Sulfur metabolisms in epsilon-and gamma-proteobacteria in deep-sea hydrothermal fields

Frontiers in Microbiology

Volumn 2, Issue SEP, 2011, Pages

  Yamamoto, Masahiro ^a   Takai, Ken ^a  

^a JAPAN AGENCY FOR MARINE EARTH SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Chemoautotroph; Deep sea hydrothermal vents; Energy metabolism

Indexed keywords

EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; PROTEOBACTERIA;

EID: 84865988318     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00192     Document Type: Review

References (65)

1. Arp, A. J., and Childress, J. J. (1983). Sulfide binding by the blood of the hydrothermal vent tube worm Riftia pachyptila. Science 219, 295-297.
2. Campbell, B. J., Engel, A. S., Porter, M. L., and Takai, K. (2006). The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4, 458-468.
3. Campbell, B. J., Jeanthon, C., Kostka, J. E., Luther, G. W. III, and Cary, S. C. (2001). Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Appl. Environ. Microbiol. 67, 4566-4572.
4. Campbell, B. J., Smith, J. L., Hanson, T. E., Klotz, M. G., Stein, L. Y., Lee, C. K., Wu, D., Robinson, J. M., Khouri, H. M., Eisen, J. A., and Cary, S. C. (2009). Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet. 5, e1000362. doi: 10.1371/journal.pgen.1000362
5. Chan, L. K., Morgan-Kiss, R. M., and Hanson, T. E. (2009). Functional analysis of three sulfide:quinone oxidoreductase homologs in Chlorobaculum tepidum. J. Bacteriol. 191, 1026-1034.
6. Dubilier, N., Bergin, C., and Lott, C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725-740.
7. Durand, P., Reysenbach, A.-L., Prieur, D., and Pace, N. (1993). Isolation and characterization of Thiobacillus hydrothermalis sp. nov., a mesophilic obligately chemolithotrophic bacterium isolated from a deep-sea hydrothermal vent in Fiji Basin. Arch. Microbiol. 159, 39-44.
8. Emerson, D., Rentz, J. A., Lilburn, T. G., Davis, R. E., Aldrich, H., Chan, C., and Moyer, C. L. (2007). A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE 2, e667. doi: 10.1371/journal. pone.0000667
9. Friedrich, C. G. (1998). Physiology and genetics of sulfur-oxidizing bacteria. Adv. Microb. Physiol. 39, 235-289.
10. Friedrich, C. G., Bardischewsky, F., Rother, D., Quentmeier, A., and Fischer, J. (2005). Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8, 253-259.
11. Friedrich, C. G., Quentmeier,A., Bardischewsky, F., Rother, D., Orawski, G., Hellwig, P., and Fischer, J. (2008). Redox control of chemotrophic sulfur oxidation of Paracoccus pantotrophus," i n Microbial Sulfur Metabolism, eds C. Dahl and C. G. Friedrich (Heidelberg: Springer), 139-150.
12. Friedrich, C. G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001). Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl. Environ. Microbiol. 67, 2873-2882.
13. Frigaard, N. U., and Dahl, C. (2009). Sulfur metabolism in phototrophic sulfur bacteria. Adv. Microb. Physiol. 54, 103-200.
14. Ghosh, W., and Dam, B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol. Rev. 33, 999-1043.
15. Gregersen, L. H., Bryant, D. A., and Frigaard, N. U. (2011). Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front. Microbiol. 2:116. doi: 10.3389/fmicb.2011.00116
16. Grzymski, J. J., Murray, A. E., Campbell, B. J., Kaplarevic, M., Gao, G. R., Lee, C., Daniel, R., Ghadiri, A., Feldman, R. A., and Cary, S. C. (2008). Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility. Proc. Natl. Acad. Sci. U.S.A. 105, 17516-17521.
