Skip to main content
SpringerLink
Log in

Relations between Hydrogen and Sulfur Metabolism in Purple Sulfur Bacteria

  • REVIEWS
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract—

The review considers the role of purple sulfur bacteria in the global cycles of hydrogen and sulfur, as well as the ecology and physiology of these bacteria in relation to the metabolism of sulfur and hydrogen. Information is presented on five types of hydrogenases involved in consumption or production of hydrogen, as well as on various enzymes involved in the oxidation/reduction of sulfur compounds. Advances in the biochemistry and genetics of the enzymes from these microorganisms make it possible to analyze the interconnection of processes at a new level.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Appel, J. and Schulz, R., Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?, J. Photochem. Photobiol. B. Biol., 1998, vol. 47, pp. 1‒11.

    Article  CAS  Google Scholar 

  2. Berg, J.S., Pjevac, P., Sommer, T., Buckner, C.R.T., Philippi, M., Hach, P.F., Liebeke, M., Holtappels, M., Danza, F., Tonolla, M., Sengupta, A., Schubert, C.J., Milucka, J., and Kuypers, M.M.M., Dark aerobic sulfide oxidation by anoxygenic phototrophs in anoxic waters, Environ. Microbiol., 2019, vol. 21, pp. 1611‒1626.

    Article  CAS  PubMed  Google Scholar 

  3. Bhatnagar, S., Cowley, E.S., Kopf, S.H., Pérez Castro, S., Kearney, S., Dawson, S.C., Hanselmann, K., and Ruff, S.E., Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom, Environ. Microbiome, 2020, vol. 15, pp. 1‒17. https://doi.org/10.1186/s40793-019-0348-0

    Article  CAS  Google Scholar 

  4. Brugna-Guiral, M., Tron, P., Nitschke, W., Stetter, K.-O., Burlat, B., Guigliarelli, B., Bruschi, M., and Giudici-Orticoni, M.T., [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics, Extremophiles, 2003, vol. 7, pp. 145‒157.

    Article  CAS  PubMed  Google Scholar 

  5. Brune, D.C., Sulfur compounds as photosynthetic electron donors, in Anoxygenic Photosynthetic Bacteria, Blankenship, R.E., Madigan, M.T., and Bauer, C.E., Eds., Advances in Photosynthesis and Respiration, Dordrecht: Springer, 1995, vol. 2, pp. 847‒870.

  6. Bryantseva, I.A., Gorlenko, V.M., Kompantseva, E.I., Imhoff, J.F., Süling, J., and Mityushina, L., Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian soda lake, Int. J. Syst. Evol. Microbiol., 1999, vol. 49, pp. 697‒703.

    Article  Google Scholar 

  7. Calusinska, M., Happe, T., Joris, B., and Wilmotte, A., The surprising diversity of clostridial hydrogenases: a comparative genomic perspective, Microbiology (Reading), 2010, vol. 156, pp. 1575‒1588.

    Article  CAS  PubMed  Google Scholar 

  8. Dahl, C., Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum, Microbiology (Reading), 1996, vol. 142, pp. 3363‒3372.

    Article  CAS  PubMed  Google Scholar 

  9. Dahl, C., Rákhely, G., Pott-Sperling, A.S., Fodor, B., Takács, M., Tóth, A., Kraeling, M., Gyorfi, K., Kovács, A., Tusz, J., and Kovács, K.L., Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria, FEMS Microbiol. Lett., 1999, vol. 180, pp. 317‒324.

    Article  CAS  PubMed  Google Scholar 

  10. Dahl, C., Franz, B., Hensen, D., Kesselheim, A., and Zigann, R., Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process, Microbiology (Reading), 2013, vol. 159, pp. 2626‒2638.

    Article  CAS  PubMed  Google Scholar 

  11. Dahl, C., Cytoplasmic sulfur trafficking in sulfur-oxidizing prokaryotes, IUBMB Life, 2015, vol. 67, pp. 268‒274.

    Article  CAS  PubMed  Google Scholar 

  12. Dahl, C., Sulfur metabolism in phototrophic bacteria, in Modern Topics in the Phototrophic Prokaryotes: Metabolism, Bioenergetics, and Omics, Hallenbeck, P.C., Ed., Cham: Springer Int. Publishing, 2017, pp. 27‒66.

