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Metagenomic Signatures of Microbial Communities in Deep-Sea Hydrothermal Sediments of Azores Vent Fields

  • Environmental Microbiology
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Abstract

The organisms inhabiting the deep-seafloor are known to play a crucial role in global biogeochemical cycles. Chemolithoautotrophic prokaryotes, which produce biomass from single carbon molecules, constitute the primary source of nutrition for the higher organisms, being critical for the sustainability of food webs and overall life in the deep-sea hydrothermal ecosystems. The present study investigates the metabolic profiles of chemolithoautotrophs inhabiting the sediments of Menez Gwen and Rainbow deep-sea vent fields, in the Mid-Atlantic Ridge. Differences in the microbial community structure might be reflecting the distinct depth, geology, and distance from vent of the studied sediments. A metagenomic sequencing approach was conducted to characterize the microbiome of the deep-sea hydrothermal sediments and the relevant metabolic pathways used by microbes. Both Menez Gwen and Rainbow metagenomes contained a significant number of genes involved in carbon fixation, revealing the largely autotrophic communities thriving in both sites. Carbon fixation at Menez Gwen site was predicted to occur mainly via the reductive tricarboxylic acid cycle, likely reflecting the dominance of sulfur-oxidizing Epsilonproteobacteria at this site, while different autotrophic pathways were identified at Rainbow site, in particular the Calvin–Benson–Bassham cycle. Chemolithotrophy appeared to be primarily driven by the oxidation of reduced sulfur compounds, whether through the SOX-dependent pathway at Menez Gwen site or through reverse sulfate reduction at Rainbow site. Other energy-yielding processes, such as methane, nitrite, or ammonia oxidation, were also detected but presumably contributing less to chemolithoautotrophy. This work furthers our knowledge of the microbial ecology of deep-sea hydrothermal sediments and represents an important repository of novel genes with potential biotechnological interest.

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References

  1. Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–725. https://doi.org/10.1126/science.229.4715.717

    Article  PubMed  CAS  Google Scholar 

  2. Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75:361–422. https://doi.org/10.1128/MMBR.00039-10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Reysenbach AL, Shock E (2002) Merging genomes with geochemistry in hydrothermal ecosystems. Science 296:1077–1082. https://doi.org/10.1126/science.1072483

    Article  PubMed  CAS  Google Scholar 

  4. Teske A, Hinrichs KU, Edgcomb V, de Vera Gomez A, Kysela D, Sylva SP, Sogin ML, Jannasch HW (2002) Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl Environ Microb 68:1994–2007. https://doi.org/10.1128/AEM.68.4.1994-2007.2002

    Article  CAS  Google Scholar 

  5. Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T, Kazama H, Hosoi-Tanabe S, Nakamura K, Kinoshita M, Hirayama H, Inagaki F, Tsunogai U, Ishibashi J, Takai K (2010) Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa trough. Appl Environ Microb 76:1198–1211. https://doi.org/10.1128/Aem.00924-09

    Article  CAS  Google Scholar 

  6. Reveillaud J, Reddington E, McDermott J, Algar C, Meyer JL, Sylva S, Seewald J, German CR, Huber JA (2016) Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman Rise. Environ. Microbiol 18:1970–1987. https://doi.org/10.1111/1462-2920.13173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Huber JA, Cantin HV, Huse SM, Welch DB, Sogin ML, Butterfield DA (2010) Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. FEMS Microbiol. Ecol. 73:538–549. https://doi.org/10.1111/j.1574-6941.2010.00910.x

    Article  PubMed  CAS  Google Scholar 

  8. Huber JA, Welch DBM, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100. https://doi.org/10.1126/science.1146689

    Article  PubMed  CAS  Google Scholar 

  9. Akerman NH, Butterfield DA, Huber JA (2013) Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front Microbiol 4:185. https://doi.org/10.3389/Fmicb.2013.00185

  10. Brazelton WJ, Ludwig KA, Sogin ML, Andreishcheva EN, Kelley DS, Shen C-C, Edwards RL, Baross JA (2010) Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys. PNAS 107:1612–1617. https://doi.org/10.1073/pnas.0905369107

    Article  PubMed  Google Scholar 

  11. Roussel EG, Konn C, Charlou JL, Donval JP, Fouquet Y, Querellou J, Prieur D, Bonavita MAC (2011) Comparison of microbial communities associated with three Atlantic ultramafic hydrothermal systems. FEMS Microbiol. Ecol. 77:647–665. https://doi.org/10.1111/j.1574-6941.2011.01161.x

