The globally widespread genus Sulfurimonas: Versatile energy metabolisms and adaptations to redox clines

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Han, Yuchen ^a   Perner, Mirjam ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Horizontal gene transfer; Hydrogen metabolism; Sulfur metabolism; Sulfurimonas; Versatile metabolism

Indexed keywords

HYDROGEN; HYDROGENASE; HYDROLASE; NITROGEN; OXIDOREDUCTASE; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SULFIDE; SULFITE DEHYDROGENASE; SULFUR;

ADAPTATION; CARBON DIOXIDE FIXATION; CHEMOAUTOTROPHY; ENERGY METABOLISM; EPSILONPROTEOBACTERIA; HABITAT; HORIZONTAL GENE TRANSFER; HUMAN; NONHUMAN; OXIDATION; POLYMERASE CHAIN REACTION; REVIEW; SULFURIMONAS;

EID: 84946739086     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00989     Document Type: Review

References (103)

1. Akerman, N. H., Butterfield, D. A., and Huber, J. A. (2013). Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front. Microbiol. 4:185. doi: 10.3389/fmicb.2013.00185
2. Bertini, I., Cavallaro, G., and Rosato, A. (2005). Cytochrome c: occurrence and functions. Chem. Rev. 106, 90-115. doi: 10.1021/cr050241v
3. Brettar, I., Labrenz, M., Flavier, S., Bötel, J., Kuosa, H., Christen, R., et al. (2006). Identification of a Thiomicrospira denitrificans-like Epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea. Appl. Environ. Microbiol. 72, 1364-1372. doi: 10.1128/AEM.72.2.1364-1372.2006
4. Brettar, I., and Rheinheimer, G. (1992). Influence of carbon availability on denitrification in the central Baltic Sea. Limnol. Oceanogr. 37, 1146-1163. doi: 10.4319/lo.1992.37.6.1146
5. Brito, J. A., Sousa, F. L., Stelter, M., Bandeiras, T. M., Vonrhein, C., Teixeira, M., et al. (2009). Structural and functional insights into sulfide:quinone oxidoreductase. Biochemistry 48, 5613-5622. doi: 10.1021/bi9003827
6. Brugna-Guiral, M., Tron, P., Nitschke, W., Stetter, K.-O., Burlat, B., Guigliarelli, B., et al. (2003). [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics. Extremophiles 7, 145-157.
7. Cai, L., Shao, M.-F., and Zhang, T. (2014). Non-contiguous finished genome sequence and description of Sulfurimonas hongkongensis sp. nov., a strictly anaerobic denitrifying, hydrogen-and sulfur-oxidizing chemolithoautotroph isolated from marine sediment. Stand. Genomic Sci. 9, 1302-1310. doi: 10.4056/sigs.4948668
8. Campbell, B. J., and Cary, S. C. (2004). Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal Vents. Appl. Environ. Microbiol. 70, 6282-6289. doi: 10.1128/AEM.70.10.6282-6289.2004
9. 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. doi: 10.1038/nrmicro1414
10. Campbell, B. J., Smith, J. L., Hanson, T. E., Klotz, M. G., Stein, L. Y., Lee, C. K., et al. (2009). Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet. 5:e1000362. doi: 10.1371/journal.pgen.1000362
11. 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. doi: 10.1128/JB.01154-08
12. Ducluzeau, A.-L., Ouchane, S., and Nitschke, W. (2008). The cbb3 oxidases are an ancient innovation of the domain bacteria. Mol. Biol. Evol. 25, 1158-1166. doi: 10.1093/molbev/msn062
13. Engel, A. S., Porter, M. L., Stern, L. A., Quinlan, S., and Bennett, P. C. (2004). Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic "Epsilonproteobacteria". FEMS Microbiol. Ecol. 51, 31-53. doi: 10.1016/j.femsec.2004.07.004
14. Fisher, C. R., Takai, K., and Le Bris, N. (2007). Hydrothermal vent ecosystems. Oceanography 20, 14-23. doi: 10.5670/oceanog.2007.75
15. Foster, B. A., Thomas, S. M., Mahr, J. A., Renosto, F., Patel, H. C., and Segel, I. H. (1994). Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum. Identification of a likely allosteric domain. J. Biol. Chem. 269, 19777-19786.
