Microbial Ecology

, Volume 74, Issue 2, pp 332–349 | Cite as

Sediment Microbial Diversity of Three Deep-Sea Hydrothermal Vents Southwest of the Azores

  • Teresa Cerqueira
  • Diogo Pinho
  • Hugo Froufe
  • Ricardo S. Santos
  • Raul Bettencourt
  • Conceição Egas
Environmental Microbiology


Menez Gwen, Lucky Strike and Rainbow are the three most visited and well-known deep-sea hydrothermal vent fields in the Azores region, located in the Mid-Atlantic Ridge. Their distinct geological and ecological features allow them to support a diversity of vent communities, which are largely dependent on Bacteria and Archaea capable of anaerobic or microaerophilic metabolism. These communities play important ecological roles through chemoautotrophy, feeding and in establishing symbiotic associations. However, the occurrence and distribution of these microbes remain poorly understood, especially in deep-sea sediments. In this study, we provide for the first time a comparative survey of the sediment-associated microbial communities from these three neighbouring vent fields. Sediment samples collected in the Menez Gwen, Lucky Strike and Rainbow vent fields showed significant differences in trace-metal concentrations and associated microbiomes. The taxonomic profiles of bacterial, archaeal and eukaryotic representatives were assessed by rRNA gene-tag pyrosequencing, identified anaerobic methanogens and microaerobic Epsilonproteobacteria, particularly at the Menez Gwen site, suggesting sediment communities potentially enriched in sub-seafloor microbes rather than from pelagic microbial taxa. Cosmopolitan OTUs were also detected mostly at Lucky Strike and Rainbow sites and affiliated with the bacterial clades JTB255, Sh765B-TzT-29, Rhodospirillaceae and OCS155 marine group and with the archaeal Marine Group I. Some variations in the community composition along the sediment depth were revealed. Elemental contents and hydrothermal influence are suggested as being reflected in the composition of the microbial assemblages in the sediments of the three vent fields. Altogether, these findings represent valuable information for the understanding of the microbial distribution and potential ecological roles in deep-sea hydrothermal fields.


Pyrosequencing Microbial diversity Deep-sea sediments Hydrothermal vent field Menez Gwen Lucky Strike Rainbow 



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 samples handling on board, Tomás Melo for map and figures design, Ricardo Medeiros from ImageDOP for map data and Valentina Costa for all technical assistance in the laboratory. We also acknowledge IMAR-Centre management unit of the University of the Azores. This study was supported by the Azorean Directorate for Science, Technology and Communications (DRCTC) (TC doctoral grant—M3.1.2/F/052/2011).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

248_2017_943_MOESM1_ESM.jpg (6.1 mb)
Figure S1 Photographs of the sediment sampling sites during the BIOBAZ cruise, in August 2013. A blade corer device was used to retrieve sediment samples from the most suitable area near an active vent from the Menez Gwen (MG), Lucky Strike (LS) and Rainbow (RB) hydrothermal vent fields in the northern MAR. The left panel represents the general view of the seafloor to be sampled in comparison to the right panel corresponding to the actual sampling spots where the corers successfully retrieved the sediments. MG (right panel)—sampling was performed in the ‘MG2 site’ ~4 m from an active vent chimney, at a depth of 825 m. LS (right panel)—sampling was performed between the South and the Northeast volcanic summits of the vent system, ~40 m from an active vent, at 1603 m deep. RB (right panel)—sampling was performed ~100 m from an active vent, at 2362 m deep. (JPEG 6243 kb)
248_2017_943_MOESM2_ESM.png (197 kb)
Figure S2 Rarefaction curves for 16S rRNA gene amplicon sequences from bacteria (a) and archaea (b). Number of sequences are illustrated in relation to the number of operational taxonomic units (OTUs), grouped at 97% similarity level for each sediment sample under study. Samples retrieved from Menez Gwen (MG), Lucky Strike (LS) and Rainbow (RB) hydrothermal fields are plotted in blue, red and yellow, respectively. The curves show a good coverage of the diversity present in the communities under study even though there is still a hidden biodiversity within the sediments. (PNG 197 kb)
248_2017_943_MOESM3_ESM.docx (40 kb)
Supplementary file 1 Detailed description of the study sites and vent field characteristics. (DOCX 40 kb)
248_2017_943_MOESM4_ESM.xlsx (13 kb)
Table S1 Diversity and richness estimators. (XLSX 12 kb)
248_2017_943_MOESM5_ESM.xlsx (377 kb)
Table S2 Genus-level taxonomic affiliations of all OTUs derived from 454 sequencing of SSU rRNA genes from Menez Gwen (MG), Lucky Strike (LS) and Rainbow (RB) sediment samples. (XLSX 377 kb)


  1. 1.