    Google Scholar 

  13. de Wit, R. and van Gemerden, H., Growth and metabolism of the purple sulfur bacterium Thiocapsa roseopersicina under combined light/dark and oxic/anoxic regimens, Arch. Microbiol., 1990, vol. 154, pp. 459‒464.

    Article  CAS  Google Scholar 

  14. Del Don, C., Hanselmann, K.W., Peduzzi, R., and Bachofen, R., Biomass composition and methods for the determination of metabolic reserve polymers in phototrophic sulfur bacteria, Aquat. Sci., 1994, vol. 56, pp. 1‒15.

    Article  Google Scholar 

  15. Dhillon, A., Goswami, S., Riley, M., Teske, A., and Sogin, M., Domain evolution and functional diversification of sulfite reductases, Astrobiology, 2005, vol. 5, pp. 18‒29.

    Article  CAS  PubMed  Google Scholar 

  16. Frigaard, N.U. and Dahl, C., Sulfur metabolism in phototrophic sulfur bacteria, in Advances in Microbial Physiology, Poole, R., Ed., Academic Press, 2008, vol. 54, pp. 103‒200.

  17. Fritsch, J., Lenz, O., and Friedrich, B., The maturation factors HoxR and HoxT contribute to oxygen tolerance of membrane-bound [NiFe] hydrogenase in Ralstonia eutropha H16, J. Bacteriol., 2011, vol. 193, pp. 2487‒2497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Fritsch, J., Lenz, O., and Friedrich, B., Structure, function and biosynthesis of O2-tolerant hydrogenases, Nat. Rev. Microbiol., 2013, vol. 11, pp. 106‒114.

    Article  CAS  PubMed  Google Scholar 

  19. Ghosh, W. and Dam, B., Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea, FEMS Microbiol. Rev., 2009, vol. 33, pp. 999‒1043.

    Article  CAS  PubMed  Google Scholar 

  20. Gorlenko, V.M., Dubinina, G.A., and Kuznetsov, S.I., Ekologiya vodnykh mikroorganismov (Ecology of Aquatic Microorganisms), Moscow: Nauka, 1977.

  21. Grabovich, M.Yu., Involvement of prokaryotes in sulfur cycle, Sorosovskii Obrazovatelnyi Zh., 1999, vol. 12, pp. 16‒20.

    Google Scholar 

  22. Greening, C., Biswas, A., Carere, C.R., Jackson, C.J., Taylor, M.C., Stott, M.B., Cook, G.M., and Morales, S.E., Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival, ISME J., 2016, vol. 10, pp. 761‒777.

    Article  CAS  PubMed  Google Scholar 

  23. Greening, C. and Boyd, E., Editorial: microbial hydrogen metabolism, Front. Microbiol., 2020, vol. 11, art. 56, pp. 1‒4.

  24. Greening, C., Constant, P., Hards, K., Morales, S.E., Oakeshott, J.O., Russell, R.J., Taylor, M.C., Berney, M., Conrad, R., Gregory, M., and Cook, G.M., Atmospheric hydrogen scavenging: from enzymes to ecosystems, Appl. Environ. Microbiol., 2015, vol. 81, pp. 1190‒1199.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Gregersen, L.H., Bryant, D.A., and Frigaard, N.-U., Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria, Front. Microbiol., 2011, vol. 2, art. 116, pp. 1‒14.

  26. Gogotov, I.N., Zorin, N.A., Serebriakova, L.T., and Kondratieva, E.N., The properties of hydrogenase from Thiocapsa roseopersicina, Biochim. Biophys. Acta, 1978, vol. 523, pp. 335–343.

    Article  CAS  PubMed  Google Scholar 

  27. Imhoff, J.F., Family Chromaticeae, in Bergey’s Manual of Systematic Bacteriology, Brenner, D.J., Krieg, N.R., and Staley, J.T., Eds., New York: Springer, 2005, vol. 2, 2nd edn., pp. 3‒9.

    Google Scholar 

  28. Imhoff, J.F., The Family Chromatiaceae, in The Prokaryotes: Gammaproteobacteria, Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F., Eds., Berlin, Heidelberg: Springer, 2014, pp. 151‒178.

