A submarine volcanic eruption leads to a novel microbial habitat

  • A Corrigendum to this article was published on 22 May 2017


Submarine volcanic eruptions are major catastrophic events that allow investigation of the colonization mechanisms of newly formed seabed. We explored the seafloor after the eruption of the Tagoro submarine volcano off El Hierro Island, Canary Archipelago. Near the summit of the volcanic cone, at about 130 m depth, we found massive mats of long, white filaments that we named Venus’s hair. Microscopic and molecular analyses revealed that these filaments are made of bacterial trichomes enveloped within a sheath and colonized by epibiotic bacteria. Metagenomic analyses of the filaments identified a new genus and species of the order Thiotrichales, Thiolava veneris. Venus’s hair shows an unprecedented array of metabolic pathways, spanning from the exploitation of organic and inorganic carbon released by volcanic degassing to the uptake of sulfur and nitrogen compounds. This unique metabolic plasticity provides key competitive advantages for the colonization of the new habitat created by the submarine eruption. A specialized and highly diverse food web thrives on the complex three-dimensional habitat formed by these microorganisms, providing evidence that Venus’s hair can drive the restart of biological systems after submarine volcanic eruptions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Macroscopic and microscopic view of the Venus’s hair.
Figure 2: Phylogenomic analyses on genome bins reconstructed from the Venus’s hair metagenome.
Figure 3: Metabolic potential of Thiolava veneris.
Figure 4: Output of prokaryotic 16S rDNA sequencing.


  1. 1

    Smith, D. K. & Cann, J. R. The role of seamount volcanism in crustal construction at the Mid-Atlantic Ridge (24°–30° N). J. Geophys. Res. 97, 1645–1658 (1992).

    Article  Google Scholar 

  2. 2

    Rubin, K. H. et al. Volcanic eruptions in the deep sea. Oceanography 25, 142–157 (2012).

    Article  Google Scholar 

  3. 3

    Rivera, J. et al. Construction of an oceanic island: insights from El Hierro 2011–12 submarine volcanic eruption. Geology 41, 355–358 (2013).

    Article  Google Scholar 

  4. 4

    Fraile-Nuez, E. et al. The submarine volcano eruption at the island of El Hierro: physical–chemical perturbation and biological response. Sci. Rep. 2, 486 (2012).

    Article  Google Scholar 

  5. 5

    Santana-Casiano, J. M. et al. The natural ocean acidification and fertilization event caused by the submarine eruption of El Hierro. Sci. Rep. 3, 1140 (2013).

    Article  Google Scholar 

  6. 6

    Ferrera, I. et al. Effects of the submarine volcanic eruption of El Hierro (Canary Islands) on the bacterioplankton communities of the surrounding. PLoS ONE 10, e0118136 (2014).

    Article  Google Scholar 

  7. 7

    Gulmann, L. K. et al. Bacterial diversity and successional patterns during biofilm formation on freshly exposed basalt surfaces at diffuse-flow deep-sea vents. Front. Microbiol. 6, 901 (2015).

    Article  Google Scholar 

  8. 8

    Meyer, J. L., Akerman, N. H., Proskurowski, G. & Huber, J. A. Microbiological characterization of post-eruption “snowblower” vents at Axial Seamount, Juan de Fuca Ridge. Front. Microbiol. 4, 153 (2013).

    Google Scholar 

  9. 9

    Emerson, D. & Moyer, C. L. Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl. Environ. Microbiol. 68, 3085–3093 (2002).

    Article  Google Scholar 

  10. 10

    Garcia, M., Caplan-Auerbach, J., De Carlo, E., Kurz, M. D. & Becker, N. Geology, geochemistry and earthquake history of Lō`ihi seamount, Hawai`i’s youngest volcano. Chem. Erde Geochem. 66, 81–108 (2006).

    Article  Google Scholar 

  11. 11

    de Ronde, C. E. et al. Evolution of a submarine magmatic-hydrothermal system: Brothers volcano, southern Kermadec arc, New Zealand. Econ. Geol. 100, 1097–1133 (2005).

    Article  Google Scholar 

  12. 12

    Baker, E. T. et al. Hydrothermal activity and volcano distribution along the Mariana arc. J. Geophys. Res. 113, B8 (2008).

    Article  Google Scholar 

  13. 13

    Kelley, D. S., Baross, J. A. & Delaney, J. R. Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu. Rev. Earth Planet. Sci. 30, 385–491(2002).

    Article  Google Scholar 

  14. 14

    Rivera, J. et al. Morphometry of Concepcion Bank: evidence of geological and biological processes on a large volcanic seamount of the Canary Islands Seamount Province. PLoS ONE 11, e0156337 (2016).

