Skip to main content
Log in

Diversity of Sulfur-Disproportionating Microorganisms

  • REVIEWS
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Microorganisms disproportionating inorganic sulfur compounds are involved in biogeochemical cycles of elements in the modern biosphere. Sulfur-disproportionating prokaryotes are represented by 30 species of the Bacteria domain and belong to the phyla Proteobacteria, Thermodesulfobacteria, and Firmicutes. Most of the sulfur-disproportionating bacteria belong to four orders of the class Deltaproteobacteria. The microorganisms responsible for dismutation of sulfur compounds inhabit freshwater and shallow marine sediments, hypersaline and soda lakes, anthropogenic environments, and various natural thermal ecosystems. Most sulfur-disproportionating organisms are able to use other processes for growth, primarily dissimilatory sulfate reduction. Ability to grow autotrophically was shown for 17 sulfur-disproportionating strains from different phylogenetic groups. The biochemical mechanisms involved in disproportionation of sulfur compounds remain uncertain, which hinders the application of the current omics techniques. Comparative analysis of available complete genomes of the microorganisms capable of elemental sulfur disproportionation is provided. The presence of the complete set of the dissimilatory sulfate reduction genes was found not to be necessary for S0 disproportionation. This process does not require dissimilatory sulfite reductase (Dsr) and adenylyl-sulfate reductase (Apr). Sulfur relay proteins and the elemental sulfur- and/or polysulfides-reducing enzymes are important in sulfur disproportionation, but different microorganisms probably employ different sulfur transferases and polysulfide reductases in these processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Bak, F. and Cypionka, H., A novel type of energy metabolism involving fermentation of inorganic sulphur compounds, Nature, 1987, vol. 326, pp. 891‒892.

    Article  CAS  Google Scholar 

  2. Bak, F. and Phennig, N., Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur compounds, Arch. Microbiol., 1987, vol. 147, pp. 184‒189.

    Article  CAS  Google Scholar 

  3. Blumentals, I.I., Itoh, M., Olson, G.J. and Kelly, R.M., Role of polysulphides in reduction of elemental sulfur by the hyperthermophilic archaebacterium Pyrococcus furiosus, Appl. Environ. Microbiol., 1990, vol. 56, pp. 1255‒1262.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Boyd, E.S. and Druschel, G.K., Involvement of intermediate sulfur species in biological reduction of elemental sulfur under acidic, hydrothermal conditions, Appl. Environ. Microbiol., 2013, vol. 79, pp. 2061‒2068.

    Article  CAS  Google Scholar 

  5. Canfield, D.E. and Thamdrup, B., The production of 34S depleted sulfide during bacterial disproportionation of elemental sulfur, Science, 1994, vol. 266, pp. 1973–1975.

    Article  CAS  Google Scholar 

  6. Canfield, D.E. and Thamdrup, B., Fate of elemental sulfur in an intertidal sediment, FEMS Microbiol. Ecol., 1996, vol. 19, pp. 95–103.

    Article  CAS  Google Scholar 

  7. Chernyh, N.A., Mardanov, A.V., Gumerov, V.M., Miroshnichenko, M.L., Lebedinsky, A.V., Merkel, A.Y., Crowe, D., Pimenov, N.V., Rusanov, I.I., Ravin, N.V., Moran, and M.A., Bonch-Osmolovskaya, E.A., Microbial life in Bourlyashchy, the hottest thermal pool of Uzon Caldera, Kamchatka, Extremophiles, 2015, vol. 19, pp. 1157–1171.

    Article  CAS  Google Scholar 

  8. Cypionka, H., Smock, A.M, and Böttcher, M.E., A combined pathway of sulfur compound disproportionation in Desulfovivrio desulfuricans, FEMS Microbiol. Lett., 1998, vol. 166, pp. 181–186.

    Article  CAS  Google Scholar 

  9. DeWeerd, K.A., Mandelco, L., Tanner, R.S., Woese, C.R., and Suflita, J.M., Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium, Arch. Microbiol., 1990, vol. 154, pp. 23‒30.

    Article  CAS  Google Scholar 

  10. Finster, K.A.I., Liesack, W., and Thamdrup, B.O., Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment, Appl. Environ. Microbiol., 1998, vol. 64, pp. 119‒125.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Finster, K., Microbiological disproportionation of inorganic sulfur compounds, J. Sulfur Chem., 2008, vol. 29, pp. 281–292. https://doi.org/10.1080/17415990802105770

    Article  CAS  Google Scholar 

  12. Finster K.W., Kjeldsen K.U., Kube M., Reinhardt R., Mussmann M., Amann R., Schreiber L. Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds, Stand. Genomic. Sci. 2013, vol. 8, pp. 58‒68.

