Advertisement

Microbial community differentiation between active and inactive sulfide chimneys of the Kolumbo submarine volcano, Hellenic Volcanic Arc

Abstract

Over the last decades, there has been growing interest about the ecological role of hydrothermal sulfide chimneys, their microbial diversity and associated biotechnological potential. Here, we performed dual-index Illumina sequencing of bacterial and archaeal communities on active and inactive sulfide chimneys collected from the Kolumbo hydrothermal field, situated on a geodynamic convergent setting. A total of 15,701 OTUs (operational taxonomic units) were assigned to 56 bacterial and 3 archaeal phyla, 133 bacterial and 16 archaeal classes. Active chimney communities were dominated by OTUs related to thermophilic members of Epsilonproteobacteria, Aquificae and Deltaproteobacteria. Inactive chimney communities were dominated by an OTU closely related to the archaeon Nitrosopumilus sp., and by members of Gammaproteobacteria, Deltaproteobacteria, Planctomycetes and Bacteroidetes. These lineages are closely related to phylotypes typically involved in iron, sulfur, nitrogen, hydrogen and methane cycling. Overall, the inactive sulfide chimneys presented highly diverse and uniform microbial communities, in contrast to the active chimney communities, which were dominated by chemolithoautotrophic and thermophilic lineages. This study represents one of the most comprehensive investigations of microbial diversity in submarine chimneys and elucidates how the dissipation of hydrothermal activity affects the structure of microbial consortia in these extreme ecological niches.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Change history

  • 01 March 2018

    In the original publication there is a mistake in the supplementary material. The correct supplementary material is provided in this correction article.

References

  1. Black M, Moolhuijzen P, Chapman B et al (2012) The genetics of symbiotic nitrogen fixation: comparative genomics of 14 Rhizobia strains by resolution of protein clusters. Genes (Basel) 3:138–166. doi:10.3390/genes3010138

  2. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170

  3. Bonch-Osmolovskaya EA, Sokolova TG, Kostrikina NA, Zavarzin GA (1990) Desulfurella acetivorans gen. nov. and sp. nov.—a new thermophilic sulfur-reducing eubacterium. Arch Microbiol 153:151–155. doi:10.1007/BF00247813

  4. Brazelton WJ, Baross JA (2010) Metagenomic comparison of two Thiomicrospira lineages inhabiting contrasting deep-sea hydrothermal environments. PLoS One 5:e13530. doi:10.1371/journal.pone.0013530

  5. Brazelton WJ, Ludwig KA, Sogin ML et al (2010) Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys. Proc Natl Acad Sci 107:1612–1617. doi:10.1073/pnas.0905369107

  6. Campbell BJ, Polson SW, Zeigler Allen L et al (2013) Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities. Front Microbiol 4:182. doi:10.3389/fmicb.2013.00182

  7. Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8

  8. Carey S, Bell KLC, Nomikou P et al (2011) Exploration of the Kolumbo volcanic rift zone. In: Bell KLC, Fuller SA (eds) New frontiers in ocean exploration: the E/V Nautilus 2010 field season. Oceanography, vol 24, no 1 supplement, pp 24–25

  9. Carey S, Nomikou P, Bell KC et al (2013) CO2 degassing from hydrothermal vents at Kolumbo submarine volcano, Greece, and the accumulation of acidic crater water. Geology 41:1035–1038. doi:10.1130/G34286.1

  10. Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. doi:10.1093/nar/gkt1244

  11. Dahle H, Okland I, Thorseth IH et al (2015) Energy landscapes shape microbial communities in hydrothermal systems on the Arctic Mid-Ocean Ridge. ISME J 9:1593–1606

  12. DeSantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. doi:10.1128/AEM.03006-05

  13. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

  14. Elderfield H, Schultz A (1996) Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Annu Rev Earth Planet Sci 24:191–224. doi:10.1146/annurev.earth.24.1.191

  15. Elshahed MS, Youssef NH, Luo Q et al (2007) Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma. Appl Environ Microbiol 73:4707–4716. doi:10.1128/AEM.00591-07

  16. Flores GE, Campbell JH, Kirshtein JD et 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

  17. Flores GE, Shakya M, Meneghin J et al (2012) Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10:333–346. doi:10.1111/j.1472-4669.2012.00325.x

  18. Frank KL, Rogers DR, Olins HC et al (2013) Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents. ISME J 7:1391–1401

  19. He T, Zhang X (2016) Characterization of bacterial communities in deep-sea hydrothermal vents from three oceanic regions. Mar Biotechnol (NY) 18:232–241. doi:10.1007/s10126-015-9683-3

  20. Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564. doi:10.1099/mic.0.045344-0

  21. Hübscher C, Ruhnau M, Nomikou P (2015) Volcano-tectonic evolution of the polygenetic Kolumbo submarine volcano/Santorini (Aegean Sea). J Volcanol Geotherm Res 291:101–111. doi:10.1016/j.jvolgeores.2014.12.020