    Article  PubMed  CAS  Google Scholar 

  12. Voordeckers JW, Do MH, Hugler M, Ko V, Sievert SM, Vetriani C (2008) Culture dependent and independent analyses of 16S rRNA and ATP citrate lyase genes: a comparison of microbial communities from different black smoker chimneys on the Mid-Atlantic Ridge. Extremophiles: life under extreme conditions 12:627–640. https://doi.org/10.1007/s00792-008-0167-5

    Article  CAS  Google Scholar 

  13. Dick GJ, Anantharaman K, Baker BJ, Li M, Reed DC, Sheik CS (2013) The microbiology of deep-sea hydrothermal vent plumes: ecological and biogeographic linkages to seafloor and water column habitats. Front. Microbiol. 4:124. https://doi.org/10.3389/fmicb.2013.00124

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li M, Jain S, Dick GJ (2016) Genomic and transcriptomic resolution of organic matter utilization among deep-sea bacteria in Guaymas Basin hydrothermal plumes. Front Microbiol 7:1125. https://doi.org/10.3389/Fmicb.2016.01125

  15. Flores GE, Campbell JH, Kirshtein JD, Meneghin J, Podar M, Steinberg JI, Seewald JS, Tivey MK, Voytek MA, Yang ZK, Reysenbach AL (2011) Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ. Microbiol. 13:2158–2171. https://doi.org/10.1111/j.1462-2920.2011.02463.x

    Article  PubMed  CAS  Google Scholar 

  16. Flores GE, Shakya M, Meneghin J, Yang ZK, Seewald JS, Wheat CG, Podar M, Reysenbach AL (2012) Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10:333–346. https://doi.org/10.1111/j.1472-4669.2012.00325.x

    Article  PubMed  CAS  Google Scholar 

  17. Anantharaman K, Breier JA, Dick GJ (2016) Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center. Isme J 10:225–239. https://doi.org/10.1038/ismej.2015.81

    Article  PubMed  CAS  Google Scholar 

  18. Wang H-l, Sun L (2016) Comparative metagenomic analysis of the microbial communities in the surroundings of Iheya north and Iheya ridge hydrothermal fields reveals insights into the survival strategy of microorganisms in deep-sea environments. J Mar Syst in press. doi:https://doi.org/10.1016/j.jmarsys.2016.10.006

  19. Oulas A, Polymenakou PN, Seshadri R, Tripp HJ, Mandalakis M, Paez-Espino AD, Pati A, Chain P, Nomikou P, Carey S, Kilias S, Christakis C, Kotoulas G, Magoulas A, Ivanova NN, Kyrpides NC (2016) Metagenomic investigation of the geologically unique Hellenic Volcanic Arc reveals a distinctive ecosystem with unexpected physiology. Environ. Microbiol. 18:1122–1136. https://doi.org/10.1111/1462-2920.13095

    Article  PubMed  CAS  Google Scholar 

  20. Von Damm KL (1995) Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions (222–247). https://doi.org/10.1029/GM091

  21. Charlou JL, Donval JP, Douville E, Jean-Baptiste P, Radford-Knoery J, Fouquet Y, Dapoigny A, Stievenard M (2000) Compared geochemical signatures and the evolution of Menez Gwen (37 degrees 50 ' N) and Lucky Strike (37 degrees 17 ' N) hydrothermal fluids, south of the Azores Triple Junction on the Mid-Atlantic Ridge. Chem. Geol. 171:49–75. https://doi.org/10.1016/S0009-2541(00)00244-8

    Article  CAS  Google Scholar 

  22. Mügler C, Jean-Baptiste P, Perez F, Charlou J-L (2016) Modeling of hydrogen production by serpentinization in ultramafic-hosted hydrothermal systems: application to the Rainbow field. Geofluids 16:476–489. https://doi.org/10.1111/gfl.12169

    Article  CAS  Google Scholar 

  23. Charlou JL, Donval JP, Konn C, Ondréas H, Fouquet Y, Jean-Baptiste P, Fourré E (2010) High production and fluxes of H2 and CH4 and evidence of abiotic hydrocarbon synthesis by serpentinization in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge. In: in Diversity of hydrothermal systems on slow spreading ocean ridges (eds Rona PA, Devey CW, Dyment J, and Murton BJ), American Geophysical Union, Washington, D. C.. https://doi.org/10.1029/2008GM000752

