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Endemic hydrothermal vent species identified in the open ocean seed bank

Nature Microbiology volume 1, Article number: 16086 (2016) Cite this article

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Abstract

Hydrothermal vent systems host microbial communities among which several microorganisms have been considered endemic to this type of habitat. It is still unclear how these organisms colonize geographically distant hydrothermal environments. Based on 16S rRNA gene sequences, we compare the bacterial communities of sixteen Atlantic hydrothermal vent samples with our own and publicly available global open ocean samples. Analysing sequences obtained from 63 million 16S rRNA genes, the genera we could identify in the open ocean waters contained 99.9% of the vent reads. This suggests that previously observed vent exclusiveness is, in most cases, probably an artefact of lower sequencing depth. These findings are a further step towards elucidating the role of the open ocean as a seed bank. They can explain the predicament of how species expected to be endemic to vent systems are able to colonize geographically distant hydrothermal habitats and contribute to our understanding of whether ‘everything is really everywhere’.

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Figure 1: Percentage of the number and total counts of vent OTUs shared with our southern deep-sea Atlantic Ocean sample.
Figure 2: Prochlorococcus OTUs exhibiting significantly different relative abundances in distinct habitat types.

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References

  1. Gibbons, S. M. et al. Evidence for a persistent microbial seed bank throughout the global ocean. Proc. Natl Acad. Sci. USA 110, 4651–4655 (2013).

    Article  Google Scholar 

  2. Campbell, B. J., Engel, A. S., Porter, M. L. & Takai, K. The versatile ε-proteobacteria: key players in sulphidic habitats. Nature Rev. Microbiol. 4, 458–468 (2006).

    Article  Google Scholar 

  3. Sievert, S. M. & Vetriani, C. Chemoautotrophy at deep-sea vents: past, present, and future. Oceanogr. Mar. Biol. 25, 218–233 (2012).

    Google Scholar 

  4. Perner, M. et al. In-situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. Environ. Microbiol. 15, 1551–1560 (2013).

    Article  Google Scholar 

  5. Huber, J. A. et al. Isolated communities of ε-proteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. FEMS Microbiol. Ecol. 73, 538–549 (2010).

    Google Scholar 

  6. Beaulieu, S. E., Baker, E. T. & German, C. R. Where are the undiscovered hydrothermal vents on oceanic spreading ridges?. Deep-Sea Res. II 121, 202–212 (2015).

    Article  Google Scholar 

  7. Stein, J. & Fisher, A. Observations and models of lateral hydrothermal circulation on a young ridge flank: numerical evaluation of thermal and chemical constraints. G3 4, 1026 (2003).

    Google Scholar 

  8. Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).

    Article  Google Scholar 

  9. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).

    Article  Google Scholar 

  10. Galand, P. E., Casamayor, E. O., Kirchman, D. L. & Lovejoy, C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl Acad. Sci. USA 106, 22427–22432 (2009).

    Article  Google Scholar 

  11. Caporaso, J. G., Paszkiewicz, K., Field, D., Knight, R. & Gilbert, J. A. The western English Channel contains a persistent microbial seed bank. ISME J. 6, 1089–1093 (2012).

    Article  Google Scholar 

  12. Anderson, R., Sogin, M. L. & Baross, J. A. Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vent. FEMS Microbiol. Ecol. 91, 1–11 (2015).

    Article  Google Scholar 

  13. Huber, J. A. et al. Microbial population structures in the deep marine biosphere. Science 318, 97–100 (2007).

    Article  Google Scholar 

  14. Pedrós-Alió, C. Marine microbial diversity: can it be determined? Trends Microbiol. 14, 257–263 (2006).

    Article  Google Scholar 

  15. Friedline, C., Franklin, R., McCallister, S. & Rivera, M. Bacterial assemblages of the eastern Atlantic Ocean reveal both vertical and latitudinal biogeographic signatures. Biogeosciences 9, 2177–2193 (2012).