16. Frias-Lopez, J., Zerkle, A. L., Bonheyo, G. T., and Fouke, B. W. (2002). Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl. Environ. Microbiol. 68, 2214-2228. doi: 10.1128/AEM.68.5.2214-2228.2002
17. Friedrich, C. G., Bardischewsky, F., Rother, D., Quentmeier, A., and Fischer, J. (2005). Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8, 253-259. doi: 10.1016/j.mib.2005.04.005
18. Frigaard, N.-U., and Dahl, C. (2008). "Sulfur metabolism in phototrophic sulfur bacteria," in Advances in Microbial Physiology, Vol. 54, ed. K. P. Robert (Waltham, MA: Academic Press), 103-200.
19. Gevertz, D., Telang, A. J., Voordouw, G., and Jenneman, G. E. (2000). Isolation and characterization of strains CVO and FWKO B, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Appl. Environ. Microbiol. 66, 2491-2501. doi: 10.1128/AEM.66.6.2491-2501.2000
20. Giovannelli, D., Ferriera, S., Johnson, J., Kravitz, S., Pérez-Rodríguez, I., Ricci, J., et al. (2011). Draft genome sequence of Caminibacter mediatlanticus strain TB-2T, an epsilonproteobacterium isolated from a deep-sea hydrothermal vent. Stand. Genomic Sci. 5, 135-143. doi: 10.4056/sigs.2094859
21. Glaubitz, S., Lueders, T., Abraham, W.-R., Jost, G., Jürgens, K., and Labrenz, M. (2009). 13C-isotope analyses reveal that chemolithoautotrophic Gamma-and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ. Microbiol. 11, 326-337. doi: 10.1111/j.1462-2920.2008.01770.x
22. Gleeson, D. F., Williamson, C., Grasby, S. E., Pappalardo, R. T., Spear, J. R., and Templeton, A. S. (2011). Low temperature S0 biomineralization at a supraglacial spring system in the Canadian High Arctic. Geobiology 9, 360-375. doi: 10.1111/j.1472-4669.2011.00283.x
23. Golovacheva, R., and Karavaiko, G. (1977). [Sulfobacillus, a new genus of thermophilic sporulating bacteria]. Mikrobiologiia 47, 815-822.
24. Grabowski, A., Nercessian, O., Fayolle, F., Blanchet, D., and Jeanthon, C. (2005). Microbial diversity in production waters of a low-temperature biodegraded oil reservoir. FEMS Microbiol. Ecol. 54, 427-443. doi: 10.1016/j.femsec.2005.05.007
25. Griesbeck, C., Hauska, G., and Schütz, M. (2000). "Biological sulfide oxidation: sulfide-quinone reductase (SQR), the primary reaction," in Recent Research Developments in Microbiology, Vol. 4, ed. S. G. Pandalai (Trivadrum: Research Signpost), 179-203.
26. Groenendaal, M. (1979). On sulphide and the distribution of Arenicola marina in a tidal mud flat in the Dutch Wadden Sea. Net. J. Sea Res. 13, 562-570. doi: 10.1016/0077-7579(79)90026-7
27. Grote, J., Jost, G., Labrenz, M., Herndl, G. J., and Jurgens, K. (2008). Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl. Environ. Microbiol. 74, 7546-7551. doi: 10.1128/AEM.01186-08
28. Grote, J., Schott, T., Bruckner, C. G., Glockner, F. O., Jost, G., Teeling, H., et al. (2012). Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. Proc. Natl. Acad. Sci. U.S.A. 109, 506-510. doi: 10.1073/pnas.1111262109
29. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. doi: 10.1080/10635150390235520
30. Hamilton, T. L., Jones, D. S., Schaperdoth, I., and Macalady, J. L. (2014). Metagenomic insights into S(0) precipitation in a terrestrial subsurface lithoautotrophic ecosystem. Front. Microbiol. 5:756. doi: 10.3389/fmicb.2014.00756
31. Han, C., Kotsyurbenko, O., Chertkov, O., Held, B., Lapidus, A., Nolan, M., et al. (2012). Complete genome sequence of the sulfur compounds oxidizing chemolithoautotroph Sulfuricurvum kujiense type strain (YK-1T). Stand. Genomic Sci. 6, 94-103. doi: 10.4056/sigs.2456004
32. Han, Y., and Perner, M. (2014). The role of hydrogen for Sulfurimonas denitrificans' metabolism. PLoS ONE 9:e106218. doi: 10.1371/journal.pone.0106218
33. Headd, B., and Summers Engel, A. (2014). Biogeographic congruency among bacterial communities from terrestrial sulfidic springs. Front. Microbiol. 5:473. doi: 10.3389/fmicb.2014.00473
34. Hedderich, R., Klimmek, O., Kröger, A., Dirmeier, R., Keller, M., and Stetter, K. O. (1998). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol. Rev. 22, 353-381. doi: 10.1021/bi3014399
35. Henneberger, R.M. (2008). The Microbial Diversity and Ecology of Selected Andesitic Hydrothermal Environment. Ph.D. thesis, Macquarie University, Sydney, NSW.