  24. Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N (2002) Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′N, MAR). Chem. Geol. 191:345–359. https://doi.org/10.1016/S0009-2541(02)00134-1

    Article  CAS  Google Scholar 

  25. Meier DV, Bach W, Girguis PR, Gruber-Vodicka HR, Reeves EP, Richter M, Vidoudez C, Amann R, Meyerdierks A (2016) Heterotrophic Proteobacteria in the vicinity of diffuse hydrothermal venting. Environ. Microbiol. 18:4348–4368. https://doi.org/10.1111/1462-2920.13304

    Article  PubMed  Google Scholar 

  26. Rossel PE, Stubbins A, Hach PF, Dittmar T (2015) Bioavailability and molecular composition of dissolved organic matter from a diffuse hydrothermal system. Mar. Chem. 177:257–266. https://doi.org/10.1016/j.marchem.2015.07.002

    Article  CAS  Google Scholar 

  27. Mills R, Elderfield H, Thomson J (1993) A dual origin for the hydrothermal component in a metalliferous sediment core from the Mid-Atlantic Ridge. Journal of Geophysical Research: Solid Earth 98:9671–9681

    Article  CAS  Google Scholar 

  28. Amend JP, McCollom TM, Hentscher M, Bach W (2011) Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types. Geochim Cosmochim Ac 75:5736–5748. https://doi.org/10.1016/j.gca.2011.07.041

    Article  CAS  Google Scholar 

  29. Cerqueira T, Pinho D, Egas C, Froufe H, Altermark B, Candeias C, Santos RS, Bettencourt R (2015) Microbial diversity in deep-sea sediments from the Menez Gwen hydrothermal vent system of the Mid-Atlantic Ridge. Marine genomics 24, Part 3: 343–355. doi:https://doi.org/10.1016/j.margen.2015.09.001

  30. Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ. Microbiol. 5:961–976. https://doi.org/10.1046/j.1462-2920.2003.00495.x

    Article  PubMed  CAS  Google Scholar 

  31. Nercessian O, Fouquet Y, Pierre C, Prieur D, Jeanthon C (2005) Diversity of Bacteria and Archaea associated with a carbonate-rich metalliferous sediment sample from the rainbow vent field on the Mid-Atlantic Ridge. Environ. Microbiol. 7:698–714. https://doi.org/10.1111/j.1462-2920.2005.00744.x

    Article  PubMed  CAS  Google Scholar 

  32. Cerqueira T, Pinho D, Froufe H, Santos RS, Bettencourt R, Egas C (2017) Sediment microbial diversity of three deep-sea hydrothermal vents southwest of the Azores. Microb. Ecol. 74:332–349. https://doi.org/10.1007/s00248-017-0943-9

    Article  PubMed  CAS  Google Scholar 

  33. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Markowitz VM, Chen I-MA, Chu K, Szeto E, Palaniappan K, Pillay M, Ratner A, Huang J, Pagani I, Tringe S (2014) IMG/M 4 version of the integrated metagenome comparative analysis system. Nucleic Acids Res. 42:D568–D573. https://doi.org/10.1093/nar/gkt919

    Article  PubMed  CAS  Google Scholar 

  35. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9(1):386. https://doi.org/10.1186/1471-2105-9-386

  36. Seyfried W, Pester NJ, Ding K, Rough M (2011) Vent fluid chemistry of the Rainbow hydrothermal system (36 N, MAR): phase equilibria and in situ pH controls on subseafloor alteration processes. Geochim Cosmochim Ac 75:1574–1593

    Article  CAS  Google Scholar 

  37. McCollom TM, Seewald JS, German CR (2015) Investigation of extractable organic compounds in deep-sea hydrothermal vent fluids along the Mid-Atlantic Ridge. Geochim Cosmochim Ac 156:122–144. https://doi.org/10.1016/j.gca.2015.02.022

    Article  CAS  Google Scholar 

  38. Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol. Ecol. 65:1–14. https://doi.org/10.1111/j.1574-6941.2008.00502.x

