Abstract
Microbial disproportionation of elemental sulfur to sulfide and sulfate is a poorly characterized part of the anoxic sulfur cycle. So far, only a few bacterial strains have been described that can couple this reaction to cell growth. Continuous removal of the produced sulfide, for instance by oxidation and/or precipitation with metal ions such as iron, is essential to keep the reaction exergonic. Hitherto, the process has exclusively been reported for neutrophilic anaerobic bacteria. Here, we report for the first time disproportionation of elemental sulfur by three pure cultures of haloalkaliphilic bacteria isolated from soda lakes: the Deltaproteobacteria Desulfurivibrio alkaliphilus and Desulfurivibrio sp. AMeS2, and a member of the Clostridia, Dethiobacter alkaliphilus. All cultures grew in saline media at pH 10 by sulfur disproportionation in the absence of metals as sulfide scavengers. Our data indicate that polysulfides are the dominant sulfur species under highly alkaline conditions and that they might be disproportionated. Furthermore, we report the first organism (Dt. alkaliphilus) from the class Clostridia that is able to grow by sulfur disproportionation.
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Adrian L, Hansen SK, Fung JM, Görisch H, Zinder SH (2007) Growth of Dehalococcoides strains with chlorophenols as electron acceptors. Environm Sci Technol 41:2318–2323
Bak F, Cypionka H (1987) A novel type of energy-metabolism involving fermentation of inorganic sulfur-compounds. Nature 326:891–892
Bak F, Pfennig N (1987) Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur-compounds. Arch Microbiol 147:184–189
Boulegue J, Michard G (1978) Constantes de formation des ions polysulfures S6 2−, S5 2− et S4 2− en phase aqueuese. J F Hydrol 9:27–33
Canfield DE, Thamdrup B (1996) Fate of elemental sulfur in an intertidal sediment. FEMS Microbiol Ecol 19:95–103
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458
Duckworth AW, Grant WD, Jones BE, van Steenbergen R (1996) Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiol Ecol 19:181–191
Finster K (2008) Microbiological disproportionation of inorganic sulfur compounds. J Sulfur Chem 29:281–292
Finster K, Liesack W, Thamdrup B (1998) Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol 64:119–125
Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2008) Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12:133–145
Franz B, Lichtenberg H, Hormes J, Modrow H, Dahl C, Prange A (2007) Utilization of solid ‘elemental’ sulfur by the phototrophic purple sulfur bacterium Allochromatium vinosum: a sulfur K-edge X-ray absorption spectroscopy study. Microbiology 153:1268–1274
Frederiksen TM, Finster K (2003) Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulfate and elemental sulfur. Biodegradation 14:189–198
Frederiksen TM, Finster K (2004) The transformation of inorganic sulfur compounds and the assimilation of organic and inorganic carbon by the sulfur disproportionating bacterium Desulfocapsa sulfoexigens. Antonie Van Leeuwenhoek 85:141–149
Grant WD (1992) Alkaline Environments. In: Lederberg J (ed) Encyclopedia of microbiology, vol 1. Academic Press, San Diego, pp 73–80
Gütlich P, Schröder C (2012) Mössbauer Spectroscopy. In: Schäfer R, Schmidt PC (eds) Methods in Physical Chemistry. Wiley-VCH, New York, pp 351–389
Gütlich P, Schröder C, Schünemann V (2012) Mössbauer spectroscopy—an indispensable tool in solid state research. Spectrosc Eur 24(4):21–32
Hedderich R, Klimmek O, Kröger A, Dirmeier R, Keller M, Stetter KO (1999) Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 22:353–381
Herrmann S, Kleinsteuber S, Neu TU, Richnow HH, Vogt C (2008) Enrichment of anaerobic benzene degrading microorganisms by in situ microcosms. FEMS Microbiol Ecol 63:94–106
Janssen PH, Schuhmann A, Bak F, Liesack W (1996) Disproportionation of inorganic sulfur compounds by the sulfate-reducing bacterium Desulfocapsa thiozymogenes gen. nov., sp. nov. Arch Microbiol 166:184–192
Jones BE, Grant WD, Duckworth AW, Owenson GG (1996) Microbial diversity of soda lakes. Extremophiles 2:191–200
Kamyshny A, Goifman A, Rizkov D, Lev O (2004) Kinetics of disproportionation of inorganic polysulfides in undersaturated aqueous solutions at environmentally relevant conditions. Aquat Geochem 9:291–304
Kamyshny A, Ekeltchik I, Gun J, Lev O (2006) Method for the determination of inorganic polysulfide distribution in aquatic systems. Anal Chem 78:2631–2639