    Article  CAS  Google Scholar 

  13. Florentino, A.P., Brienza, C., Stams, A.J.M., and Sánchez-Andrea, I., Desulfurella amilsii sp. nov., a novel acidotolerant sulfur-respiring bacterium isolated from acidic river sediments, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1249‒1253. https://doi.org/10.1099/ijsem.0.000866

    Article  CAS  PubMed  Google Scholar 

  14. Florentino, A.P., Stams, A.J.M., and Sánchez-Andrea, I., Genome sequence of Desulfurella amilsii strain TR1 and comparative genomics of Desulfurellaceae family, Front. Microbiol., 2017, vol. 8, p. 222.https://doi.org/10.3389/fmicb.2017.00222

    Article  PubMed  PubMed Central  Google Scholar 

  15. Florentino, A.P., Pereira, I.A.C., Boeren, S., van den Born, M., Stams, A.J.M., and Sánchez-Andrea, I., Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics, Environ. Microbiol., 2019, vol. 21, pp. 209-225. https://doi.org/10.1111/1462-2920.14442

    Article  CAS  PubMed  Google Scholar 

  16. Flores, G.E., Campbell, J.H., Kirshtein, J.D., Meneghin, J., Podar, M., Steinberg, J.I., Seewald, J.S., Tivey, M.K., Voytek, M.A., Yang, Z.K., and Reysenbach, A.L., Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge, Environ. Microbiol., 2011, vol. 13, pp. 2158–2171.

    Article  CAS  Google Scholar 

  17. Francis, C.A., Obraztsova, A.Y., and Tebo, B.M., Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1, Appl. Environ. Microbiol., 2000, vol. 66, pp. 543‒548.

    Article  CAS  Google Scholar 

  18. Frederiksen, T.M. and Finster, K., Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulfate and elemental sulfur, Biodegradation, 2003, vol. 14, pp. 189–198.

    Article  CAS  Google Scholar 

  19. Friedrich, M., Springer, N., Ludwig, W., and Schink, B., Phylogenetic positions of Desulfofustis glycolicus gen. nov., sp. nov., and Syntrophobotulus glycolicus gen. nov., sp. nov., two new strict anaerobes growing with glycolic acid, Int. J. Syst. Bacteriol., 1996, vol. 46, pp. 1065‒1069.

    Article  CAS  Google Scholar 

  20. Frolova, A.A., Slobodkina, G.B. Baslerov, R.V., Novikov, A.A., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I. Thermosulfurimonas marina sp. nov., an autotrophic sulfur-disproportionating and nitrate-reducing bacterium isolated from a shallow-sea hydrothermal vent, Microbiology (Moscow), 2018, vol. 87, no. 4, pp. 502–507. https://doi.org/10.1134/S0026261718040082

    Article  CAS  Google Scholar 

  21. Hardisty, D.S., Olyphant, G.A., Bell, J.B., Johnson, A.P., and Pratt, L.M., Acidophilic sulfur disproportionation, Geochim. Cosmochim. Acta, 2013, vol. 113, pp. 136–151.

    Article  CAS  Google Scholar 

  22. Janssen, P.H., Schuhmann, A., Bak, F., and Liesack, W., Disproportionation of inorganic sulfur compounds by the sulfate-reducing bacterium Desulfocapsa thiozymogenes gen. nov., sp. nov., Arch. Microbiol., 1996, vol. 166, pp. 184–192.

    Article  CAS  Google Scholar 

  23. Jackson, B.E. and McInerney, M., Thiosulfate disproportionation by Desulfotomaculum thermobenzoicum, Appl. Environ. Microbiol., 2000, vol. 66, pp. 3650‒3653.

    Article  CAS  Google Scholar 

  24. Jorgensen, B.B., A thiosulfate shunt in the sulfur cycle ofmarine sediments, Science, 1990, vol. 249, pp. 152‒154.

    Article  CAS  Google Scholar 

  25. Kamyshny, A., Jr., Goifman, A., Gun, J., Rizkov, D., and Lev, O., Equilibrium distribution of polysulfide ions in aqueous solutions at 25°C:  a new approach for the study of polysulfides' equilibria, Environ. Sci. Technol., 2004, vol. 38, pp. 6633–6644.