    Article  PubMed  CAS  Google Scholar 

  39. Hügler M, Gärtner A, Imhoff JF (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. https://doi.org/10.1111/j.1574-6941.2010.00919.x

    Article  PubMed  CAS  Google Scholar 

  40. Hugler M, Sievert SM (2011) Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3:261–289. https://doi.org/10.1146/annurev-marine-120709-142712

    Article  Google Scholar 

  41. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4:458–468. https://doi.org/10.1038/nrmicro1414

    Article  PubMed  CAS  Google Scholar 

  42. Lanzen A, Jorgensen SL, Bengtsson MM, Jonassen I, Ovreas L, Urich T (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. Fems Microbiol Ecol 77:577–589. https://doi.org/10.1111/j.1574-6941.2011.01138.x

    Article  PubMed  CAS  Google Scholar 

  43. Sievert SM, Hugler M, Taylor CD, Wirsen CO (2008) Sulfur oxidation at deep-sea hydrothermal vents. In: Dahl C, Friedrich CG (eds). Microbial Sulfur Metabolism:238-258. https://doi.org/10.1007/978-3-540-72682-1_19

  44. Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, Hourdez S, Girguis PR, Wankel SD, Barbe V, Pelletier E, Fink D, Borowski C, Bach W, Dubilier N (2011) Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476:176–180. https://doi.org/10.1038/nature10325

    Article  PubMed  CAS  Google Scholar 

  45. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6:725–740. https://doi.org/10.1038/nrmicro1992

    Article  PubMed  CAS  Google Scholar 

  46. Won YJ, Hallam SJ, O'Mullan GD, Pan IL, Buck KR, Vrijenhoek RC (2003) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus bathymodiolus. Appl Environ Microb 69:6785–6792. https://doi.org/10.1128/AEM.69.11.6785-6792.2003

    Article  CAS  Google Scholar 

  47. Egas C, Pinheiro M, Gomes P, Barroso C, Bettencourt R (2012) The transcriptome of Bathymodiolus azoricus gill reveals expression of genes from endosymbionts and free-living deep-sea bacteria. Marine drugs 10:1765–1783. https://doi.org/10.3390/md10081765

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Ponnudurai R, Kleiner M, Sayavedra L, Petersen JM, Moche M, Otto A, Becher D, Takeuchi T, Satoh N, Dubilier N, Schweder T, Markert S (2017) Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis. Isme J 11:463–477. https://doi.org/10.1038/ismej.2016.124

    Article  PubMed  CAS  Google Scholar 

  49. Wentrup C, Wendeberg A, Schimak M, Borowski C, Dubilier N (2014) Forever competent: deep-sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime. Environ. Microbiol. 16:3699–3713. https://doi.org/10.1111/1462-2920.12597

    Article  PubMed  Google Scholar 

  50. Kono T, Mehrotra S, Endo C, Kizu N, Matusda M, Kimura H, Mizohata E, Inoue T, Hasunuma T, Yokota A, Matsumura H, Ashida H (2017) A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea 8:14007. https://doi.org/10.1038/ncomms14007

  51. Hugler M, Wirsen CO, Fuchs G, Taylor CD, Sievert SM (2005) Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the epsilon subdivision of proteobacteria. J. Bacteriol. 187:3020–3027. https://doi.org/10.1128/Jb.187.9.3020-3027.2005

    Article  PubMed  PubMed Central  Google Scholar 

  52. King GM, Weber CF (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat. Rev. Microbiol. 5:107–118. https://doi.org/10.1038/nrmicro1595

    Article  PubMed  CAS  Google Scholar 

  53. Wu M, Ren QH, Durkin AS, Daugherty SC, Brinkac LM, Dodson RJ, Madupu R, Sullivan SA, Kolonay JF, Nelson WC, Tallon LJ, Jones KM, Ulrich LE, Gonzalez JM, Zhulin IB, Robb FT, Eisen JA (2005) Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLoS Genet. 1:563–574. https://doi.org/10.1371/journal.pgen.0010065

    Article  CAS  Google Scholar 

  54. Fuchs G (1994) Variations of the acetyl-CoA pathway in diversely related microorganisms that are not acetogens. In: Drake HL (ed) Acetogenesis. Springer US, Boston, MA, pp 507–520. https://doi.org/10.1007/978-1-4615-1777-1_19