    Google Scholar 

  29. Kondrat’eva, E.N., Avtotrofnye prokarioty (Autotrophic Prokaryotes), Moscow: Moscow State Univ., 1996.

  30. Kondrat’eva, E.N. and Gogotov, I.N., Molekulyarnyi vodorod v metabolizme microorganizmov (Molecular Hydrogen in Microbial Metabolism), Moscow: Nauka, 1981.

  31. Kovács, K.L., Fodor, B., Kovács, Á.T., Csanádi, G., Maróti, G., Balogh, J., Arvani, S., and Rákhely, G., Hydrogenases, accessory genes and the regulation of [NiFe] hydrogenase biosynthesis in Thiocapsa roseopersicina, Int. J. Hydrogen Energy, 2002, vol. 27, pp. 1463‒1469.

    Article  Google Scholar 

  32. Kovács, K.L., Kovács, A.T., Maróti, G., Mészáros, L.S., Balogh, J., Latinovics, D., Fülöp, A., Dávid, R., Dorogházi, E., and Rákhely, G., The hydrogenases of Thiocapsa roseopersicina, Biochem. Soc. Trans., 2005a, vol. 33, pp. 61‒63.

    Article  PubMed  Google Scholar 

  33. Kovács, Á.T., Rákhely, G., Balogh, J., Maróti, G., Cournac, L., Carrier, P., Mészáros, L.S., Peltier, G., and Kovács, K.L., Hydrogen independent expression of hupSL genes in Thiocapsa roseopersicina BBS, FEBS J., 2005b, vol. 272, pp. 4807‒4816.

    Article  PubMed  Google Scholar 

  34. Kovács, Á.T., Rákhely, G., Browning, D.F., Fülöp, A., Maróti, G., Busby, S.J., and Kovács, K.L., An FNR-type regulator controls the anaerobic expression of hyn hydrogenase in Thiocapsa roseopersicina, J. Bacteriol., 2005c, vol. 187, pp. 2618‒2627.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Krassilnikova, E.N., Anaerobic metabolism of Thiocapsa roseopersicina in the darkness, Mikrobilologiya, 1976, vol. 45, pp. 372–374.

    Google Scholar 

  36. Laurinavichene, T.V., Rákhely, G., Kovács, K.L., and Tsygankov, A.A., The effect of sulfur compounds on H2 evolution/consumption reactions, mediated by various hydrogenases, in the purple sulfur bacterium, Thiocapsa roseopersicina, Arch. Microbiol., 2007, vol. 188, pp. 403‒410.

    Article  CAS  PubMed  Google Scholar 

  37. Laurinavichene, T., Kitashima, M., Nagashima, K.V.P., Sato, T., Sakurai, H., Inoue, K., and Tsygankov, A., Effect of growth conditions on advantages of hup− strain for H2 photoproduction by Rubrivivax gelatinosus, Int. J. Hydrogen Energy, 2017, vol. 42, pp. 8497‒8504.

    Article  CAS  Google Scholar 

  38. Lenz, O. and Friedrich, B., A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 12474‒12479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Löffler, M., Wallerang, K.B., Venceslau, S.S., Pereira, I.A.C., and Dahl, C., The iron-sulfur flavoprotein DsrL as NAD(P)H:acceptor oxidoreductase in oxidative and reductive dissimilatory sulfur metabolism, Front. Microbiol., 2020, vol. 11, art. 578209, pp. 1‒15.

  40. Long, M., Liu, J., Chen, Z., Bleijlevens, B., Roseboom, W., and Albracht, S.P.J., Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module, J. Biol. Inorg. Chem., 2007, vol. 12, pp. 62–78.

    Article  CAS  PubMed  Google Scholar 

  41. Lovley, D.R. and Goodwin, S., Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments, Geochim. Cosmochim. Acta, 1988, vol. 52, pp. 2993‒3003.

    Article  CAS  Google Scholar 

  42. Luedin, S.M., Pothier, J.F., Danza, F., Storelli, N., Frigaard, N.-U., Wittwer, M., and Tonolla, M., Complete genome sequence of “Thiodictyon syntrophicum” sp. nov. strain Cad16T, a photolithoautotrophic purple sulfur bacterium isolated from the alpine meromictic Lake Cadagno, Stand. Genom. Sci., 2018, vol. 13, pp. 1‒14.