    Article  Google Scholar 

  16. Sunagawa, S. et al. Ocean plankton. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).

    Article  Google Scholar 

  17. Rideout, J. R. et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2, e545 (2014).

    Article  Google Scholar 

  18. Baas Becking, L. Geobiologie of Inleiding Tot de Milieukunde. in Geobiology or Introduction to the Science of the Environment (Van Stockum & Zoon, 1934).

    Google Scholar 

  19. Liu, Z., Lozupone, C., Hamady, M., Bushman, F. D. & Knight, R. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res. 35, e120 (2007).

    Article  Google Scholar 

  20. Dworkin, M. & Falkow, S. The Prokaryotes: A Handbook on the Biology of Bacteria 3rd edn (Springer, 2006).

    Book  Google Scholar 

  21. Zielinski, F. U. et al. Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ. Microbiol. 11, 1150–1167 (2009).

    Article  Google Scholar 

  22. Wentrup, C., Wendeberg, A., Schimak, M., Borowski, C. & Dubilier, N. Forever competent: deep-sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime. Environ. Microbiol. 16, 3699–3713 (2014).

    Article  Google Scholar 

  23. Rocap, G. et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042–1047 (2003).

    Article  Google Scholar 

  24. Perner, M. et al. Linking geology, fluid chemistry and microbial activity of basalt- and ultramafic-hosted deep-sea hydrothermal vent environments. Geobiology 11, 340–355 (2013).

    Article  Google Scholar 

  25. Garbe-Schönberg, D., Jähmlich, H., Koschinsky, A., Ratmeyer, V. & Westernströer, U. KIPS—a new multiport valve-based all-Teflon fluid sampling system for ROVs. EGU Meeting, Geophys. Res. Abstr. 8, 07032 (2006).

  26. Perner, M. et al. Short-term microbial and physico-chemical variability in low-temperature hydrothermal fluids near 5°S on the Mid-Atlantic Ridge. Environ. Microbiol. 11, 2526–2541 (2009).

    Article  Google Scholar 

  27. 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 (2013).

    Article  Google Scholar 

  28. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  Google Scholar 

  29. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357–359 (2012).

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Caporaso, J. G., Kuczynski, J. & Stombaugh, J. QIIME allows analysis of high-throughput community sequencing data. Nature 7, 335–336 (2010).

    Google Scholar 

  32. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).

    Article  Google Scholar 

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

    Article  Google Scholar 

  34. Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267 (2010).

    Article  Google Scholar 

  35. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article  Google Scholar 

  36. Chao, A. et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).

    Article  Google Scholar 

  37. Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J. & Knight, R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 5, 169–172 (2011).

    Article  Google Scholar 

  38. Leinonen, R., Sugawara, H. & Shumway, M. The sequence read archive. Nucleic Acids Res. 39, D19–D21 (2011).

    Article  Google Scholar 

  39. Huse, S. M. et al. VAMPS: a website for visualization and analysis of microbial population structures. BMC Bioinformatics 15, 41 (2014).

    Article  Google Scholar 

  40. Egbert, G. & Erofeeva, S. Efficient inverse modeling of barotropic ocean tides. J. Atmos. Ocean. Technol. 19, 183–204 (2002).

    Article  Google Scholar 

  41. Walter, M. et al. Rapid dispersal of a hydrothermal plume by turbulent mixing. Deep-Sea Res I 57, 931–945 (2010).

    Article  Google Scholar 

  42. Carpenter, J. H. The Chesapeake Bay Institute technique for the Winkler dissolved oxygen method. Limnol. Oceanogr. 10, 141–143 (1965).

    Article  Google Scholar 

  43. Cline, J. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14, 454–458 (1969).

    Article  Google Scholar 

  44. Perner, M. et al. The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15°N on the Mid-Atlantic Ridge. FEMS Microbiol. Ecol. 61, 97–109 (2007).

    Article  Google Scholar 

  45. Seifert, R. et al. Ethylene and methane in the upper water column of the subtropical Atlantic. Biogeochemistry 44, 73–91 (1999).