  55. Jansen K, Thauer RK, Widdel F, Fuchs G (1984) Carbon assimilation pathways in sulfate reducing bacteria. Formate, carbon dioxide, carbon monoxide, and acetate assimilation by Desulfovibrio baarsii. Arch. Microbiol. 138:257–262. https://doi.org/10.1007/bf00402132

    Article  CAS  Google Scholar 

  56. Zarzycki J, Brecht V, Muller M, Fuchs G (2009) Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. PNAS 106:21317–21322. https://doi.org/10.1073/pnas.0908356106

    Article  PubMed  CAS  Google Scholar 

  57. Herbold CW, Lebedeva E, Palatinszky M, Wagner M (2015) Candidatus Nitrosotenuis. Bergey's manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118960608.gbm01291

  58. Reinthaler T, van Aken HM, Herndl GJ (2010) Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic's interior. Deep-Sea Res Pt Ii 57:1572–1580. https://doi.org/10.1016/j.dsr2.2010.02.023

    Article  CAS  Google Scholar 

  59. Anantharaman K, Breier JA, Sheik CS, Dick GJ (2013) Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. PNAS 110:330–335. https://doi.org/10.1073/pnas.1215340110

    Article  PubMed  Google Scholar 

  60. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8:253–259. https://doi.org/10.1016/j.mib.2005.04.005

    Article  PubMed  CAS  Google Scholar 

  61. Yamamoto M, Takai K (2011) Sulfur metabolisms in epsilon- and gamma-Proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2:192. https://doi.org/10.3389/Fmicb.2011.00192

  62. Jormakka M, Yokoyama K, Yano T, Tamakoshi M, Akimoto S, Shimamura T, Curmi P, Iwata S (2008) Molecular mechanism of energy conservation in polysulfide respiration. Nat. Struct. Mol. Biol. 15:730–737. https://doi.org/10.1038/nsmb.1434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Nakagawa S, Takaki Y, Shimamura S, Reysenbach A-L, Takai K, Horikoshi K (2007) Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens. PNAS 104:12146–12150. https://doi.org/10.1073/pnas.0700687104

    Article  PubMed  CAS  Google Scholar 

  64. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ. Microbiol. 7:1619–1632. https://doi.org/10.1111/j.1462-2920.2005.00856.x

    Article  PubMed  CAS  Google Scholar 

  65. Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53:1801–1805. https://doi.org/10.1099/ijs.0.02682-0

    Article  PubMed  CAS  Google Scholar 

  66. Xie W, Wang F, Guo L, Chen Z, Sievert SM, Meng J, Huang G, Li Y, Yan Q, Wu S, Wang X, Chen S, He G, Xiao X, Xu A (2011) Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. Isme J 5:414–426. https://doi.org/10.1038/ismej.2010.144

    Article  PubMed  Google Scholar 

  67. Meyer B, Kuever J (2007) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfuroxidizing prokaryotes. Microbiology-Sgm 153:3478–3498. https://doi.org/10.1099/mic.0.2007/008250-0

    Article  CAS  Google Scholar 

  68. Lam P, Cowen JP, Jones RD (2004) Autotrophic ammonia oxidation in a deep-sea hydrothermal plume. FEMS Microbiol. Ecol. 47:191–206. https://doi.org/10.1016/S0168-6496(03)00256-3

    Article  PubMed  CAS  Google Scholar 

  69. Stein LY (2011) Heterotrophic nitrification and nitrifier denitrification. Nitrification. American Society of Microbiology:95-114. https://doi.org/10.1128/9781555817145.ch5

  70. Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ε-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int. J. Syst. Evol. Microbiol. 54:1477–1482. https://doi.org/10.1099/ijs.0.03042-0

    Article  PubMed  CAS  Google Scholar 

  71. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F, Horikoshi K (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. https://doi.org/10.1099/ijs.0.64255-0

    Article  PubMed  CAS  Google Scholar 

  72. Nakagawa S, Takai K, Inagaki F, Horikoshi K, Sako Y (2005) 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. https://doi.org/10.1099/ijs.0.63480-0

    Article  PubMed  CAS  Google Scholar 

  73. Vetriani C, Voordeckers JW, Crespo-Medina M, O'Brien CE, Giovannelli D, Lutz RA (2014) Deep-sea hydrothermal vent Epsilonproteobacteria encode a conserved and widespread nitrate reduction pathway (Nap). Isme J 8:1510–1521. https://doi.org/10.1038/ismej.2013.246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Byrne N, Strous M, Crepeau V, Kartal B, Birrien JL, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten M, Prieur D, Godfroy A (2009) Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. Isme J 3:117–123. https://doi.org/10.1038/ismej.2008.72