    Google Scholar 

  43. Luedin, S.M., Storelli, N., Danza, F., Roman, S., Wittwer, M., Pothier, J.F., and Tonolla, M., Mixotrophic growth under micro-oxic conditions in the purple sulfur bacterium Thiodictyon syntrophicum, Front. Microbiol., 2019, vol. 10, art. 384, pp. 1‒15.

  44. Ma, K., Schicho, R.N., Kelly, R.M., and Adams, M.W.W., Hydrogenase of the hyperthermophile Pyrococcus furiosus is an elemental sulfur reductase or sulfhydrogenase: evidence for a sulfur-reducing hydrogenase ancestor, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 5341–5344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Madigan, M.T., Anoxygenic phototrophic bacteria from extreme environments, Photosynth. Res., 2003, vol. 76, pp. 157‒171.

    Article  CAS  PubMed  Google Scholar 

  46. Madigan, M.T. and Jung, D.O., An overview of purple bacteria: systematics, physiology, and habitats, in The Purple Phototrophic Bacteria, Hunter, C.N., Daldal, F., Thurnauer, M.C., and Beatty, J.T., Eds., Dordrecht: Springer Netherlands, 2009, pp. 1‒15.

    Google Scholar 

  47. Maróti, G., Fodor, B.D., Rákhely, G., Kovács, Á.T., Arvani, S., and Kovács, K.L., Accessory proteins functioning selectively and pleiotropically in the biosynthesis of [NiFe] hydrogenases in Thiocapsa roseopersicina, Eur. J. Biochem., 2003, vol. 270, pp. 2218‒2227.

    Article  PubMed  Google Scholar 

  48. Maróti, J., Farkas, A., Nagy, I.K., Maróti, G., Kondorosi, E., Rákhely, G., and Kovács, K.L., A second soluble Hox-type NiFe enzyme completes the hydrogenase set in Thiocapsa roseopersicina BBS, Appl. Environ. Micro-biol., 2010, vol. 76, pp. 5113‒5123.

    Article  Google Scholar 

  49. Mas, J. and Van Gemerden, H., Storage products in purple and green sulfur bacteria, in Anoxygenic Photosynthetic Bacteria, Blankenship, R.E., Madigan, M.T., and Bauer, C.E., Eds., Dordrecht: Springer Netherlands, 1995, Ch. 45, pp. 973‒990.

    Google Scholar 

  50. Massé, A., Pringault, O., and de Wit, R., Experimental study of interactions between purple and green sulfur bacteria in sandy sediments exposed to illumination deprived of near-infrared wavelengths, Appl. Environ. Microbiol., 2002, vol. 68, pp. 2972‒2981.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Meyer, B. and Kuever, J., Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5'-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes, Microbiology (Reading), 2007, vol. 153, pp. 3478‒3498.

    Article  CAS  PubMed  Google Scholar 

  52. Meuer, J., Kuettner, H.C., Zhang, J.K., Hedderich, R., and Metcalf, W.W., Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 5632‒5637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Nagy, I.K., Kovács, K.L., Rákhely, G., and Maróti, G., HupO, a novel regulator involved in thiosulfate-responsive control of HupSL [NiFe]-hydrogenase synthesis in Thiocapsa roseopersicina, Appl. Environ. Microbiol., 2016, vol. 82, pp. 2039‒2049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Netrusov, A.I., Bonch-Osmolovskaya, E.A., Gorlen-ko, V.M., Ivanov, M.V., Karavaiko, G.I., Kozhevin, P.A., Kolotilova, N.N., Kotova, I.B., Maksimov, V.N., Nozhevnikova, A.N., Semenov, A.M., Tourova, T.P., and Yudina, T.G., Ekologiya mikroorganismov (Microbial Ecology), Moscow: Yurait, 2013.

  55. Neumann, S., Wynen, A., Trüper, H.G., and Dahl, C., Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway, Mol. Biol. Rep., 2000, vol. 27, pp. 27‒33.