    Reysenbach A-L, Banta AB, Boone DR, Cary SC, Luther GW (2000) Biogeochemistry: microbial essentials at hydrothermal vents. Nature 404:835–835CrossRefPubMedGoogle Scholar
  2. 2.
    Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25:175–243CrossRefPubMedGoogle Scholar
  3. 3.
    Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–725. doi: 10.1126/science.229.4715.717 CrossRefPubMedGoogle Scholar
  4. 4.
    Wirsen CO, Jannasch HW, Molyneaux SJ (1993) Chemosynthetic microbial activity at Mid-Atlantic Ridge hydrothermal vent sites. Journal of Geophysical Research: Solid Earth 98:9693–9703CrossRefGoogle Scholar
  5. 5.
    Van Dover C (2000) The ecology of deep-sea hydrothermal vents. Princeton University PressGoogle Scholar
  6. 6.
    Karl D (1995) Ecology of free-living, hydrothermal vent microbial communities. The microbiology of deep-sea hydrothermal vents:35–124Google Scholar
  7. 7.
    Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4:458–468. doi: 10.1038/nrmicro1414 CrossRefPubMedGoogle Scholar
  8. 8.
    Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol. Ecol. 65:1–14. doi: 10.1111/j.1574-6941.2008.00502.x CrossRefPubMedGoogle Scholar
  9. 9.
    German C, Higgs N, Thomson J, Mills R, Elderfield H, Blusztajn J, Fleer A, Bacon M (1993) A geochemical study of metalliferous sediment from the TAG Hydrothermal Mound, 26° 08′ N, Mid-Atlantic Ridge. Journal of Geophysical Research: Solid Earth 98:9683–9692CrossRefGoogle Scholar
  10. 10.
    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 98:9671–9681CrossRefGoogle Scholar
  11. 11.
    Hilton DR, McMurtry GM, Goff F (1998) Large variations in vent fluid CO2/He-3 ratios signal rapid changes in magma chemistry at Loihi seamount, Hawaii. Nature 396:359–362. doi: 10.1038/24603 CrossRefGoogle Scholar
  12. 12.
    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. doi: 10.1016/j.gca.2011.07.041 CrossRefGoogle Scholar
  13. 13.
    Fustec A, Desbruyères D, Juniper SK (1987) Deep-Sea hydrothermal vent communities at 13°N on the East Pacific Rise: microdistribution and temporal variations. Biol. Oceanogr. 4:121–164. doi: 10.1080/01965581.1987.10749487 Google Scholar
  14. 14.
    Hessler RR, Smithey WM, Boudrias MA, Keller CH, Lutz RA, Childress JJ (1988) Temporal change in megafauna at the Rose Garden Hydrothermal Vent (Galapagos Rift—Eastern Tropical Pacific). Deep-Sea Res. 35:1681–168&. doi: 10.1016/0198-0149(88)90044-1 CrossRefGoogle Scholar
  15. 15.
    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. doi: 10.1128/Aem.00924-09 CrossRefGoogle Scholar
  16. 16.
    Durbin AM, Teske A (2012) Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Frontiers in microbiology 3. doi:  10.3389/Fmicb.2012.00168
  17. 17.