Kamyshny A, Gun J, Rizkov D, Voitsekovski T, Lev O (2007) Equilibrium distribution of polysulfide ions in aqueous solutions at different temperatures by rapid single phase derivatization. Environ Sci Technol 41:2395–2400
Knickerbocker C, Nordstrom DK, Southam G (2000) The role of ‘‘blebbing’’ in overcoming the hydrophobic barrier during biooxidation of elemental sulfur by Thiobacillus thiooxidans. Chem Geol 169:425–433
Koschorreck M (2008) Microbial sulphate reduction at a low pH. FEMS Microbiol Ecol 64:329–342
Krämer M, Cypionka H (1989) Sulfate formation via ATP sulfurylase in thiosulfate-disproportionating and sulfite-disproportionation bacteria. Arch Microbiol 151:232–237
Melack JM, Kilham P (1974) Photosynthetic rates of phytoplankton in East African alkaline, saline lakes. Limnol Oceanogr 19:743–755
Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M, Lieberwirth I, Wagner M, Widdel F, Kuypers MMM (2012) Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491:541–546
Nielsen AH, Hvitved-Jacobsen T, Vollertson J (2008) Effects of pH and iron concentrations on sulfide precipitation in wastewater collection systems. Water Environ Res 80:380–384
Oren A (2011) Thermodynamic limits to microbial life at high salt concentration. Environ Microbiol 13:1908–1923
Peiffer S, dos Santos Afonso M, Wehrl B, Gachter R (1992) Kinetics and mechanism of the reaction of H2S with lepidocrocite. Environm Sci Technol 26:2408–2413
Philippot P, van Zuilen M, Lepot K, Thomazo C, Farquhar J, van Kranendonk MJ (2007) Early archaen microorganisms preferred elemental sulfur, not sulfate. Science 317:1534–1537
Pikuta EV, Hoover RB, Bej AK, Marsic D, Whitman WB, 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
Rizkov D, Lev O, Gun J, Anisimov B, Kuselman I (2004) Development of in-house reference materials for determination of inorganic polysulfides in water. Accred Qual Assur 9:399–403
Sorokin DY, Tourova TP, Henstra AM, Stams AJM, Galinski EA, Muyzer G (2008a) 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
Sorokin DY, Tourova T, Mußmann M, Muyzer G (2008b) Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles 12:431–439
Sorokin DY, Rusanov II, Pimenov NV, Tourova TP, Abbas B, Muyzer G (2010) Sulfidogenesis under extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol Ecol 73:273–290
Sorokin DY, Tourova TP, Detkova EN, Kolganova TV, Galinski EA, Muyzer G (2011a) 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
Sorokin DY, Kuenen JG, Muyzer G (2011b) The microbial sulfur cycle at extremely haloalkaline conditions of soda lakes. Front Microbiol 2:44
Sorokin DY, Detkova EN, Muyzer G (2011c) Sulfur-dependent respiration under extremely haloalkaline conditions in soda-lake acetogens and the description of Natronella sulfidigena sp. nov. FEMS Microbiol Lett 319:88–95
Sorokin DY, Banciu H, Robertson LA, Kuenen JG, Muyzer G (2013) Halophilic and haloalkaliphilic sulfur-oxidizing bacteria from habitats and soda lakes. In: Rosenberg E et al (eds) The prokaryotes—prokaryotic physiology and biochemistry. Springer-Verlag, Berlin-Heidelberg, pp 530–551
Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural water. Wiley-Interscience, New York
Sullivan PJ, Reddy KJ, Yelton JL (1988) Iron sulfide oxidation and the chemistry of acid generation. Environ Geol Water Sci 11:289–295
Thamdrup B, Finster K, Hansen JW, Bak F (1993) Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese. Appl Environ Microbiol 59:101–108
Zamana LV, Borzenko SV (2011) Elemental sulfur in the brine of Lake Doroninskoe (Eastern Transbaikalia). Dokl Earth Sci 438:775–778
Acknowledgments
Alexander Poser was supported by the German Research Foundation within the FOR 580 e-TraP project (Grant FOR 580 RIC). Britta Planer-Friedrich and Regina Lohmayer acknowledge funding by the German Research Foundation within project PL 302/5-1. Kai Finster acknowledges support by the Danish agency for science technology and innovation (Ref. no. 272-08-0497). This work was also supported by the RFBR Grant 13-04-40205 Comfi to Dimitry Y. Sorokin. We thank Christian Schröder (University Tübingen) for the Mössbauer analyses and Stephanie Hinke for valuable technical assistance.
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Poser, A., Lohmayer, R., Vogt, C. et al. Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes. Extremophiles 17, 1003–1012 (2013). https://doi.org/10.1007/s00792-013-0582-0
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DOI: https://doi.org/10.1007/s00792-013-0582-0