36. Hubert, C. R. J., Oldenburg, T. B. P., Fustic, M., Gray, N. D., Larter, S. R., Penn, K., et al. (2012). Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil. Environ. Microbiol. 14, 387-404. doi: 10.1111/j.1462-2920.2011.02521.x
37. Hügler, M., Petersen, J. M., Dubilier, N., Imhoff, J. F., and Sievert, S. M. (2011). Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS ONE 6:e16018. doi: 10.1371/journal.pone.0016018
38. Hügler, M., Wirsen, C. O., Fuchs, G., Taylor, C. D., and Sievert, S. M. (2005). Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the e subdivision of proteobacteria. J. Bacteriol. 187, 3020-3027. doi: 10.1128/JB.187.9.3020-3027.2005
39. Inagaki, F., Takai, K., Kobayashi, H., Nealson, K. H., and Horikoshi, K. (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing e-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53, 1801-1805. doi: 10.1099/ijs.0.02682-0
40. Jansen, S., Walpersdorf, E., Werner, U., Billerbeck, M., Böttcher, M., and De Beer, D. (2009). Functioning of intertidal flats inferred from temporal and spatial dynamics of O2, H2S and pH in their surface sediment. Ocean Dynam. 59, 317-332.
41. Kappler, U., and Dahl, C. (2001). Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol. Lett. 203, 1-9. doi: 10.1111/j.1574-6968.2001.tb10813.x
42. Kiehlbauch, J., Brenner, D., Nicholson, M., Baker, C., Patton, C., Steigerwalt, A., et al. (1991). Campylobacter butzleri sp. nov. isolated from humans and animals with diarrheal illness. J. Clin. Microbiol. 29, 376-385.
43. Kodama, Y., and Watanabe, K. (2003). Isolation and characterization of a sulfur-oxidizing chemolithotroph growing on crude oil under anaerobic conditions. Appl. Environ. Microbiol. 69, 107-112. doi: 10.1128/AEM.69.1.107-112.2003
44. Kodama, Y., and Watanabe, K. (2004). Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int. J. Syst. Evol. Microbiol. 54, 2297-2300. doi: 10.1099/ijs.0.63243-0
45. Labrenz, M., Grote, J., Mammitzsch, K., Boschker, H. T., Laue, M., Jost, G., et al. (2013). Sulfurimonas gotlandica sp. nov., a chemoautotrophic and psychrotolerant epsilonproteobacterium isolated from a pelagic redoxcline, and an emended description of the genus Sulfurimonas. Int. J. Syst. Evol. Microbiol. 63, 4141-4148. doi: 10.1099/ijs.0.048827-0
46. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., Mcgettigan, P. A., Mcwilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948. doi: 10.1093/bioinformatics/btm404
47. Li, B., Chen, Y., Liu, Q., Hu, S., and Chen, X. (2011). Complete genome analysis of Sulfobacillus acidophilus strain TPY, isolated from a hydrothermal vent in the Pacific ocean. J. Bacteriol. 193, 5555-5556. doi: 10.1128/JB.05684-11
48. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, A., et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi: 10.1093/nar/gkh293
49. Mammitzsch, K., Jost, G., and Jürgens, K. (2014). Impact of dissolved inorganic carbon concentrations and pH on growth of the chemolithoautotrophic epsilonproteobacterium Sulfurimonas gotlandica GD1T. MicrobiologyOpen 3, 80-88. doi: 10.1002/mbo3.153
50. Marchal, K., Sun, J., Keijers, V., Haaker, H., and Vanderleyden, J. (1998). A cytochrome cbb3 (Cytochrome c) terminal oxidase in Azospirillum brasilense Sp7 supports microaerobic growth. J. Bacteriol. 180, 5689-5696.