    Jorgensen SL, Hannisdal B, Lanzen A, Baumberger T, Flesland K, Fonseca R, Ovreas L, Steen IH, Thorseth IH, Pedersen RB, Schleper C (2012) Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. P Natl Acad Sci USA 109:E2846–E2855. doi: 10.1073/pnas.1207574109 CrossRefGoogle Scholar
  18. 18.
    Nunoura T, Takaki Y, Shimamura S, Kakuta J, Kazama H, Hirai M, Masui N, Tomaru H, Morono Y, Imachi H, Inagaki F, Takai K (2016) Variance and potential niche separation of microbial communities in subseafloor sediments off Shimokita Peninsula, Japan. Environ. Microbiol. 18:1889–1906. doi: 10.1111/1462-2920.13096 CrossRefPubMedGoogle Scholar
  19. 19.
    Langmuir C, Humphris S, Fornari D, Van Dover C, Von Damm K, Tivey MK, Colodner D, Charlou JL, Desonie D, Wilson C, Fouquet Y, Klinkhammer G, Bougault H (1997) Hydrothermal vents near a mantle hot spot: the Lucky Strike vent field at 37°N on the Mid-Atlantic Ridge. Earth Planet. Sci. Lett. 148:69–91. doi: 10.1016/S0012-821X(97)00027-7 CrossRefGoogle Scholar
  20. 20.
    Humphris SE, Fornari DJ, Scheirer DS, German CR, Parson LM (2002) Geotectonic setting of hydrothermal activity on the summit of Lucky Strike Seamount (37 degrees 17 ' N, Mid-Atlantic Ridge). Geochem Geophy Geosy 3. doi:  10.1029/2001gc000284
  21. 21.
    Fouquet Y, Charlou JL, Donval JP, Radford-Knoery J, Pelle P, Ondreas H, Lourenco N, Segonzac M, Tivey MK (1994) A detailed study of the Lucky Strike hydrothermal site and discovery of a new hydrothermal site: « Menez-Gwen ». Preliminary results of DIVA 1 cruise (5–29 May, 1994). Inter-Ridge News 3:14–17Google Scholar
  22. 22.
    Parson L, Gràcia E, Coller D, German C, Needham D (2000) Second-order segmentation; the relationship between volcanism and tectonism at the MAR, 38 N–35 40′ N. Earth Planet. Sci. Lett. 178:231–251CrossRefGoogle Scholar
  23. 23.
    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. doi: 10.1016/S0009-2541(00)00244-8 CrossRefGoogle Scholar
  24. 24.
    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. doi: 10.1016/j.dsr.2013.01.008 CrossRefGoogle Scholar
  25. 25.
    Fouquet Y, Charlou JL, Ondreas H, Radford-Knoery J, Donval J, Douville E, Apprioual R, Cambon P, Pellé H, Landuré J (1997) Discovery and first submersible investigations on the Rainbow hydrothermal field on the MAR (36 14′ N). Eos Trans AGU 78:F832Google Scholar
  26. 26.
    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. doi: 10.1016/S0009-2541(02)00134-1 CrossRefGoogle Scholar
  27. 27.
    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. 184:37–48CrossRefGoogle Scholar
  28. 28.
    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 75:1574–1593CrossRefGoogle Scholar
  29. 29.
    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. doi: 10.1038/ismej.2008.72 CrossRefPubMedGoogle Scholar
  30. 30.
    Crépeau V, Bonavita M-AC, Lesongeur F, Randrianalivelo H, Sarradin P-M, Sarrazin J, Godfroy A (2011) Diversity and function in microbial mats from the Lucky Strike hydrothermal vent field. FEMS Microbiol. Ecol. 76:524–540CrossRefPubMedGoogle Scholar
  31. 31.
    Scott JJ, Breier JA, Luther III GW, Emerson D (2015) Microbial iron mats at the Mid-Atlantic Ridge and evidence that Zetaproteobacteria may be restricted to iron-oxidizing marine systems. PLoS One 10:e0119284CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    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. doi: 10.3390/md10081765 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Guri M, Durand L, Cueff-Gauchard V, Zbinden M, Crassous P, Shillito B, Cambon-Bonavita M-A (2012) Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. The ISME journal 6:597–609CrossRefPubMedGoogle Scholar
  34. 34.