    Article  CAS  Google Scholar 

  26. Kamyshny, A., Solubility of cyclooctasulfur in pure water and sea water at different temperatures, Geochim. Cosmochim. Acta, 2009, vol. 73, pp. 6022–6028.

    Article  CAS  Google Scholar 

  27. Kojima, H., Umezawa, K., and Fukui, M. Caldimicrobium thiodismutans sp. nov., a sulfur-disproportionating bacterium isolated from a hot spring, and emended description of the genus Caldimicrobium, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1828‒1831. https://doi.org/10.1099/ijsem.0.000947

    Article  CAS  PubMed  Google Scholar 

  28. Kramer, M. and Cypionka, H., Sulfate formation via ATP sulfurylase in thiosulfate- and sulfite-disproportionating bacteria, Arch. Microbiol., 1989, vol. 151, pp. 232‒237.

    Article  Google Scholar 

  29. Krekeler, D., Sigalevich, P., Teske, A., Cypionka, H., and Cohen, Y., A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov., Arch. Microbiol., 1997, vol. 167, pp. 369‒375.

    Article  CAS  Google Scholar 

  30. Lloyd, K.G., Lapham, L., and Teske, A., An anaerobic methane- oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments, Appl. Environ. Microbiol., 2006, vol. 72, pp. 7218–7230. doi:. 00886-06https://doi.org/10.1128/AEM

  31. Lovley, D.R. and Phillips, E.J.P., Novel processes for anaerobic sulfate production from elemental sulfur by sulfate-reducing bacteria, Appl. Environ. Microbiol., 1994, vol. 60, pp. 2394–2399.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lübbe, Y.J., Youn, H.-S., Timkovich, R., and Dahl, C., Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a,c-diamide synthase, for sulphur oxidation, FEMS Microbiol. Lett., 2006, vol. 261, pp. 194–202.

    Article  Google Scholar 

  33. Ma, K., Weiss, R., and Adams, M.W.W., Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction, J. Bacteriol., 2000, vol. 182, pp. 1864–1871.

    Article  CAS  Google Scholar 

  34. Mardanov, A.V., Beletsky, A.V., Kadnikov, V.V., Slobodkin, A.I., and Ravin, N.V., Genome analysis of Thermosulfurimonas dismutans, the first thermophilic sulfur-disproportionating bacterium of the phylum Thermodesulfobacteria, Front. Microbiol., 2016, vol. 7, p. 950. https://doi.org/10.3389/fmicb.2016.00950

    Article  PubMed  PubMed Central  Google Scholar 

  35. Melton, E.D., Sorokin, D.Y., Overmars, L., Lapidus, A.L., Pillay, M., Ivanova, N., del Rio, T.G., Kyrpides, N.C., Woyke, T., and Muyzer, G., Draft genome sequence of Dethiobacter alkaliphilus strain AHT1T, a gram-positive sulfidogenic polyextremophile, Stand. Genomic Sci., 2017, vol. 12, p. 57.

    Article  Google Scholar 

  36. Merkel, A.Yu., Pimenov, N.V., Rusanov, I.I., Slobodkin, A.I., Slobodkina, G.B., Tarnovetckii, I.Yu., Frolov, E.N., Dubin, A.V., Perevalova, A.A., and Bonch‑Osmolovskaya, E.A., Microbial diversity and autotrophic activity in Kamchatka hot springs, Extremophiles, 2017, vol. 21, pp. 307–317. https://doi.org/10.1007/s00792-016-0903-1

    Article  CAS  PubMed  Google Scholar 

  37. Milucka, J., Ferdelman, T.G., Polerecky, L., Franzke, D., Wegener, G., Schmid, M., Lieberwirth, I., Wagner, M., Widdel, F., and Kuypers, M.M.,Zero-valent sulphur is a key intermediate in marine methane oxidation, Nature,2012, vol. 491, pp. 541–546. https://doi.org/10.1038/nature11656

    Article  CAS  Google Scholar 

  38. Mohn, W.W. and Tiedje, J.M., Catabolic thiosulfate disproportionation and carbon dioxide reduction in strain DCB-1, a reductively dechlorinating anaerobe, J. Bacteriol., 1990, vol. 172, pp. 2065–2070.