    Article  Google Scholar 

  15. 15

    Pérez-Torrado, F. J. et al. La erupción submarina de La Restinga en la isla de El Hierro, Canarias: Octubre 2011–Marzo 2012. Estud. Geol. 68, 5–27 (2012).

    Article  Google Scholar 

  16. 16

    Santana-Casiano, J. M. et al. Significant discharge of CO2 from hydrothermalism associated with the submarine volcano of El Hierro Island. Sci. Rep. 6, 25686 (2016).

  17. 17

    Jørgensen, B. B. & Gallardo, V. A. Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles. FEMS Microbiol. Ecol. 28, 301–313 (1999).

    Article  Google Scholar 

  18. 18

    Preisler, A. et al. Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J. 1, 341–353 (2007).

    Article  Google Scholar 

  19. 19

    Kojima, H. et al. Ecophysiology of Thioploca ingrica as revealed by the complete genome sequence supplemented with proteomic evidence. ISME J. 9, 1166–1176 (2015).

    Article  Google Scholar 

  20. 20

    Klatt, J. M. & Polerecky, L. Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation. Front. Microbiol. 6, 484 (2014).

    Google Scholar 

  21. 21

    Albareda, M. et al. Dual role of HupF in the biosynthesis of [NiFe] hydrogenase in Rhizobium leguminosarum. BMC Microbiol. 12, 256 (2012).

    Article  Google Scholar 

  22. 22

    Stewart, F., Dmytrenko, O., DeLong, E. & Cavanaugh, C. Metatranscriptomic analysis of sulfur oxidation genes in the endosymbiont of Solemya velum. Front. Microbiol. 2, 134 (2011).

    Article  Google Scholar 

  23. 23

    Sanders, J. G., Beinart, R. A., Stewart, F. J., Delong, E. F. & Girguis, P. R. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J. 7, 1556–1567 (2013).

    Article  Google Scholar 

  24. 24

    Hügler, M. & Sievert, S. M. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Ann. Rev. Mar. Sci. 3, 261–289 (2011).

    Article  Google Scholar 

  25. 25

    Oulas, A. et al. Metagenomic investigation of the geologically unique Hellenic Volcanic Arc reveals a distinctive ecosystem with unexpected physiology. Environ. Microbiol. 18, 1122–1136 (2016).

    Article  Google Scholar 

  26. 26

    Kirchman, D. L. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39, 91–100 (2002).

    Google Scholar 

  27. 27

    Klatt, J. M. et al. Structure and function of natural sulphide-oxidizing microbial mats under dynamic input of light and chemical energy. ISME J. 10, 921–933 (2016).

    Article  Google Scholar 

  28. 28

    Van Gaever, S. et al. Trophic specialisation of metazoan meiofauna at the Håkon Mosby mud volcano: fatty acid biomarker isotope evidence. Mar. Biol. 156, 1289–1296 (2009).

    Article  Google Scholar 

  29. 29

    Tchesunov, A. V. Free-living nematode species (Nematoda) dwelling in hydrothermal sites of the North Mid-Atlantic Ridge. Helgoland Mar. Res. 69, 343 (2015).

    Article  Google Scholar 

  30. 30

    Noble, R. T. & Fuhrman, J. A. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14, 113–118 (1998).

    Article  Google Scholar 

  31. 31

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS  Article  Google Scholar 

  32. 32

    Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002).

    Article  Google Scholar 

  33. 33

    Teira, E., Reinthaler, T., Pernthaler, A., Pernthaler, J. & Herndl, G. J. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Appl. Environ. Microbiol. 70, 4411–4414 (2004).

    Article  Google Scholar 

  34. 34

    Molari, M. & Manini, E. Reliability of CARD-FISH procedure for enumeration of Archaea in deep-sea surficial sediments. Curr. Microbiol. 64, 242–250 (2012).

    Article  Google Scholar 

  35. 35

    Hazrin-Chong, N. H. & Manefield, M. An alternative SEM drying method using hexamethyldisilazane (HMDS) for microbial cell attachment studies on sub-bituminous coal. J. Microbiol. Meth. 90, 96–99 (2012).

    Article  Google Scholar 

  36. 36

    Fischer, C. B., Rohrbeck, M., Wehner, S., Richter, M. & Schmeißer, D. Interlayer formation of diamond-like carbon coatings on industrial polyethylene: thickness dependent surface characterization by SEM, AFM and NEXAFS. Appl. Surf. Sci. 271, 381–389 (2013).