    Jan C, Petersen JM, Werner J, Teeling H, Huang S, Glöckner FO, Golyshina OV, Dubilier N, Golyshin PN, Jebbar M (2014) The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environ. Microbiol. 16:2723–2738CrossRefPubMedGoogle Scholar
  35. 35.
    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. doi: 10.1007/s00792-008-0167-5 CrossRefGoogle Scholar
  36. 36.
    Reed AJ, Dorn R, Van Dover CL, Lutz RA, Vetriani C (2009) Phylogenetic diversity of methanogenic, sulfate-reducing and methanotrophic prokaryotes from deep-sea hydrothermal vents and cold seeps. Deep-Sea Res Pt Ii 56:1665–1674. doi: 10.1016/j.dsr2.2009.05.012 CrossRefGoogle Scholar
  37. 37.
    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. doi: 10.1111/j.1462-2920.2011.02463.x CrossRefPubMedGoogle Scholar
  38. 38.
    Winkel M, Pjevac P, Kleiner M, Littmann S, Meyerdierks A, Amann R, Mussmann M (2014) Identification and activity of acetate-assimilating bacteria in diffuse fluids venting from two deep-sea hydrothermal systems. FEMS Microbiol. Ecol. 90:731–746. doi: 10.1111/1574-6941.12429 CrossRefPubMedGoogle Scholar
  39. 39.
    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. 5:961–976CrossRefPubMedGoogle Scholar
  40. 40.
    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. doi: 10.1111/j.1462-2920.2005.00744.x CrossRefPubMedGoogle Scholar
  41. 41.
    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. doi: 10.1111/j.1574-6941.2011.01161.x CrossRefPubMedGoogle Scholar
  42. 42.
    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. Mar. Genomics. doi: 10.1016/j.margen.2015.09.001 PubMedGoogle Scholar
  43. 43.
    Lallier F (2013) BIOBAZ 2013 cruise, RV Pourquoi pas ?Google Scholar
  44. 44.
    Mccollom TM (2007) Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems. Astrobiology 7:933–950. doi: 10.1089/ast.2006.0119 CrossRefPubMedGoogle Scholar
  45. 45.
    Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4:e7401. doi: 10.1371/journal.pone.0007401 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Pires ACC, Cleary DFR, Almeida A, Cunha A, Dealtry S, Mendonca-Hagler LCS, Smalla K, Gomes NCM (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Appl Environ Microb 78:5520–5528. doi: 10.1128/Aem.00386-12 CrossRefGoogle Scholar
  47. 47.
    Fonseca VG, Carvalho GR, Sung W, Johnson HF, Power DM, Neill SP, Packer M, Blaxter ML, Lambshead PJD, Thomas WK, Creer S (2010) Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nat. Commun. 1. doi: 10.1038/Ncomms1095
  48. 48.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. doi: 10.1038/Nmeth.F.303 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi: 10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  50. 50.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596. doi: 10.1093/nar/gks1219 CrossRefPubMedGoogle Scholar
  51. 51.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267. doi: 10.1128/Aem.00062-07 CrossRefGoogle Scholar
  52. 52.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan’. Community ecology package, version 2.Google Scholar
  53. 53.
    Kolde R (2013) pheatmap—Pretty Heatmaps in R. In: package, R (ed.). CRAN.Google Scholar
  54. 54.
    Dray S, Legendre P, Blanchet G (2009) packfor: Forward Selection with permutation (Canoco p. 46). R package version 00-7/r58.Google Scholar
  55. 55.
    Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefPubMedGoogle Scholar
  56. 56.
    Dias A, Mills R, Taylor R, Ferreira P, Barriga F (2008) Geochemistry of a sediment push-core from the Lucky Strike hydrothermal field, Mid-Atlantic Ridge. Chem. Geol. 247:339–351CrossRefGoogle Scholar
  57. 57.