    Article  PubMed  CAS  Google Scholar 

  75. Lücker S, Nowka B, Rattei T, Spieck E, Daims H (2013) The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front Microbiol 4:27. https://doi.org/10.3389/fmicb.2013.00027

  76. Baker BJ, Sheik CS, Taylor CA, Jain S, Bhasi A, Cavalcoli JD, Dick GJ (2013) Community transcriptomic assembly reveals microbes that contribute to deep-sea carbon and nitrogen cycling. Isme J 7:1962. https://doi.org/10.1038/ismej.2013.85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Mehta MP, Butterfield DA, Baross JA (2003) Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge. Appl Environ Microb 69:960–970. https://doi.org/10.1128/AEM.69.2.960-970.2003

    Article  CAS  Google Scholar 

  78. Voss M, Bange HW, Dippner JW, Middelburg JJ, Montoya JP, Ward B (2013) The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 368:20130121. https://doi.org/10.1098/rstb.2013.0121

    Article  CAS  Google Scholar 

  79. Douville E, Charlou J, Oelkers E, Bienvenu P, Colon CJ, Donval J, Fouquet Y, Prieur D, Appriou P (2002) The rainbow vent fluids (36 14′ N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids. Chem. Geol. 184:37–48

    Article  CAS  Google Scholar 

  80. Marcon Y, Sahling H, Borowski C, Ferreira CD, Thal J, Bohrmann G (2013) Megafaunal distribution and assessment of total methane and sulfide consumption by mussel beds at Menez Gwen hydrothermal vent, based on geo-referenced photomosaics. Deep-Sea Res Pt I 75:93–109. https://doi.org/10.1016/j.dsr.2013.01.008

    Article  CAS  Google Scholar 

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Acknowledgements

We are thankful to the scientific parties of the BioBaz 2013 cruise, in particular to the crew members of the RV “Pourquoi Pas?,” the ROV “Victor6000” team (Ifremer, France) for their assistance in obtaining the sediment samples, Eva Martins and Cátia Cardoso for sample handling on board, Tomás Melo for map and figure design, and Valentina Costa and Diogo Pinho for all technical assistance in the laboratory and with data sequencing. We also acknowledge IMAR-Centre management unit of the University of the Azores. This study was supported by the “Direção Regional da Ciência e Tecnologia” (DRCT) (TC doctoral grant—M3.1.2/F/052/2011) and “Fundação para a Ciência e Tecnologia” (FCT), through the strategic project UID/MAR/04292/2013 granted to MARE.

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Authors and Affiliations

  1. Department of Oceanography and Fisheries, University of the Azores, Rua Prof. Dr. Frederico Machado, 9901-862, Horta, Portugal

    Teresa Cerqueira

  2. MARE - Marine and Environmental Sciences Centre, 9901-862, Horta, Portugal

    Teresa Cerqueira & Raul Bettencourt

  3. Next Generation Sequencing Unit – UC-Biotech, Center for Neuroscience and Cell Biology, Parque Tecnológico de Cantanhede, Núcleo 04, Lote 8, 3060-197, Cantanhede, Portugal

    Cristina Barroso & Conceição Egas

  4. Biocant, Parque Tecnológico de Cantanhede, Núcleo 04, Lote 8, 3060-197, Cantanhede, Portugal

    Cristina Barroso, Hugo Froufe & Conceição Egas

  5. OKEANOS Research Unit, Faculty of Science and Technology, University of the Azores, 9901-862, Horta, Portugal

    Teresa Cerqueira & Raul Bettencourt

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  1. Teresa Cerqueira
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  2. Cristina Barroso
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Correspondence to Teresa Cerqueira.

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Cerqueira, T., Barroso, C., Froufe, H. et al. Metagenomic Signatures of Microbial Communities in Deep-Sea Hydrothermal Sediments of Azores Vent Fields. Microb Ecol 76, 387–403 (2018). https://doi.org/10.1007/s00248-018-1144-x

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  • DOI: https://doi.org/10.1007/s00248-018-1144-x

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