  22. Hügler M, Huber H, Molyneaux SJ et al (2007) Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ Microbiol 9:81–92. doi:10.1111/j.1462-2920.2006.01118.x

  23. Jaeschke A, Jørgensen SL, Bernasconi SM et al (2012) Microbial diversity of Loki’s Castle black smokers at the Arctic Mid-Ocean Ridge. Geobiology 10:548–561. doi:10.1111/gbi.12009

  24. Jiang L, Long M, Shao Z (2014) Draft genome sequence of Defluviimonas indica strain 20V17T, isolated from a deep-sea hydrothermal vent environment in the Southwest Indian Ocean. Genome Announc 2:e00479–e00514. doi:10.1128/genomeA.00479-14

  25. Kato S, Takano Y, Kakegawa T et al (2010) Biogeography and biodiversity in sulfide structures of active and inactive vents at deep-sea hydrothermal fields of the Southern Mariana Trough. Appl Environ Microbiol 76:2968–2979. doi:10.1128/AEM.00478-10

  26. Kato S, Nakamura K, Toki T et al (2012) Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the Southern Mariana Trough. Front Microbiol 3:89. doi:10.3389/fmicb.2012.00089

  27. Kilias SP, Nomikou P, Papanikolaou D et al (2013) New insights into hydrothermal vent processes in the unique shallow-submarine arc-volcano, Kolumbo (Santorini), Greece. Sci Rep 3:2421. doi:10.1038/srep02421

  28. Kolde R (2015) Pheatmap: pretty heatmaps version 1.0.8. https://CRAN.R-project.org/package=pheatmap. Accessed 28 May 2017

  29. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

  30. Lee MD, Walworth NG, Sylvan JB et al (2015) Microbial communities on seafloor basalts at Dorado Outcrop reflect level of alteration and highlight global lithic clades. Front Microbiol 6:1470. doi:10.3389/fmicb.2015.01470

  31. Lesniewski RA, Jain S, Anantharaman K et al (2012) The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J 6:2257–2268. doi:10.1038/ismej.2012.63

  32. Macur RE, Jay ZJ, Taylor WP et al (2013) Microbial community structure and sulfur biogeochemistry in mildly-acidic sulfidic geothermal springs in Yellowstone National Park. Geobiology 11:86–99. doi:10.1111/gbi.12015

  33. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10

  34. Mccollom TM, Shock EL (1997) Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61:4375–4391. doi:10.1016/S0016-7037(97)00241-X

  35. Miroshnichenko ML, L’Haridon S, Jeanthon C et al (2003) Oceanithermus profundus gen. nov., sp. nov., a thermophilic, microaerophilic, facultatively chemolithoheterotrophic bacterium from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 53:747–752. doi:10.1099/ijs.0.02367-0

  36. Nomikou P, Carey S, Papanikolaou D et al (2012) Submarine volcanoes of the Kolumbo volcanic zone NE of Santorini Caldera, Greece. Glob Planet Change 90–91:135–151. doi:10.1016/j.gloplacha.2012.01.001

  37. Nomikou P, Hübscher C, Ruhnau M, Bejelou K (2016) Tectono-stratigraphic evolution through successive extensional events of the Anydros Basin, hosting Kolumbo volcanic field at the Aegean Sea, Greece. Tectonophysics 671:202–217. doi:10.1016/j.tecto.2016.01.021

  38. Oksanen J, Blanchet G, Friendly M et al (2017) Vegan: community ecology package version 2.4-4. https://CRAN.R-project.org/package=vegan. Accessed 28 May 2017

  39. Olins HC, Rogers DR, Frank KL et al (2013) Assessing the influence of physical, geochemical and biological factors on anaerobic microbial primary productivity within hydrothermal vent chimneys. Geobiology 11:279–293. doi:10.1111/gbi.12034

  40. 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. doi:10.1128/MMBR.00039-10

  41. Oulas A, Polymenakou PN, Seshadri R et al (2016) Metagenomic investigation of the geologically unique Hellenic Volcanic Arc reveals a distinctive ecosystem with unexpected physiology. Environ Microbiol 18:1122–1136. doi:10.1111/1462-2920.13095

  42. Pereira IAC, Ramos AR, Grein F et al (2011) A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front Microbiol 2:69. doi:10.3389/fmicb.2011.00069

  43. Quast C, Pruesse E, Yilmaz P et al (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

  44. Reveillaud J, Reddington E, McDermott J et al (2015) Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman Rise. Environ Microbiol 18:1970–1987. doi:10.1111/1462-2920.13173

  45. Rizzo AL, Caracausi A, Chavagnac V et al (2016) Kolumbo submarine volcano (Greece): an active window into the Aegean subduction system. Sci Rep 6:28013