    Google Scholar 

  46. Schmidt, K. A. et al. Fluid elemental and stable isotope composition of the Nibelungen hydrothermal field (8°18′S, Mid-Atlantic Ridge): constraints on fluid–rock interaction in heterogeneous lithosphere. Chem. Geol. 280, 1–18 (2011).

    Article  Google Scholar 

  47. Schmidt, K., Koschinsky, A., Garbe-Schönberg, D., de Carvalho, L. M. & Seifert, R. Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15°N on the Mid-Atlantic Ridge: temporal and spatial investigation. Chem. Geol. 242, 1–21 (2007).

    Article  Google Scholar 

  48. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).

    Google Scholar 

Download references

Acknowledgements

The authors thank the captain and crews of the research vessels and ROV Kiel6000 (GEOMAR, Kiel) for helping us to obtain deep-sea vent samples. The authors also thank H. Strauss for providing data on hydrogen sulfide and M. Alawi for discussions regarding the sequencing and bioinformatics analysis. The work was supported by grants from priority programme 1144 ‘From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes’ of the German Science Foundation (DFG). S.B. was funded by grant no. DFG PE 1549-6/1.

Author information

Authors and Affiliations

  1. Center for Bioinformatics, University of Hamburg, Bundesstraße 43, 20146 Hamburg, Germany

    Giorgio Gonnella & Stefan Kurtz

  2. Molecular Biology of Microbial Consortia, University of Hamburg, Biocenter Klein Flottbek, Ohnhorststraße 18, 22609 Hamburg, Germany

    Stefanie Böhnke & Mirjam Perner

  3. Heinrich-Pette-Institut, Leibniz Institute for Experimental Virology, Martinistraße 52, 20251 Hamburg, Germany

    Daniela Indenbirken

  4. Institute of Geosciences, University of Kiel, Ludewig-Meyn-Straße 10, 24118 Kiel, Germany

    Dieter Garbe-Schönberg

  5. Institute for Geology, University of Hamburg, Bundesstraße 55, 20146 Hamburg, Germany

    Richard Seifert

  6. Institute of Environmental Physics, University Bremen, Otto-Hahn-Allee 1, 28359 Bremen, Germany

    Christian Mertens

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  1. Giorgio Gonnella
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Contributions

M.P. designed the research project, planned the sequencing and wrote the paper. G.G. co-planned the sequencing, performed bioinformatics and statistical analyses and wrote the paper. S.B. performed experiments. D.I. performed sequencing. D.G.-S. contributed fluid elemental compositions and geochemical data. R.S. measured hydrogen and methane concentrations. C.M. performed tidal measurements. S.K. advised on the bioinformatics analyses and wrote the paper.

Corresponding author

Correspondence to Mirjam Perner.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Results and Discussion 1-4, Supplementary Figures 1-6, Supplementary Tables 1-4, Supplementary Table legends 5-10, and Supplementary References (PDF 896 kb)

Supplementary Table 5

Genera shared between hydrothermal vent and open ocean samples. (XLSX 190 kb)

Supplementary Table 6

Open-reference based OTUs shared between hydrothermal vent and open ocean samples. (XLSX 1109 kb)

Supplementary Table 7

Environmental parameters of the different samples used for correlation analyses. (XLSX 14 kb)

Supplementary Table 8

Spearman correlations for the different sites between environmental parameters and bacterial classes. (XLSX 31 kb)

Supplementary Table 9

Spearman correlations for the different sites between environmental parameters and bacterial genera. (XLSX 78 kb)

Supplementary Table 10

Spearman correlations for the different sites between environmental parameters and bacterial OTUs. (XLSX 2668 kb)

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Gonnella, G., Böhnke, S., Indenbirken, D. et al. Endemic hydrothermal vent species identified in the open ocean seed bank. Nat Microbiol 1, 16086 (2016). https://doi.org/10.1038/nmicrobiol.2016.86

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