51. Marcia, M., Ermler, U., Peng, G., and Michel, H. (2009). The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc. Natl. Acad. Sci. U.S.A. 106, 9625-9630. doi: 10.1073/pnas.0904165106
52. Marcia, M., Ermler, U., Peng, G., and Michel, H. (2010). A new structure-based classification of sulfide:quinone oxidoreductases. Proteins 78, 1073-1083. doi: 10.1002/prot.22665
53. McClung, C. R., Patriquin, D. G., and Davis, R. E. (1983). Campylobacter nitrofigilis sp. nov., a nitrogen-fixing bacterium associated with roots of Spartina alterniflora Loisel. Int. J. Syst. Bacteriol. 33, 605-612. doi: 10.1099/00207713-33-3-605
54. Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R., and Metcalf, W. W. (2002). 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. U.S.A. 99, 5632-5637. doi: 10.1073/pnas.072615499
55. Meyer, J. L., and Huber, J. A. (2014). Strain-level genomic variation in natural populations of Lebetimonas from an erupting deep-sea volcano. ISME J. 8, 867-880. doi: 10.1038/ismej.2013.206
56. Miller, W. G., Parker, C. T., Rubenfield, M., Mendz, G. L., Wösten, M. M. S. M., Ussery, D. W., et al. (2007). The complete genome sequence and analysis of the Epsilonproteobacterium Arcobacter butzleri. PLoS ONE 2:e1358. doi: 10.1371/journal.pone.0001358
57. Mouncey, N. J., and Kaplan, S. (1998). Oxygen regulation of the ccoN gene encoding a component of the cbb3 oxidase in Rhodobacter sphaeroides 2.4.1T: involvement of the FnrL Protein. J. Bacteriol. 180, 2228-2231.
58. Nakagawa, S., Takai, K., Inagaki, F., Chiba, H., Ishibashi, J.-I., Kataoka, S., et al. (2005a). Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol. Ecol. 54, 141-155. doi: 10.1016/j.femsec.2005.03.007
59. Nakagawa, S., Takai, K., Inagaki, F., Hirayama, H., Nunoura, T., Horikoshi, K., et al. (2005b). Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ. Microbiol. 7, 1619-1632. doi: 10.1111/j.1462-2920.2005.00856.x
60. Nakagawa, S., Takai, K., Inagaki, F., Horikoshi, K., and Sako, Y. (2005c). Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the epsilon-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 55, 925-933. doi: 10.1099/ijs.0.63480-0
61. Nakagawa, S., and Takaki, Y. (2009). "Nonpathogenic Epsilonproteobacteria," in Ecyclopedia of Life Sciences. Chichester: John Wiley & Sons, Ltd. doi: 10.1002/9780470015902.a0021895
62. Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A. L., Takai, K., and Horikoshi, K. (2007). Deep-sea vent e-proteobacterial genomes provide insights into emergence of pathogens. Proc. Natl. Acad. Sci. U.S.A. 104, 12146-12150. doi: 10.1073/pnas.0700687104
63. Neumann, S., Wynen, A., Trüper, H., and Dahl, C. (2000). Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway. Mol. Biol. Rep. 27, 27-33. doi: 10.1023/A:1007058421714
64. Noguchi, K., Riggins, D. P., Eldahan, K. C., Kitko, R. D., and Slonczewski, J. L. (2010). Hydrogenase-3 contributes to anaerobic acid resistance of Escherichia coli. PLoS ONE 5:e10132. doi: 10.1371/journal.pone.0010132
65. Palmer, T., and Berks, B. C. (2012). The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Micro. 10, 483-496. doi: 10.1038/nrmicro2814
66. Park, S.-J., Ghai, R., Martín-Cuadrado, A.-B., Rodríguez-Valera, F., Jung, M.-Y., Kim, J.-G., et al. (2012). Draft genome sequence of the sulfur-oxidizing bacterium "Candidatus Sulfurovum sediminum" AR, which belongs to the Epsilonproteobacteria. J. Bacteriol. 194, 4128-4129. doi: 10.1128/JB.00741-12
67. Perner, M., Gonnella, G., Hourdez, S., Böhnke, S., Kurtz, S., and Girguis, P. (2013a). In-situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. Environ. Microbiol. 15, 1551-1560. doi: 10.1111/1462-2920.12038