17. Hedderich, R., Klimmek, O., Kroger, A., Dirmeier, R., Keller, M., and Stetter, K. O. (1999). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol. Rev. 22, 353-381.
18. Holkenbrink, C., Ocon Barbas, S., Mellerup,A., Otaki, H., and Frigaard, N. U. (2011). Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system. Microbiology 157, 1229-1239.
19. Hügler, M., Gartner, A., and Imhoff, J. F. (2010). Functional genes as markers for sulfur cycling and CO2 fixation in microbial communities of hydrothermal vents of the Logatchev field. FEMS. Microbiol. Ecol. 73, 526-537.
20. Inagaki, F., Takai, K., Kobayashi, H., Nealson, K. H., and Horikoshi, K. (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfuroxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53, 1801-1805.
21. Inagaki, F., Takai, K., Nealson, K. H., and Horikoshi, K. (2004). Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int. J. Syst. Evol. Microbiol. 54, 1477-1482.
22. Jannasch, H. W., and Mottl, M. J. (1985). Geomicrobiology of deepsea hydrothermal vents. Science 229, 717-725.
23. Jeanthon, C. (2000). Molecular ecology of hydrothermal vent microbial communities. Antonie Van Leeuwenhoek 77, 117-133.
24. Kappler, U., and Dahl, C. (2001). Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol. Lett. 203, 1-9.
25. Kletzin, A., Urich, T., Muller, F., Bandeiras, T. M., and Gomes, C. M. (2004). Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J. Bioenerg. Biomembr. 36, 77-91.
26. Kuever, J., Sievert, S. M., Stevens, H., Brinkhoff, T., and Muyzer, G. (2002). Microorganisms of the oxidative and reductive part of the sulphur cycle at a shallow-water hydrothermal vent in the Aegean Sea (Milos, Greece). Cah. Biol. Mar. 43, 413-416.
27. Kusai, K., and Yamanaka, T. (1973). The oxidation mechanisms of thiosulphate and sulphide in Chlorobium thiosulphatophilum: roles of cytochrome c-551 and cytochrome c-553. Biochim. Biophys. Acta 325, 304-314.
28. Kuwahara, H., Yoshida, T., Takaki, Y., Shimamura, S., Nishi, S., Harada, M., Matsuyama, K., Takishita, K., Kawato, M., Uematsu, K., Fujiwara, Y., Sato, T., Kato, C., Kitagawa, M., Kato, I., and Maruyama, T. (2007). Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr. Biol. 17, 881-886.
29. Kvenvolden, K. A., Weliky, K., Nelson, H., and Marais, D. J. (1979). Submarine seep of carbon dioxide in Norton sound, Alaska. Science 205, 1264-1266.
30. Marcia, M., Ermler, U., Peng, G. H., and Michel, H. (2010). A new structure-based classification of sulfide: quinone oxidoreductases. Proteins 78, 1073-1083.
31. McCollom, T. M., and Shock, E. L. (1997). Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta. 61, 4375-4391.
32. Muyzer, G., and Stams, A. J. (2008). The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6, 441-454.
33. Mußmann, M., Hu, F. Z., Richter, M., De Beer, D., Preisler,A., Jorgensen, B. B. Huntemann, M., Glöckner, F. O., Amann, R., Koopman, W. J., Lasken, R. S., Janto, B., Hogg, J., Stoodley, P., Boissy, R., and Ehrlich, G. D. (2007). Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol. 5, e230. doi: 10.1371/journal. 0050230
34. Nakagawa, S., and Takai, K. (2008). Deep-sea vent chemoautotrophs:diversity, biochemistry and ecological significance. FEMS. Microbiol. Ecol. 65, 1-14.
35. Nakagawa, S., Takai, K., Inagaki, F., Hirayama, H., Nunoura, T., Horikoshi, K., and Sako, Y. (2005). Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ. Microbiol. 7, 1619-1632.
36. Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A. L., Takai, K., and Horikoshi, K. (2007). Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc. Natl. Acad. Sci. U.S.A. 104, 12146-12150.
37. Nealson, K. H., Inagaki, F., and Takai, K. (2005). Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? Trends Microbiol. 13, 405-410.
38. Nelson, D. C., and Castenholz, R. W. (1981). Use of reduced sulfurcompounds by Beggiatoa sp. J. Bacteriol. 147, 140-154.
39. Newton, I. L., Woyke, T., Auchtung, T. A., Dilly, G. F., Dutton, R. J., Fisher, M. C.Fontanez,K. M., Lau, E., Stewart, F. J., Richardson, P. M., Barry, K. W., Saunders, E., Detter, J. C., Wu, D., Eisen, J. A., and Cavanaugh, C. M. (2007). The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315, 998-1000.
40. Numoto, N., Nakagawa, T., Kita, A., Sasayama, Y., Fukumori, Y., and Miki, K. (2005). Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi. Proc. Natl. Acad. Sci. U.S.A. 102, 14521-14526.
41. Ohoka, H., and Blankenship, R. E. (2004). Green bacteria: secondary electron donor (cytochromes), in Encyclopedia of Biological Chemistry, eds W. J. Lennarz and M. D. Lane (Boston, MA: Elsevier), 321-324.
42. Pfennig, N., and Biebel, H. (1986). The dissimilatory sulfate-reducing bacteria," in The Prokaryotes: A Handbook on Habitats, Isolation and Identification of Bacteria, ed. M. P. Starr (Heidelberg: Springer), 928-940.
43. Reinartz, M., Tschape, J., Bruser, T., Truper, H. G., and Dahl, C. (1998). Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch. Microbiol. 170, 59-68.
44. Reysenbach, A. L., Gotz, D., Banta, A., Jeanthon, C., and Fouquet,Y. (2002). Expanding the distribution of the Aquificales to the deep-sea vents on Mid-Atlantic Ridge and Central Indian Ridge. Cah. Biol. Mar. 43, 425-428.
45. Reysenbach, A. L., Longnecker, K., and Kirshtein, J. (2000). Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic Ridge hydrothermal vent. Appl. Environ. Microbiol. 66, 3798-3806.
46. Robidart, J. C., Bench, S. R., Feldman, R. A., Novoradovsky,A., Podell, S. B., Gaasterland, T., Allen, E. E., and Felbeck, H. (2008). Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727-737.
47. Schmidt, T. M., Arieli, B., Cohen, Y., Padan, E., and Strohl, W. R. (1987). Sulfur metabolism in Beggiatoa alba. J. Bacteriol. 169, 5466-5472.
48. Scott, K. M., Sievert, S. M., Abril, F. N., Ball, L. A., Barrett, C. J., Blake, R. A., Boller, A. J., Chain, P. S., Clark, J. A., Davis, C. R., Detter, C., Do, K. F., Dobrinski, K. P., Faza, B. I., Fitzpatrick, K. A., Freyermuth, S. K., Harmer, T. L., Hauser, L. J., Hügler, M., Kerfeld, C. A., Klotz, M. G., Kong, W. W., Land, M., Lapidus, A., Larimer, F. W., Longo, D. L., Lucas, S., Malfatti, S. A., Massey, S. E., Martin, D. D., McCuddin, Z., Meyer, F., Moore, J. L., Ocampo, L. H. Jr., Paul, J. H., Paulsen, I. T., Reep, D. K., Ren, Q., Ross, R. L., Sato, P. Y., Thomas, P., Tinkham, L. E., and Zeruth, G. T. (2006). The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol. 4, e383. doi: 10.1371/journal. pbio.0040383
49. Shahak,Y., and Hauska,G. (2008). Sulfide oxidation from cyanobacteria to humans: sulfide-quinone oxidoreductase (SQR)," in Sulfur Metabolism in Phototrophic Organisms, eds R. Hell, C. Dahl, D. B. Knaff, and T. Leustek (Dordrecht: Springer), 319-335.
50. Sievert, S. M., Scott, K. M., Klotz, M. G., Chain, P. S. G., Hauser, L. J., Hemp, J,. Hügler, M., Land, M., Lapidus, A., Larimer, F. W., Lucas, S., Malfatti, S. A., Meyer, F., Paulsen, I. T., Ren, Q., Simon, J., (2008) and USF Genomics Class. Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol. 74, 1145-1156.