    Article  CAS  PubMed  Google Scholar 

  56. Overmann, J., Mahoney Lake: a case study of the ecological significance of phototrophic sulfur bacteria, in Advances in Microbial Ecology, Jones J.G., Ed., Boston: Springer US, 1997, vol. 15, pp. 251‒288.

    Google Scholar 

  57. Overmann, J. and van Gemerden, H., Microbial interactions involving sulfur bacteria: implications for the ecology and evolution of bacterial communities, FEMS Microbiol. Rev., 2000, vol. 24, pp. 591‒599.

    Article  CAS  PubMed  Google Scholar 

  58. Overmann, J. and Pfennig, N., Continuous chemotrophic growth and respiration of Chromatiaceae species at low oxygen concentrations, Arch. Microbiol., 1992, vol. 158, pp. 59‒67.

    Article  CAS  Google Scholar 

  59. Palágyi-Mészáros, L.S., Maróti, J., Latinovics, D., Ba-logh, T., Klement, E., Medzihradszky, K.F., Rákhely, G., and Kovács, K.L., Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS, FEBS J., 2009, vol. 276, pp. 164‒174.

    Article  PubMed  Google Scholar 

  60. Pattaragulwanit, K., Brune, D.C., Trüper, H.G., and Dahl, C., Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum, Arch. Microbiol., 1998, vol. 169, pp. 434‒444.

    Article  CAS  PubMed  Google Scholar 

  61. Peduzzi, S., Tonolla, 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  PubMed  Google Scholar 

  62. Peters, J.W., Schut, G.J., Boyd, E.S., Mulder, D.W., Shepard, E.M., Broderick, J.B., King, P.W., and Adams, M.W.W., [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation, Biochim. Biophys. Acta– Mol. Cell. Res., 2015, vol. 1853, pp. 1350‒1369.

    CAS  Google Scholar 

  63. Pfennig, N. and Biebl, H., The dissimilatory sulfur-reducing bacteria, in The Prokaryotes, Starr, M.P., Stolp, H., Trüper, H.G., Balows, A., and Schlegel, H.G., Eds., Berlin, Heidelberg: Springer, 1981, pp. 941‒947.

    Google Scholar 

  64. Prange, A., Chauvistré, R., Modrow, H., Hormes, J., Trüper, H.G., and Dahl, C., Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different species of sulfur, Microbiology (Reading), 2002, vol. 148, pp. 267‒276.

    Article  CAS  PubMed  Google Scholar 

  65. Pringault, O., de Wit, R., and Kühl, M., A microsensor study of the interaction between purple sulfur and green sulfur bacteria in experimental benthic gradients, Microb. Ecol., 1999, vol. 37, pp. 173‒184.

    Article  CAS  PubMed  Google Scholar 

  66. Rákhely, G., Colbeau, A., Garin, J., Vignais, P.M., and Kovács, K.L., Unusual organization of the genes coding for HydSL, the stable [NiFe]hydrogenase in the photosynthetic bacterium Thiocapsa roseopersicina BBS, J. Bacteriol., 1998, vol. 180, pp. 1460‒1465.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rákhely, G., Kovács, Á.T., Maróti, G., Fodor, B.D., Csanadi, G., Latinovics, D., and Kovács, K.L., Cyanobacterial-type, heteropentameric, NAD+-reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina, Appl. Environ. Microbiol., 2004, vol. 70, pp. 722‒728.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Rákhely, G., Laurinavichene, T.V., Tsygankov, A.A., and Kovács, K.L., The role of Hox hydrogenase in the H2 metabolism of Thiocapsa roseopersicina, Biochim. Biophys. Acta ‒ Bioenerg., 2007, vol. 1767, pp. 671‒676.

    Google Scholar 

  69. Reinartz, M., Tschäpe, J., Brüser, T., Trüper, H.G., and Dahl, C., Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum, Arch. Microbiol., 1998, vol. 170, pp. 59‒68.

    Article  CAS  PubMed  Google Scholar 

  70. Sander, J. and Dahl, C., Metabolism of inorganic sulfur compounds in purple bacteria, in The Purple Phototrophic Bacteria, Hunter, C.N., Daldal, F., Thurnauer, M.C., and Beatty, J.T., Eds., Dordrecht: Springer Netherlands, 2009, pp. 595‒622.