    Reimann C, Caritat P (1998) Chemical elements in the environment. Factsheets for the geochemist and environmental scientist. Geol. Mag. 137:593–598Google Scholar
  58. 58.
    Ondreas H, Cannat M, Fouquet Y, Normand A, Sarradin PM, Sarrazin J (2009) Recent volcanic events and the distribution of hydrothermal venting at the Lucky Strike hydrothermal field. Mid-Atlantic Ridge. Geochem Geophy Geosy 10. doi: 10.1029/2008gc002171
  59. 59.
    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. doi: 10.1111/j.1462-2920.2005.00856.x CrossRefPubMedGoogle Scholar
  60. 60.
    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. P Natl Acad Sci USA 103:12115–12120. doi: 10.1073/pnas.0605127103 CrossRefGoogle Scholar
  61. 61.
    Takai K, Nakagawa S, Reysenbach AL, Hoek J (2006) Microbial ecology of mid-ocean ridges and back-arc basins. Geophys Monogr Ser 166:185–213Google Scholar
  62. 62.
    Campbell BJ, Polson SW, Allen LZ, Williamson SJ, Lee CK, Wommack KE, Cary SC (2013) Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities. Frontiers in microbiology 4. doi:  10.3389/Fmicb.2013.00182
  63. 63.
    Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiology and molecular biology reviews: MMBR 75:361–422. doi: 10.1128/MMBR.00039-10 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Han Y, Perner M (2015) The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines. Front. Microbiol. 6. doi: 10.3389/fmicb.2015.00989
  65. 65.
    Huber JA, Welch DBM, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100CrossRefPubMedGoogle Scholar
  66. 66.
    Perner M, Hentscher M, Rychlik N, Seifert R, Strauss H, Bach W (2011) Driving forces behind the biotope structures in two low-temperature hydrothermal venting sites on the southern Mid-Atlantic Ridge. Environ. Microbiol. Rep. 3:727–737. doi: 10.1111/j.1758-2229.2011.00291.x CrossRefPubMedGoogle Scholar
  67. 67.
    Perner M, Kuever J, Seifert R, Pape T, Koschinsky A, Schmidt K, Strauss H, Imhoff JF (2007) The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15 degrees N on the Mid-Atlantic Ridge. FEMS Microbiol. Ecol. 61:97–109. doi: 10.1111/j.1574-6941.2007.00325.x CrossRefPubMedGoogle Scholar
  68. 68.
    Desbruyères D, Biscoito M, Caprais JC, Colaco A, Comtet T, Crassous P, Fouquet Y, Khripounoff A, Le Bris N, Olu K, Riso R, Sarradin PM, Segonzac M, Vangriesheim A (2001) Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep-Sea Res Pt I 48:1325–1346. doi: 10.1016/S0967-0637(00)00083-2 CrossRefGoogle Scholar
  69. 69.
    Riou V, Halary S, Duperron S, Bouillon S, Elskens M, Bettencourt R, Santos R, Dehairs F, Colaço A (2008) Influence of CH4 and H2S availability on symbiont distribution, carbon assimilation and transfer in the dual symbiotic vent mussel Bathymodiolus azoricus. Biogeosciences 5:1681–1691CrossRefGoogle Scholar
  70. 70.
    Teske A, Hinrichs KU, Edgcomb V, de Vera GA, 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. Microbiol. 68:1994–2007CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Reysenbach AL, Longnecker K, Kirshtein J (2000) Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic Ridge hydrothermal vent. Appl Environ Microb 66:3798–3806. doi: 10.1128/Aem.66.9.3798-3806.2000 CrossRefGoogle Scholar
  72. 72.
    Reysenbach A-L, Liu Y, Lindgren AR, Wagner ID, Sislak CD, Mets A, Schouten S (2013) Mesoaciditoga lauensis gen. nov., sp. nov., a moderately thermoacidophilic member of the order Thermotogales from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 63:4724–4729CrossRefPubMedGoogle Scholar
  73. 73.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J. Mol. Biol. 215:403–410CrossRefPubMedGoogle Scholar
  74. 74.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol: msw054. doi:  10.1093/molbev/msw054
  75. 75.