68. Perner, M., Hansen, M., Seifert, R., Strauss, H., Koschinsky, A., and Petersen, S. (2013b). Linking geology, fluid chemistry, and microbial activity of basalt-and ultramafic-hosted deep-sea hydrothermal vent environments. Geobiology 11, 340-355. doi: 10.1111/gbi.12039
69. Pham, V. H., Yong, J.-J., Park, S.-J., Yoon, D.-N., Chung, W.-H., and Rhee, S.-K. (2008). Molecular analysis of the diversity of the sulfide: quinone reductase (sqr) gene in sediment environments. Microbiology 154, 3112-3121. doi: 10.1099/mic.0.2008/018580-0
70. Pitcher, R. S., and Watmough, N. J. (2004). The bacterial cytochrome cbb3 oxidases. BBA-Bioenergetics 1655, 388-399. doi: 10.1016/j.bbabio.2003.09.017
71. Potter, L., Angove, H., Richardson, D., and Cole, J. (2001). Nitrate reduction in the periplasm of gram-negative bacteria. Adv. Microb. Physiol. 45, 51-112. doi: 10.1016/S0065-2911(01)45002-8
72. Prabagaran, S. R., Manorama, R., Delille, D., and Shivaji, S. (2007). Predominance of Roseobacter, Sulfitobacter, Glaciecola and Psychrobacter in seawater collected off Ushuaia, Argentina, Sub-Antarctica. FEMS Microbiol. Ecol. 59, 342-355.
73. Preisig, O., Anthamatten, D., and Hennecke, H. (1993). Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. U.S.A. 90, 3309-3313. doi: 10.1073/pnas.90.8.3309
74. Rajagopalan, K. V., and Johnson, J. L. (1992). The pterin molybdenum cofactors. J. Biol. Chem. 267, 10199-10202.
75. Reysenbach, A.-L., Liu, Y., Banta, A. B., Beveridge, T. J., Kirshtein, J. D., Schouten, S., et al. (2006). A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444-447. doi: 10.1038/nature04921
76. Shahak, Y., and Hauska, G. (2008). "Sulfide oxidation from cyanobacteria to humans: sulfide-quinone oxidoreductase (SQR)," in Sulfur Metabolism in Phototrophic Organisms, Vol. 27, eds C. Dahl, D. Knaff, and T. Leustek (Amsterdam: Springer), 319-335.
77. Shao, M., Zhang, T., and Fang, H. H. P. (2009). Autotrophic denitrification and its effect on metal speciation during marine sediment remediation. Water Res. 43, 2961-2968. doi: 10.1016/j.watres.2009.04.016
78. Shibata, H., and Kobayashi, S. (2006). Characterization of a HMT2-like enzyme for sulfide oxidation from Pseudomonas putida. Can. J. Microbiol. 52, 724-730. doi: 10.1139/w06-022
79. Sievert, S. M., Hügler, M., Taylor, C., and Wirsen, C. (2008a). "Sulfur oxidation at deep-sea hydrothermal vents," in Microbial Sulfur Metabolism, eds C. Dahl and C. Friedrich (Berlin: Springer), 238-258.
80. Sievert, S. M., Scott, K. M., Klotz, M. G., Chain, P. S. G., Hauser, L. J., Hemp, J., et al. (2008b). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol. 74, 1145-1156. doi: 10.1128/AEM.01844-07
81. Sikorski, J., Lapidus, A., Copeland, A., Glavina Del Rio, T., Nolan, M., Lucas, S., et al. (2010a). Complete genome sequence of Sulfurospirillum deleyianum type strain (5175T). Stand. Genomic Sci. 2, 149-157. doi: 10.4056/sigs.671209
82. Sikorski, J., Munk, C., Lapidus, A., Ngatchou Djao, O. D., Lucas, S., Glavina Del Rio, T., et al. (2010b). Complete genome sequence of Sulfurimonas autotrophica type strain (OK10T). Stand. Genomic Sci. 3, 194-202. doi: 10.4056/sigs.1173118
83. Smith, J. L., Campbell, B. J., Hanson, T. E., Zhang, C. L., and Cary, S. C. (2008). Nautilia profundicola sp. nov., a thermophilic, sulfur-reducing Epsilonproteobacterium from deep-sea hydrothermal vents. Int. J. Syst. Evol. Microbiol. 58, 1598-1602. doi: 10.1099/ijs.0.65435-0
84. Snaidr, J., Amann, R., Huber, I., Ludwig, W., and Schleifer, K. H. (1997). Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl. Environ. Microbiol. 63, 2884-2896.