  46. Salter SJ, Cox MJ, Turek EM et al (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. doi:10.1186/s12915-014-0087-z

  47. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

  48. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

  49. Schmidt I (2002) Aerobic and anaerobic ammonia oxidizing bacteria—competitors or natural partners? FEMS Microbiol Ecol 39:175–181. doi:10.1016/S0168-6496(01)00208-2

  50. Sigurdsson H, Carey S, Alexandri M et al (2006) Marine investigations of Greece’s Santorini Volcanic Field. EOS Trans Am Geophys Union 87:337–348. doi:10.1029/2006EO340001

  51. Spieck E, Bock E (2005) The lithoautotrophic nitrite-oxidizing bacteria. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s Manual® of systematic bacteriology: volume two: the Proteobacteria, part A introductory essays. Springer, Boston, pp 149–153

  52. Suzuki Y, Inagaki F, Takai K et al (2004) Microbial diversity in inactive chimney structures from deep-sea hydrothermal systems. Microb Ecol 47:186–196. doi:10.1007/s00248-003-1014-y

  53. Sylvan JB, Toner BM, Edwards KJ (2012) Life and death of deep-sea vents: bacterial diversity and ecosystem succession on inactive hydrothermal sulfides. MBio 3:e00279–e00311. doi:10.1128/mBio.00279-11

  54. Sylvan JB, Sia TY, Haddad AG et al (2013) Low temperature geomicrobiology follows host rock composition along a geochemical gradient in Lau Basin. Front Microbiol 4:61

  55. Takai K, Nakagawa S, Reysenbach AL, Hoek J (2006) Microbial ecology of Mid-Ocean Ridges and Back-Arc basins. In: Christie DM, Fisher CR, Lee S-M, Givens S (eds) Back-Arc spreading systems: geological, biological, chemical, and physical interactions. American Geophysical Union, pp 185–213

  56. Tanner MA, Goebel BM, Dojka MA, Pace NR (1998) Specific ribosomal DNA sequences from diverse environmental settings correlate with experimental contaminants. Appl Environ Microbiol 64:3110–3113

  57. Tivey MK (2004) Environmental conditions within active seafloor vent structures: sensitivity to vent fluid composition and fluid flow. Subseafloor Biosph Mid-Ocean Ridges. doi:10.1029/144GM09

  58. Toner BM, Lesniewski RA, Marlow JJ et al (2013) Mineralogy drives bacterial biogeography of hydrothermally inactive seafloor sulfide deposits. Geomicrobiol J 30:313–326. doi:10.1080/01490451.2012.688925

  59. Vetriani C, Voordeckers JW, Crespo-Medina M et al (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

  60. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

  61. Zhang Y, Zhao Z, Chen C-TA et al (2013) Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities. Front Microbiol 4:1–11. doi:10.3389/fmicb.2013.00182

Download references

Acknowledgements

The authors acknowledge the captain and crew of R/V Aegaeo and the ROV Team for their assistance during sampling. Especially acknowledged are T. Dailianis for providing the photographs of the chimney samples upon recovery and S. Kilias for his guidance during collection of the samples. We would like to thank M. Pettas, A. Kristallas, M. Maidanou for their assistance during sampling. This work was funded by the EU-FP7 project SeaBioTech (spider.science.strath.ac.uk/seabiotech) with Grant number 311932 and the General Secretariat for Research and Technology-GSRT and Siemens A.G. through the project “Programmatic agreements between Research Centres–GSRT 2015–2017”.

Author information

CC, PNP, MM, and PN performed the sampling. CC performed most of the laboratory analysis. CC and J-BK performed the sequencing analysis. PN and DL constructed the detailed bathymetric maps. PNP, GK and AM conceived the project and led the research process. CC, PNP, MM and PN processed the data and drafted the manuscript. All authors discussed the results and approved on the manuscript.

Correspondence to Paraskevi N. Polymenakou.

Ethics declarations

Conflict of interest

The authors declare that no conflict of interest exists.

Additional information

A correction to this article is available online at https://doi.org/10.1007/s00792-018-1017-8.

Communicated by H. Atomi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 4 (WMV 23622 kb)

Supplementary material 5 (WMV 24707 kb)

Supplementary material 1 (DOCX 433 kb)

Supplementary material 2 (XLSX 43 kb)

Supplementary material 3 (XLSX 143 kb)

Supplementary material 4 (WMV 23622 kb)

Supplementary material 5 (WMV 24707 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Christakis, C.A., Polymenakou, P.N., Mandalakis, M. et al. Microbial community differentiation between active and inactive sulfide chimneys of the Kolumbo submarine volcano, Hellenic Volcanic Arc. Extremophiles 22, 13–27 (2018) doi:10.1007/s00792-017-0971-x

Download citation

Keywords

  • Hydrothermal chimneys
  • Submarine volcano
  • Microbial diversity
  • Illumina sequencing
  • Microbial communities