    Google Scholar 

  71. Schwartz, E., Fritsch, J., and Friedrich, B., H2-metabolizing prokaryotes, in The Prokaryotes: Prokaryotic Physiology and Biochemistry, Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F., Eds., Berlin, Heidelberg: Springer, 2013, pp. 119‒199.

    Google Scholar 

  72. Serebryakova, L.T., Zorin, N.A., and Gogotov, I.N., Isolation and properties of hydrogenase from Rhodopseudomonas capsulata, Biochemistry (Moscow), 1984, vol. 49, pp. 1241‒1247.

    Google Scholar 

  73. Søndergaard, D., Pedersen, C.N.S., and Greening, C., HydDB: a web tool for hydrogenase classification and analysis, Sci. Rep., 2016, vol. 6, art. 34212, pp. 1‒8.

  74. Stockdreher, Y., Sturm, M., Josten, M., Sahl, H.-G., Dobler, N., Zigann, R., and Dahl, C., New proteins involved in sulfur trafficking in the cytoplasm of Allochromatium vinosum, J. Biol. Chem., 2014, vol. 289, pp. 12390‒12403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Tanabe, T.S., Leimkühler, S., and Dahl, C., The functional diversity of the prokaryotic sulfur carrier protein TusA, Adv. Microbial Physiol., 2019, vol. 75, pp. 233‒277.

    Article  CAS  Google Scholar 

  76. Teng, Y., Xu, Y., Wang, X., and Christie, P., Function of biohydrogen metabolism and related microbial communities in environmental bioremediation, Front. Microbiol., 2019, vol. 10, art. 106, pp. 1‒14.

  77. Tengölics, R., Mészáros, L., Győri, E., Doffkay, Z., Kovács, K.L., and Rákhely, G., Connection between the membrane electron transport system and Hyn hydrogenase in the purple sulfur bacterium, Thiocapsa roseopersicina BBS, Biochim. Biophys. Acta‒Bioenerg., 2014, vol. 1837, pp. 1691‒1698.

    Google Scholar 

  78. Tourova, T., Keppen, O.I., Kovaleva, O.L., Slobodova, N.V., Berg, I.A., and Ivanovsky, R., Phylogenetic characterization of the purple sulfur bacterium Thiocapsa sp. BBS by analysis of the 16S rRNA, cbbL, and nifH genes and its description as Thiocapsa bogorovii sp. nov., a new species, Microbiology (Moscow), 2009, vol. 78, pp. 339‒349.

    Article  CAS  Google Scholar 

  79. Truper, H.G., Phototrophic bacteria and their sulfur metabolism, in Sulfur: Its Significance for Chemistry, for the Geo-, Bio- and Cosmosphere and Technology, Müller, A. and Krebs, B., Eds., 1984, vol. 5, pp. 367‒382.

    Google Scholar 

  80. Tsygankov, A.A. and Khusnutdinova, A.N., Hydrogen in metabolism of purple bacteria and prospects of practical application, Microbiology (Moscow), 2015, vol. 84, pp. 1‒22.

    Article  CAS  Google Scholar 

  81. van den Ende, F.P., Laverman, A.M., and van Gemerden, H., Coexistence of aerobic chemotrophic and anaerobic phototrophic sulfur bacteria under oxygen limitation, FEMS Microbiol. Ecol., 1996, vol. 19, pp. 141‒151.

    Article  CAS  Google Scholar 

  82. van Gemerden, H., On the ATP generation by Chromatium in darkness, Arch. Mikrobiol., 1968, vol. 64, pp. 118‒124.

    Article  CAS  PubMed  Google Scholar 

  83. van Gemerden, H. and Mas, J., Ecology of phototrophic sulfur bacteria, in Anoxygenic Photosynthetic Bacteria, Blankenship, R.E., Madigan, M.T., and Bauer, C.E., Eds., Dordrecht: Springer Netherlands, 1995, pp. 49‒85.

    Google Scholar 

  84. van Heerikhuizen, H., Albracht, S.P.J., Slater, E.C., and van Rheenen, P.S., Purification and some properties of the soluble hydrogenase from Chromatium vinosum, Biochim. Biophys. Acta‒Enzymol., 1981, vol. 657, pp. 26‒39.

    Article  CAS  Google Scholar 

  85. Vandieken, V., Finke, N., and Thamdrup, B., Hydrogen, acetate, and lactate as electron donors for microbial manganese reduction in a manganese-rich coastal marine sediment, FEMS Microbiol. Ecol., 2014, vol. 87, pp. 733‒745.

    Article  CAS  PubMed  Google Scholar 

  86. 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‒Bioenerg., 2014, vol. 1837, pp. 1148‒1164.

    Book  Google Scholar 

  87. Vignais, P.M., Regulation of hydrogenase gene expression, in The Purple Phototrophic Bacteria, Hunter, C.N., Daldal, F., Thurnauer, M.C., Beaty, J.T., Eds., Dordrecht: Springer Science+Business Media B.V., 2009, pp. 743‒757.

  88. Vignais, P.M. and Billoud, B., Occurrence, classification, and biological function of hydrogenases: an overview, Chem. Rev., 2007, vol. 107, pp. 4206‒4272.

    Article  CAS  PubMed  Google Scholar 

  89. Vignais, P.M., Billoud, B., and Meyer, J., Classification and phylogeny of hydrogenases, FEMS Microbiol. Rev., 2001, vol. 25, pp. 455–501.

    Article  CAS  PubMed  Google Scholar 

  90. Visscher, P.T., van den Ende, F.P., Schaub, B.E.M., and van Gemerden, H., Competition between anoxygenic phototrophic bacteria and colorless sulfur bacteria in a microbial mat, FEMS Microbiol. Lett., 1992, vol. 101, pp. 51‒58.

    Article  CAS  Google Scholar 

  91. Volbeda, A., Darnault, C., Parkin, A., Sargent, F., Armstrong, F.A., and Fontecilla-Camps, J.C., Crystal structure of the O2-tolerant membrane-bound hydrogenase 1 from Escherichia coli in complex with its cognate cytochrome b, Structure, 2013, vol. 21, pp. 184‒190.

    Article  CAS  PubMed  Google Scholar 

  92. Weissgerber, T., Dobler, N., Polen, T., Latus, J., Stockdreher, Y., and Dahl, C., Genome-wide transcriptional profiling of the purple sulfur bacterium Allochromatium vinosum DSM 180T during growth on different reduced sulfur compounds, J. Bacteriol., 2013, vol. 195, pp. 4231‒4245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Weissgerber, T., Sylvester, M., Kröninger, L., and Dahl, C., A comparative quantitative proteomic study identifies new proteins relevant for sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum, Appl. Environ. Microbio-l., 2014a, vol. 80, pp. 2279‒2292.

    Article  Google Scholar 

  94. Weissgerber, T., Watanabe, M., Hoefgen, R., and Dahl, C., Metabolomic profiling of the purple sulfur bacterium Allochromatium vinosum during growth on different reduced sulfur compounds and malate, Metabolomics, 2014b, vol. 10, pp. 1094‒1112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Weissgerber, T., Zigann, R., Bruce, D., Chang, Y.-J., Detter, J.C., Han, C., Hauser, L., Jeffries, C.D., Land, M., Munk, A.C., Tapia, R., and Dahl, C., Complete genome sequence of Allochromatium vinosum DSM 180(T), Stand. Genomic Sci., 2011, vol. 5, pp. 311‒330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Welte, C., Hafner, S., Krätzer, C., Quentmeier, A., Friedrich, C.G., and Dahl, C., Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation, FEBS Lett., 2009, vol. 583, pp. 1281‒1286.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was financially supported by the Russian Science Foundation, project no. 19-14-00255.

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems, Russian Academy of Sciences, 142290, Pushchino, Russia

    M. K. Khasimov, T. V. Laurinavichene, E. P. Petushkova & A. A. Tsygankov

Authors
  1. M. K. Khasimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. V. Laurinavichene
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. P. Petushkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. A. Tsygankov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Tsygankov.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by D. Timchenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khasimov, M.K., Laurinavichene, T.V., Petushkova, E.P. et al. Relations between Hydrogen and Sulfur Metabolism in Purple Sulfur Bacteria. Microbiology 90, 543–557 (2021). https://doi.org/10.1134/S0026261721050106

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721050106

Keywords:

Search

Navigation