    Article  Google Scholar 

  37. 37

    Ratti, S., Knoll, A. H. & Giordano, M. Grazers and phytoplankton growth in the oceans: an experimental and evolutionary perspective. PLoS ONE 8, e77349 (2013).

    Article  Google Scholar 

  38. 38

    Hoppe, H. G. in Handbook of Methods in Aquatic Microbial Ecology (eds Kemp, P. F. et al.) 423–431 (CRC, 1993).

    Google Scholar 

  39. 39

    Corinaldesi, C., Tangherlini, M., Luna, G. M. & Dell’Anno, A. Extracellular DNA can preserve the genetic signatures of present and past viral infection events in deep hypersaline anoxic basins. Proc. R. Soc. B 281, 20133299 (2014).

    Article  Google Scholar 

  40. 40

    Danovaro, R. Methods for the Study of Deep-Sea Sediments, their Functioning and Biodiversity (CRC, 2010).

    Google Scholar 

  41. 41

    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2012).

    Article  Google Scholar 

  42. 42

    Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).

    Article  Google Scholar 

  43. 43

    Schmieder, R. & Edwards, R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863–864 (2011).

    Article  Google Scholar 

  44. 44

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    Article  Google Scholar 

  45. 45

    Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).

    Google Scholar 

  46. 46

    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    Article  Google Scholar 

  47. 47

    Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015).

    Article  Google Scholar 

  48. 48

    Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    Article  Google Scholar 

  49. 49

    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    Article  Google Scholar 

  50. 50

    Laczny, C. C. et al. VizBin—an application for reference-independent visualization and human-augmented binning of metagenomic data. Microbiome 3, 1 (2015).

    Article  Google Scholar 

  51. 51

    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article  Google Scholar 

  52. 52

    Segata, N., Börnigen, D., Morgan, X. C. & Huttenhower, C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microorganisms. Nat. Commun. 4, 2304 (2013).

    Article  Google Scholar 

  53. 53

    Li, D., Liu, C. M., Luo, R., Sadakane, K. & Lam, T. W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).

    Article  Google Scholar 

  54. 54

    Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 19 (2010).

    Article  Google Scholar 

  55. 55

    Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).

    Article  Google Scholar 

  56. 56

    Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).

    Article  Google Scholar 

  57. 57

    Rodriguez-R, L. M. & Konstantinidis, K. T. Bypassing cultivation to identify bacterial species. Microbe 9, 111–118 (2014).

    Google Scholar 

  58. 58

    Menzel, P., Ng, K. L. & Krogh, A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat. Commun. 7, 11257 (2016).

    Article  Google Scholar 

  59. 59

    Benoit, G. et al. Multiple comparative metagenomics using multiset k-mer counting. Preprint at https://arxiv.org/abs/1604.02412 (2016).

Download references


This work was carried out within the frame of the project MIDAS (GA n. 603418, EU FPVII) for which the Ministerio de Economía y Competitividad (MINECO) and Instituto Español de Oceanogafía (IEO) provided ship time and the ROV. Technical staff were provided by IEO and Consejo Superior de Investigaciones Científicas (CSIC) Unidad de Tecnología Marina. Generalitat de Catalunya supported Grup de Recerca Consolidat (GRC) en Geociències Marines through grant 2014 SGR 1068. We thank the crew and officers of the RV Ángeles Alvariño for their help during the cruise. A.S.-V. was supported by a Ramón y Cajal contract from MINECO. R.D. was supported by the project MERCES (Marine Ecosystem Restoration in Changing European Seas, EU2020, grant agreement no. 689518). D.A. was supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 658358.

Author information




R.D. and M.C. conceived the study. M.C., G.L. and A.M.C. led the research cruise where the Venus’s hair mats were found, and mapped and sampled them. J.R. played a pivotal role in the ROV operations. M.T., D.A., J.F., R.P.-P. and X.R. performed the fieldwork. A.S.-V. performed the substrate rock analyses. M.T., A.D.A. and C.C. carried out the bioinformatic analyses. C.G. performed the extraction and classification of the meiofaunal organisms. C.C., A.D.A. and M.T. conducted the laboratory analyses. R.D., M.C., C.C., A.D.A., C.G. and M.T. wrote the manuscript. G.L., A.S.-V and A.M.C. critically read and contributed to the manuscript.

Corresponding author

Correspondence to Roberto Danovaro.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Tables 1–4, Supplementary Figures 1–6. (PDF 2349 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Danovaro, R., Canals, M., Tangherlini, M. et al. A submarine volcanic eruption leads to a novel microbial habitat. Nat Ecol Evol 1, 0144 (2017). https://doi.org/10.1038/s41559-017-0144

Download citation

Further reading


Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing