbrin V. V., Zhilina T. N., Zavarzin G. A. ( 1999) Decomposition of cellulose by the anaerobic alkaliphilic microbial community. Microbiology (English translation of Mikrobiologiia) 68:601–609
    [Google Scholar]
  5. Kulp T. R., Hoeft S. E., Miller L. G., Saltikov C., Murphy J. N., Han S., Lanoil B., Oremland R. S. ( 2006). Dissimilatory arsenate and sulfate reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl Environ Microbiol 72:6514–6526 [View Article][PubMed]
    [Google Scholar]
  6. Kulp T. R., Han S., Saltikov C. W., Lanoil B. D., Zargar K., Oremland R. S. ( 2007). Effects of imposed salinity gradients on dissimilatory arsenate reduction, sulfate reduction, and other microbial processes in sediments from two California soda lakes. Appl Environ Microbiol 73:5130–5137 [View Article][PubMed]
    [Google Scholar]
  7. Lane D. J. ( 1991). 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics115–177 Stackebrandt E., Goodfellow M. Chichester: Wiley;
    [Google Scholar]
  8. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. ( 1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275[PubMed]
    [Google Scholar]
  9. Loy A., Duller S., Baranyi C., Mussmann M., Ott J., Sharon I., Béjà O., Le Paslier D., Dahl C., Wagner M. ( 2009). Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ Microbiol 11:289–299 [View Article][PubMed]
    [Google Scholar]
  10. McInerney M. J., Struchtemeyer C. G., Sieber J., Mouttaki H., Stams A. J. M., Schink B., Rohlin L., Gunsalus R. P. ( 2008). Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 1125:58–72 [View Article][PubMed]
    [Google Scholar]
  11. Oren A. ( 2011). Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923 [View Article][PubMed]
    [Google Scholar]
  12. Pfennig N., Lippert K. D. ( 1966). Über das Vitamin B12 – bedürfnis phototropher Schwefel bacterien. Arch Mikrobiol 55:245–256 [View Article]
    [Google Scholar]
  13. Pikuta E. V., Zhilina T. N., Zavarzin G. A., Kostrikina N. A., Osipov G. A., Rainey F. A. ( 1998) Desulfonatronum lacustre gen. nov., sp. nov.: a new alkaliphilic sulfate-reducing bacterium utilizing ethanol. Microbiology (English translation of Mikrobiologiia) 67:105–113
    [Google Scholar]
  14. Pikuta E. V., Hoover R. B., Bej A. K., Marsic D., Whitman W. B., Cleland D., Krader P. ( 2003). Desulfonatronum thiodismutans sp. nov., a novel alkaliphilic, sulfate-reducing bacterium capable of lithoautotrophic growth. Int J Syst Evol Microbiol 53:1327–1332 [View Article][PubMed]
    [Google Scholar]
  15. Plugge C. M. ( 2005). Anoxic media design, preparation, and considerations. Methods Enzymol 397:3–16 [View Article][PubMed]
    [Google Scholar]
  16. Schäfer H., Muyzer G. ( 2001). Denaturing gradient gel electrophoresis in marine microbial ecology. Methods Microbiol 30:425–468 [View Article]
    [Google Scholar]
  17. Schink B., Stams A. J. M. ( 2006). Syntrophism among Prokaryotes. The Prokaryotes, 3nd edn. vol. 2309–335 Dworkin M., Falkow S., Rosenberg E., Schleifer K. H., Stackebrandt E. New York: Springer; [View Article]
    [Google Scholar]
  18. Sorokin D. Y., Muyzer G. ( 2010). Desulfurispira natronophila gen. nov. sp. nov.: an obligately anaerobic dissimilatory sulfur-reducing bacterium from soda lakes. Extremophiles 14:349–355 [View Article][PubMed]
    [Google Scholar]
  19. Sorokin D. Y., Gorlenko V. M., Namsaraev B. B., Namsaraev Z. B., Lysenko A. M., Eshinimaev B. T., Khmelenina V. N., Trotsenko Y. A., Kuenen J. G. ( 2004). Prokaryotic communities of the north-eastern Mongolian soda lakes. Hydrobiologia 522:235–248 [View Article]
    [Google Scholar]
  20. Sorokin D. Y., Tourova T. P., Henstra A. M., Stams A. J. M., Galinski E. A., Muyzer G. ( 2008). Sulfidogenesis under extremely haloalkaline conditions by Desulfonatronospira thiodismutans gen. nov., sp. nov., and Desulfonatronospira delicata sp. nov. – a novel lineage of Deltaproteobacteria from hypersaline soda lakes. Microbiology 154:1444–1453 [View Article][PubMed]
    [Google Scholar]
  21. Sorokin D. Y., Rusanov I. I., Pimenov N. V., Tourova T. P., Abbas B., Muyzer G. ( 2010a). Sulfidogenesis under extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol Ecol 73:278–290[PubMed]
    [Google Scholar]
  22. Sorokin D. Y., Detkova E. N., Muyzer G. ( 2010b). Propionate and butyrate dependent bacterial sulfate reduction at extremely haloalkaline conditions and description of Desulfobotulus alkaliphilus sp. nov.. Extremophiles 14:71–77 [View Article][PubMed]
    [Google Scholar]
  23. Sorokin D. Y., Kuenen J. G., Muyzer G. ( 2011a). The microbial sulfur cycle at extremely haloalkaline conditions of soda lakes. Front Microbiol 2:44 [View Article][PubMed]
    [Google Scholar]
  24. Sorokin D. Y., Tourova T. P., Kolganova T. V., Detkova E. N., Galinski E. A., Muyzer G. ( 2011b). Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov.. Extremophiles 15:391–401 [View Article][PubMed]
    [Google Scholar]
  25. Sorokin D. Y., Panteleeva A. N., Tourova T. P., Muyzer G. ( 2012). Desulfonatronobacter acidivorans gen. nov., sp. nov. and Desulfobulbus alkaliphilus sp. nov., haloalkaliphilic heterotrophic sulfate-reducing bacteria from soda lake. Int J Syst Evol Microbiol 62:2107–2113 [View Article][PubMed]
    [Google Scholar]
  26. Stams A. J. M., Plugge C. M. ( 2009). Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577 [View Article][PubMed]
    [Google Scholar]
  27. Trüper H. G., Schlegel H. G. ( 1964). Sulfur metabolism in Thiorhodaceae. 1. Quantitative measurements on growing cells of Chromatium okenii. Antonie van Leeuwenhoek 30:225–238 [View Article][PubMed]
    [Google Scholar]
  28. Wagner M., Roger A. J., Flax J. L., Brusseau G. A., Stahl D. A. ( 1998). Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180:2975–2982[PubMed]
    [Google Scholar]
  29. Zhilina T. N., Zavarzin G. A., Rainey F. A., Pikuta E. N., Osipov G. A., Kostrikina N. A. ( 1997). Desulfonatronovibrio hydrogenovorans gen. nov., sp. nov., an alkaliphilic, sulfate-reducing bacterium. Int J Syst Bacteriol 47:144–149 [View Article][PubMed]
    [Google Scholar]
  30. Zhilina T. N., Zavarzina D. G., Kuever J., Lysenko A. M., Zavarzin G. A. ( 2005a). Desulfonatronum cooperativum sp. nov., a novel hydrogenotrophic, alkaliphilic, sulfate-reducing bacterium, from a syntrophic culture growing on acetate. Int J Syst Evol Microbiol 55:1001–1006 [View Article][PubMed]
    [Google Scholar]
  31. Zhilina T. N., Zavarzina D. G., Kolganova T. V., Turova T. P., Zavarzin G. A. ( 2005b). [“Candidatus Contubernalis alkalaceticum”, an obligately syntrophic alkaliphilic bacterium capable of anaerobic acetate oxidation in a coculture with Desulfonatronum cooperativum.]. Mikrobiologiia 74:800–809[PubMed]
    [Google Scholar]
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