    Article  CAS  Google Scholar 

  39. Nazina, T.N., Rozanova, E.P., Belyakova, E.V., Lysenko, A.M., Poltaraus, A.B., Tourova, T.P., Osipov, G.A., and Beliaev, S.S., Description of “Desulfotomaculum nigrificans subsp. salinus” as a new species, Desulfotomaculum salinum sp. nov., Microbiology (Moscow), 2005, vol. 74, no. 5, pp. 567–574. https://doi.org/10.1007/s11021-005-0104-x

    Article  CAS  Google Scholar 

  40. Obraztsova, A.Y., Francis, C.A., and Bradley, M.T., Sulfur disproportionation by the facultative anaerobe Pantoea agglomerans SP1 as a mechanism for chromium(VI) reduction, Geomicrobiol. J., 2002, vol. 19, pp. 121–132.

    Article  CAS  Google Scholar 

  41. Osorio, H., Mangold, S., Denis, Y., Ñancucheo, I., Esparza, M., Johnson, D.B., Bonnefoy, V., Dopson, M., and Holmes, D.S., Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans, Appl. Environ. Microbiol., 2013, vol. 79, pp. 2172‒2181.

    Article  CAS  Google Scholar 

  42. Pagani, I., Lapidus, A., Nolan, M., Lucas, S., Hammon, N., Deshpande, S., Cheng, J.F., Chertkov, O., Davenport, K., Tapia, R., Han, C., Goodwin, L., Pitluck, S., Liolios, K., Mavromatis, K., et al., Complete genome sequence of Desulfobulbus propionicus type strain (1pr3), Stand. Genomic Sci., 2011, vol. 4, p. 100. https://doi.org/10.4056/sigs.1613929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Peduzzi, S., Tonalla, M., and Hahn, D., Isolation and characterization of aggregate-forming sulfate-reducing and purple sulfur bacteria from the chemocline of meromictic Lake Cadagno, Switzerland, FEMS Microbiol. Ecol., 2003, vol. 45, pp. 29–37.

    Article  CAS  Google Scholar 

  44. Pereira, I.A.C., Ramos, A.R., Grein, F., Marques, M.C., da Silva, S.M., and Venceslau, S.S., A comparative genomic analysis of energy metabolism in sulfate- reducing bacteria and archaea, Front. Microbiol., 2011, vol. 2, p. 69. https://doi.org/10.3389/fmicb.2011.00069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Perez Bernal, M.F., Souza Brito, M.A., Bartoli, M., Aube, J., Fardeau, M.-L., Cuevas Rodriguez, G., Ollivier, B., Guyoneaud, R., and Hirschler-Rea, A., Desulfonatronum parangueonense sp. nov., a sulfate-reducing bacterium isolated from sediment of an alkaline crater lake, Int. J. Syst. Evol. Microbiol., 2017, vol. 67, pp. 4999–5005. https://doi.org/10.1099/ijsem.0.002399

    Article  CAS  PubMed  Google Scholar 

  46. Philippot, P., Van Zuilen, M., Lepot, K., Thomazo, C., Farquhar, J., and Van Kranendonk, M.J., Early Archaean microorganisms preferred elemental sulfur, not sulfate, Science, 2007, vol. 317, pp. 1534–1537.

    Article  CAS  Google Scholar 

  47. Pikuta, E.V., Zhilina, T.N., Zavarzin, G.A., Kostrikina, N.A., Osipov, G.A., and Rainey, F.A., Desulfonatronum lacustre gen. nov., sp. nov.: a new alkaliphilic sulfate-reducing bacterium utilizing ethanol, Microbiology (Moscow), 1998, vol. 67, no. 1, pp. 105‒113.

    CAS  Google Scholar 

  48. Pikuta, E.V., Hoover, R.B., Bej, A.K, Marsic, D., Whitman, W.B., Cleland, D., and Krader, P., Desulfonatronum thiodismutans sp. nov., a novel alkaliphilic, sulfate-reducing bacterium capable of lithoautotrophic growth, Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1327–1332.

    Article  CAS  Google Scholar 

  49. Poser, A., Lohmayer, R., Vogt, C., Knoeller, K., Planer-Friedrich, B., Sorokin, D., Richnow, H-H., and Finster, K., Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes, Extremophiles, 2013, vol. 17, pp. 1003‒1012. https://doi.org/10.1007/s00792-013-0582-1

    Article  CAS  PubMed  Google Scholar 

  50. Pjevac, P. Kamyshny, A., Jr., Dyksma, S., and Mußmann, M., Microbial consumption of zero-valence sulfur in marine benthic habitats, Environ. Microbiol., 2014, vol. 16, pp. 3416–3430. https://doi.org/10.1111/1462-2920.12410