51. Stewart, F. J., Newton, I. L., and Cavanaugh, C. M. (2005). Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces. Trends Microbiol. 13, 439-448.
52. Suzuki, Y., Sasaki, T., Suzuki, M., Nogi, Y., Miwa, T., Takai, K., Nealson, K. H., and Horikoshi, K. (2005). Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermalvent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl. Environ. Microbiol. 71, 5440-5450.
53. Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., Hirayama, H., Nakagawa, S., Suzuki, Y., Inagaki, F., and Horikoshi, K. (2005). Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl. Environ. Microbiol. 71, 7310-7320.
54. Takai, K., Gamo, T., Tsunogai, U., Nakayama, N., Hirayama, H., Nealson, K. H., and Horikoshi, K. (2004). Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 8, 269-282.
55. Takai, K., Kobayashi, H., Nealson, K. H., and Horikoshi, K. (2003a). Deferribacter desulfuricans sp. nov., a novel sulfur-, nitrate-and arsenatereducing thermophile isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 53, 839-846.
56. Takai, K., Inagaki, F., Nakagawa, S., Hirayama, H., Nunoura, T., Sako, Y., Nealson, K. H., and Horikoshi, K. (2003b). Isolation and phylogenetic diversity of members of previously uncultivated epsilon-proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol. Lett. 218, 167-174.
57. Takai, K., Miyazaki, M., Hirayama, H., Nakagawa, S., Querellou, J., and Godfroy, A. (2009). Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ. Microbiol. 11, 1983-1997.
58. Takai, K., Nakagawa, S., Reysenbach, A.-L., and Hoek, J. (2006). Microbial ecology of mid-ocean ridges and back-arc basins. Geophys. Monogr. Ser. 166, 185-213.
59. Takai, K., Nakamura, K., Suzuki, K., Inagaki, F., Nealson, K. H., and Kumagai, H. (2006). Ultramafics-Hydrothermalism-Hydrogenesis-HyperSLiME (UltraH3) linkage: a key insight into early microbial ecosystem in the Archean deep-sea hydrothermal systems. Paleontol. Res. 10, 269-282.
60. Takai, K., Miyazaki, M., Nunoura, T., Hirayama, H., Oida, H., Furushima, Y., Yamamoto, H., and Horikoshi, K. (2006). Sulfurivirga caldicuralii gen. nov., sp. nov., a novel microaerobic, thermophilic, thiosulfate-oxidizing chemolithoautotroph, isolated from a shallow marine hydrothermal system occurring in a coral reef, Japan. Int. J. Syst. Evol. Microbiol. 56, 1921-1929.
61. Teske, A., Hinrichs, K. U., Edgcomb, V., de Vera Gomez, A., Kysela, D., Sylva, S. P., Sogin, M. L., and Jannasch, H. W. (2002). Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol. 68, 1994-2007.
62. Urakawa, H., Dubilier, N., Fujiwara, Y., Cunningham, D. E., Kojima, S., and Stahl, D. A. (2005). Hydrothermal vent gastropods from the same family (Provannidae) harbour epsilon-and gammaproteobacterial endosymbionts. Environ. Microbiol. 7, 750-754.
63. Wolin, M. J., Wolin, E. A., and Jacobs, N. J. (1961). Cytochrome-producing anaerobic Vibrio succinogenes, sp. n. J. Bacteriol. 81, 911-917.
64. Yamamoto, M., Nakagawa, S., Shimamura, S., Takai, K., and Horikoshi, K. (2010). Molecular characterization of inorganic sulfur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environ. Microbiol. 12, 1144-1153.
65. Zal, F., Leize, E., Lallier, F. H., Toulmond, A., Van Dorsselaer, A., and Childress, J. J. (1998). S-Sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc. Natl. Acad. Sci. U.S.A. 95, 8997-9002.