85. Stolz, J. F., Ellis, D. J., Blum, J. S., Ahmann, D., Lovley, D. R., and Oremland, R. S. (1999). Sulfurospirillum barnesii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the epsilon-proteobacteria. Int. J. Syst. Bacteriol. 49, 1177-1180. doi: 10.1099/00207713-49-3-1177
86. Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., et al. (2005). Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl. Environ. Microbiol. 71, 7310-7320. doi: 10.1128/AEM.71.11.7310-7320.2005
87. Takai, K., Suzuki, M. T., Nakagawa, S., Miyazaki, M., Suzuki, Y., Inagaki, F., et al. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen-and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int. J. Syst. Evol. Microbiol. 56, 1725-1733.
88. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
89. Tan, B., and Foght, J. (2014). Draft genome sequences of Campylobacterales (Epsilonproteobacteria) obtained from methanogenic oil sands tailings pond metagenomes. Genome Announc. 2, e1034-14. doi: 10.1128/genomeA.01034-14
90. Timmer-Ten Hoor, A. (1975). A new type of thiosulphate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov. Net. J. Sea Res. 9, 344-351. doi: 10.1016/0077-7579(75)90008-3
91. Timmer-Ten Hoor, A. (1981). Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans. Antonie Van Leeuwenhoek 47, 231-243. doi: 10.1007/BF00403394
92. Ullrich, T. C., Blaesse, M., and Huber, R. (2001). Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J. 20, 316-329. doi: 10.1093/emboj/20.3.316
93. Vande Weghe, J. G., and Ow, D. W. (1999). A fission yeast gene for mitochondrial sulfide oxidation. J. Biol. Chem. 274, 13250-13257. doi: 10.1074/jbc.274.19.13250
94. Vetriani, C., Voordeckers, J. W., Crespo-Medina, M., O'brien, C. E., Giovannelli, D., and Lutz, R. A. (2014). Deep-sea hydrothermal vent Epsilonproteobacteria encode a conserved and widespread nitrate reduction pathway (Nap). ISME J. 8, 1510-1521. doi: 10.1038/ismej.2013.246
95. Vignais, P. M., and Billoud, B. (2007). Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107, 4206-4272. doi: 10.1021/cr050196r
96. Voordeckers, J. W., Starovoytov, V., and Vetriani, C. (2005). Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. Int. J. Syst. Evol. Microbiol. 55, 773-779. doi: 10.1099/ijs.0.63430-0
97. Voordouw, G., Armstrong, S. M., Reimer, M. F., Fouts, B., Telang, A. J., Shen, Y., et al. (1996). Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulfate-reducing, fermentative, and sulfide-oxidizing bacteria. Appl. Environ. Microbiol. 62, 1623-1629.
98. Watanabe, K., Kodama, Y., Syutsubo, K., and Harayama, S. (2000). Molecular characterization of bacterial populations in petroleum-contaminated groundwater discharged from underground crude oil storage cavities. Appl. Environ. Microbiol. 66, 4803-4809. doi: 10.1128/AEM.66.11.4803-4809.2000
99. Wirsen, C. O., Sievert, S. M., Cavanaugh, C. M., Molyneaux, S. J., Ahmad, A., Taylor, L. T., et al. (2002). Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl. Environ. Microbiol. 68, 316-325. doi: 10.1128/AEM.68.1.316-325.2002
100. Wolfe, R. S., and Penning, N. (1977). Reduction of sulfur by spirillum 5175 and syntrophism with Chlorobium. Appl. Environ. Microbiol. 33, 427-433.
101. Yagi, J. M., Neuhauser, E. F., Ripp, J. A., Mauro, D. M., and Madsen, E. L. (2009). Subsurface ecosystem resilience: long-term attenuation of subsurface contaminants supports a dynamic microbial community. ISME J. 4, 131-143. doi: 10.1038/ismej.2009.101
102. Zhang, M., Zhang, T., Shao, M. F., and Fang, H. H. P. (2009). Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76, 677-682. doi: 10.1016/j.chemosphere.2009.03.066
103. Zhang, Y., and Sievert, S. M. (2014). Pan-genome analyses identify lineage-and niche-specific markers of evolution and adaptation in Epsilonproteobacteria. Front. Microbiol. 5:110. doi: 10.3389/fmicb.2014.00110