    Article  CAS  PubMed  Google Scholar 

  51. Quatrini, R., Appia-Ayme, C., Denis, Y., Jedlicki, E., Holmes, D., and Bonnefoy, V., Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans, BMC Genomics,2009, vol. 10, p. 394. https://doi.org/10.1186/1471-2164-10-394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Rabus, R., Venceslau, S.S., Wohlbrand, L., Voordouw, G., Wall, J.D., and Pereira, I.A.C., A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes, Adv. Microb. Physiol., 2015, vol. 66, pp. 55‒321. https://doi.org/10.1016/bs.ampbs.2015.05.002

    Article  CAS  PubMed  Google Scholar 

  53. Ruff, S.E., Biddle, J.F., Teske, A.P., Knittel, K., Boetius, A., and Ramette, A.,Global dispersion and local diversification of the methane seep microbiome, Proc. Natl. Acad. Sci. U. S. A.,2015, vol. 112, pp. 4015–4020. https://doi.org/10.1073/pnas.1421865112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Schauder, R. and Muëller, E., Polysulphide as a possible substrate for sulphur-reducing bacteria, Arch. Microbiol., 1993, vol. 160, pp. 377‒382.

    Article  CAS  Google Scholar 

  55. Slobodkin, A.I., Reysenbach, A.-L., Slobodkina, G.B., Baslerov, R.V., Kostrikina, N.A., Wagner, I.D., and Bonch-Osmolovskaya, E.A. Thermosulfurimonas dismutans gen. nov., sp. nov. a novel extremely thermophilic sulfur-disproportionating bacterium from a deep-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 2565‒2571. https://doi.org/10.1099/ijs.0.034397-0

    Article  CAS  PubMed  Google Scholar 

  56. Slobodkin, A.I., Reysenbach, A.-L., Slobodkina, G.B., Kolganova, T.V., Kostrikina, N.A., and Bonch-Osmolovskaya, E.A., Dissulfuribacter thermophilus gen. nov., sp. nov. a novel thermophilic autotrophic sulfur-disproportionating deeply-branching delta-proteobacterium from a deep-sea hydrothermal vent of the Eastern Lau Spreading Center, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 1967‒1971. https://doi.org/10.1099/ijs.0.046938-0

    Article  CAS  PubMed  Google Scholar 

  57. Slobodkin, A.I., Slobodkina, G.B., Panteleeva, A.N., Chernyh, N.A., Novikov, A.A., and Bonch-Osmolovskaya, E.A., Dissulfurimicrobium hydrothermale gen. nov., sp. nov., a thermophilic, autotrophic, sulfur-disproportionating deltaproteobacterium isolated from a hydrothermal pond of Uzon Caldera, Kamchatka, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1022-1026. https://doi.org/10.1099/ijsem.0.000828

    Article  CAS  PubMed  Google Scholar 

  58. Slobodkina, G.B., Kolganova, T.V., Kopitsyn, D.S., Viryasov, M.B., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Dissulfurirhabdus thermomarina gen. nov., sp. nov. a thermophilic, autotrophic, sulfite-reducing and disproportionating deltaproteobacterium isolated from a shallow-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 2515‒2519. https://doi.org/10.1099/ijsem.0.001083

    Article  CAS  PubMed  Google Scholar 

  59. Slobodkina, G.B., Mardanov, A.V., Ravin, N.V., Frolova, A.A., Chernyh, N.A., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Respiratory ammonification of nitrate coupled to anaerobic oxidation of elemental sulfur in deep-sea autotrophic thermophilic bacteria, Front. Microbiol., 2017a, vol. 8, p. 87. https://doi.org/10.3389/fmicb.2017.00087

    Article  PubMed  PubMed Central  Google Scholar 

  60. Slobodkina, G.B., Reysenbach, A.-L., Kolganova, T.V., Novikov, A.A, Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Thermosulfuriphilus ammonigenes gen. nov., sp. nov., a thermophilic, chemolithoautotrophic bacterium capable of respiratory ammonification of nitrate with elemental sulfur, Int. J. Syst. Evol. Microbiol., 2017b, vol. 67, pp. 3474‒3479. https://doi.org/10.1099/ijsem.0.002142

    Article  CAS  PubMed  Google Scholar 

  61. Sorokin, D.Y., Tourova, T.P., Henstra, A.M., Stams, A.J.M., Galinski, E.A., and Muyzer, G., 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 (UK), 2008a, vol. 154, pp. 1444–1453.