    Reysenbach AL, Liu YT, Banta AB, Beveridge TJ, Kirshtein JD, Schouten S, Tivey MK, Von Damm KL, Voytek MA (2006) A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447. doi: 10.1038/Nature04921 CrossRefPubMedGoogle Scholar
  76. 76.
    Embley TM, Finlay BJ (1994) The use of small subunit rRNA sequences to unravel the relationships between anaerobic ciliates and their methanogen endosymbionts. Microbiology 140:225–235CrossRefPubMedGoogle Scholar
  77. 77.
    Yu Z, García-González R, Schanbacher FL, Morrison M (2008) Evaluations of different hypervariable regions of archaeal 16S rRNA genes in profiling of methanogens by Archaea-specific PCR and denaturing gradient gel electrophoresis. Appl Environ Microb 74:889–893CrossRefGoogle Scholar
  78. 78.
    Godfroy A, Lesongeur F, Raguénès G, Quérellou J, Antoine E, Meunier J-R, Guezennec J, Barbier G (1997) Thermococcus hydrothermalis sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 47:622–626Google Scholar
  79. 79.
    Li L, Kato C, Horikoshi K (1999) Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar. Biotechnol. 1:391–400. doi: 10.1007/Pl00011793 CrossRefPubMedGoogle Scholar
  80. 80.
    Li HR, Yu Y, Luo W, Zeng YX, Chen B (2009) Bacterial diversity in surface sediments from the Pacific Arctic Ocean. Extremophiles: life under extreme conditions 13:233–246. doi: 10.1007/s00792-009-0225-7 CrossRefGoogle Scholar
  81. 81.
    Schauer R, Bienhold C, Ramette A, Harder J (2010) Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean. Isme J 4:159–170. doi: 10.1038/ismej.2009.106 CrossRefPubMedGoogle Scholar
  82. 82.
    Kouridaki I, Polymenakou PN, Tselepides A, Mandalakis M, Smith KL (2010) Phylogenetic diversity of sediment bacteria from the deep Northeastern Pacific Ocean: a comparison with the deep Eastern Mediterranean Sea. Int. Microbiol. 13:143–150. doi: 10.2436/20.1501.01.119 PubMedGoogle Scholar
  83. 83.
    Dyksma S, Bischof K, Fuchs BM, Hoffmann K, Meier D, Meyerdierks A, Pjevac P, Probandt D, Richter M, Stepanauskas R (2016) Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. The ISME journal. doi: 10.1038/ismej.2015.257 PubMedPubMedCentralGoogle Scholar
  84. 84.
    Bienhold C, Zinger L, Boetius A, Ramette A (2016) Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLoS One 11:e0148016CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Bowman JP, McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl Environ Microb 69:2463–2483. doi: 10.1128/Aem.69.5.2463-2483.2003 CrossRefGoogle Scholar
  86. 86.
    Geißler A (2003) Molekulare Analyse der bakteriellen Diversität in Uranabraumhalden. Technische Universität Bergakademie FreibergGoogle Scholar
  87. 87.
    Maszenan A, Seviour R, Patel B, Janssen P, Wanner J (2005) Defluvicoccus vanus gen. nov., sp. nov., a novel Gram-negative coccus/coccobacillus in the ‘Alphaproteobacteria’ from activated sludge. Int. J. Syst. Evol. Microbiol. 55:2105–2111CrossRefPubMedGoogle Scholar
  88. 88.
    Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510. doi: 10.1038/35054051 CrossRefPubMedGoogle Scholar
  89. 89.
    Fuhrman J, Davis A (1997) Widespread Archaea and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150:275–285CrossRefGoogle Scholar
  90. 90.
    Takai K, Gamo T, Tsunogai U, Nakayama N, Hirayama H, Nealson KH, 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: life under extreme conditions 8:269–282. doi: 10.1007/s00792-004-0386-3 CrossRefGoogle Scholar
  91. 91.
    Dick GJ, Tebo BM (2010) Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environ. Microbiol. 12:1334–1347. doi: 10.1111/j.1462-2920.2010.02177.x CrossRefPubMedGoogle Scholar
  92. 92.
    Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318:1782–1786. doi: 10.1126/science.1149976 CrossRefPubMedGoogle Scholar
  93. 93.
    Ouverney CC, Fuhrman JA (2000) Marine planktonic archaea take up amino acids. Appl Environ Microb 66:4829–4833CrossRefGoogle Scholar
  94. 94.
    Mason OU, Stingl U, Wilhelm LJ, Moeseneder MM, Meo-Savoie D, Carol A, Fisk MR, Giovannoni SJ (2007) The phylogeny of endolithic microbes associated with marine basalts. Environ. Microbiol. 9:2539–2550CrossRefPubMedGoogle Scholar
  95. 95.
    Song B, Buckner CT, Hembury DJ, Mills RA, Palmer MR (2014) Impact of volcanic ash on anammox communities in deep sea sediments. Environ. Microbiol. Rep. 6:159–166. doi: 10.1111/1758-2229.12137 CrossRefPubMedGoogle Scholar
  96. 96.
    Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM, Martiny JB, Sogin M, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS One 6:e24570CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Campbell MA, Chain PS, Dang H, El Sheikh AF, Norton JM, Ward NL, Ward BB, Klotz MG (2011) Nitrosococcus watsonii sp. nov., a new species of marine obligate ammonia-oxidizing bacteria that is not omnipresent in the world's oceans: calls to validate the names ‘Nitrosococcus halophilus’ and ‘Nitrosomonas mobilis’. FEMS Microbiol. Ecol. 76:39–48CrossRefPubMedGoogle Scholar
  98. 98.
    Wang L, Lim CK, Dang H, Hanson TE, Klotz MG (2016) D1FHS, the type strain of the ammonia-oxidizing bacterium Nitrosococcus wardiae spec. nov.: enrichment, isolation, phylogenetic, and growth physiological characterization. Frontiers in microbiology 7. doi:  10.3389/fmicb.2016.00512
  99. 99.
    Hallberg KB, Hedrich S, Johnson DB (2011) Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron-and sulfur-oxidizer of the family Ectothiorhodospiraceae. Extremophiles: life under extreme conditions 15:271–279CrossRefGoogle Scholar
  100. 100.
    Urich T, Lanzen A, Stokke R, Pedersen RB, Bayer C, Thorseth IH, Schleper C, Steen IH, Ovreas L (2014) Microbial community structure and functioning in marine sediments associated with diffuse hydrothermal venting assessed by integrated meta-omics. Environ. Microbiol. 16:2699–2710. doi: 10.1111/1462-2920.12283 CrossRefPubMedGoogle Scholar
  101. 101.
    Rappé MS, Vergin K, Giovannoni SJ (2000) Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol. Ecol. 33:219–232CrossRefPubMedGoogle Scholar
  102. 102.
    Liu J, Fu B, Yang H, Zhao M, He B, Zhang X-H (2015) Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients. Front. Microbiol. 6:64PubMedPubMedCentralGoogle Scholar
  103. 103.
    Needham DM, Chow C-ET, Cram JA, Sachdeva R, Parada A, Fuhrman JA (2013) Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. The ISME journal 7:1274–1285CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach AL (1999) Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl. Environ. Microbiol. 65:4375–4384PubMedPubMedCentralGoogle Scholar
  105. 105.
    Teske A, Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? The ISME journal 2:3–18CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of Oceanography and FisheriesUniversity of the AzoresHortaPortugal
  2. 2.MARE—Marine and Environmental Sciences Centre—AzoresHortaPortugal
  3. 3.Next Generation Sequencing UnitUCBiotech–CNCCantanhedePortugal
  4. 4.OKEANOS Centre, Department of Oceanography and Fisheries, Faculty of Sciences and TechnologyUniversity of the AzoresHortaPortugal

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