    Article  CAS  Google Scholar 

  62. Sorokin, D.Y., Tourova, T.P., Mußmann, M., and Muyzer, G., Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes, Extremophiles, 2008b, vol. 12, pp. 431‒439.

    Article  CAS  Google Scholar 

  63. Sorokin, D.Y., Tourova, T.P., Kolganova, T.V., Detkova, E.N., Galinski, E.A. and Muyzer, G., 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, 2011, vol. 15, pp. 391–401.

    Article  CAS  Google Scholar 

  64. Stockdreher, Y., Venceslau, S.S., Josten, M., Sahl, H.G., Pereira, I.A.C., and Dahl, C., Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC, PLoS One, 2012, vol. 7, no. 7, e40785.

    Article  CAS  Google Scholar 

  65. Tasaki, M., Kamagata, Y., Nakamura, K., and Mikami, E., Isolation and characterization of a thermophilic benzoate-degrading, sulfate-reducing bacterium Desulfotomaculum thermobenzoicum sp. nov., Arch. Microbiol., 1991, vol. 155, pp. 348‒352.

    Article  CAS  Google Scholar 

  66. Thamdrup, B., Finster, K., Hansen, J.W., and Bak, F., Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese, Appl. Environ. Microbiol., 1993, vol. 59, pp. 101–108.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Thauer, R.K., Jungermann, K., and Decker, K., Energy conservation in chemotrophic anaerobic bacteria, Bacteriol. Rev., 1977, vol. 41, pp. 100–180.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Thorup, C., Schramm, A., Findlay, A.J., Finster, K.W., and Schreiber, L., Disguised as a sulfate reducer: growth of the deltaproteobacterium Desulfurivibrio alkaliphilus by sulfide oxidation with nitrate, mBio, 2017, vol. 8, e00671-17. https://doi.org/10.1128/mBio.00671-17

    Article  PubMed  PubMed Central  Google Scholar 

  69. Trubitsyn, D., Geurink, C., Pikuta, E., Lefèvre, C.T., McShan, W.M., Gillaspy, A.F., and Bazylinski, D., Draft genome sequence of the obligately alkaliphilic sulfate-reducing bacterium Desulfonatronum thiodismutans strain MLF1, Genome Announc., 2014, vol. 2, no. 4, e00741-14. https://doi.org/10.1128/genomeA.00741-14

    Article  PubMed  PubMed Central  Google Scholar 

  70. Venceslau, S.S., Stockdreher, Y., Dahl, C., and Pereira, I.A.C., The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism, Biochim. Biophys. Acta, 2014, vol. 1837, pp. 1148–1164.

    Article  CAS  Google Scholar 

  71. Warthmann, R., Vasconcelos, C., Sass, H., and McKenzie, J.A., Desulfovibrio brasiliensis sp. nov., a moderate halophilic sulfate-reducing bacterium from Lagoa Vermelha (Brazil) mediating dolomite formation, Extremophiles, 2005, vol. 9, pp. 255–261.

    Article  CAS  Google Scholar 

  72. Wacey, D., Kilburn, M.R., Saunders, M., Cliff, J. and Brasier, M.D., Microfossils of sulphur-metabolizing cells in 3.4-billion-yearold rocks of Western Australia, Nat. Geosci., 2011, vol. 4, pp. 698–702.

    Article  CAS  Google Scholar 

  73. Wasmund, K., Mußmann, M., and Loy, A., The life sulfuric: microbial ecology of sulfur cycling in marine sediments, Environ. Microbiol. Rep., 2017, vol. 9, pp. 323–344.

    Article  CAS  Google Scholar 

  74. Wegener, G., Krukenberg, V., Ruff, S.E., Kellermann, M.Y., and Knittel, K., Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane, Front. Microbiol., 2016, vol. 7:46. https://doi.org/10.3389/fmicb.2016.00046

    Article  PubMed  PubMed Central  Google Scholar 

  75. Widdel, F. and Pfennig, N., Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. 11. Incomplete oxidation of propionate by Desulfobulbus propionicus gen. nov., sp. nov., Arch. Microbiol., 1982, vol. l31, pp. 360‒365.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. I. Slobodkin.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by P. Sigalevich

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Slobodkin, A.I., Slobodkina, G.B. Diversity of Sulfur-Disproportionating Microorganisms. Microbiology 88, 509–522 (2019). https://doi.org/10.1134/S0026261719050138

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261719050138

Keywords:

Navigation