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Diversity and abundance of Bacteria and nirS-encoding denitrifiers associated with the Juan de Fuca Ridge hydrothermal system

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Abstract

Denitrification, which results in the loss of bioavailable nitrogen—an essential macronutrient for all living organisms—may potentially affect chemosynthetic primary production in hydrothermal vent ecosystems where sub-oxic conditions favorable to denitrification are common. Here we describe the diversity and abundance of denitrifying bacteria in the subsurface biosphere at Axial Volcano and the Endeavour Segment on the Juan de Fuca Ridge using a combination of quantitative polymerase chain reaction assays, and small subunit ribosomal RNA (SSU or 16S rRNA) pyrotag and nitrite reductase (nirS) clone library sequencing methods. Bacterial communities were diverse and dominated by members of the ε- and γ-proteobacteria, including taxonomic groups containing known denitrifiers. Assemblages of denitrifiers that could be evaluated by nirS gene sequence comparisons showed low diversity. The single nirS sequence shared by the two locations, affiliated with a γ-proteobacteria isolated from estuarine sediments (Pseudomonas sp. BA2), represented more than half of all sequences recovered when clustered at 97 % identity. All other nirS sequences clustered into different taxonomic groups, indicating important differences in denitrifier community membership between the two sites. Total nirS gene abundance was at least two orders of magnitude lower than 16S rRNA abundance. Overall, our results demonstrate that the diversity and abundance of the nirS gene-containing bacterial community are rather low, as might be expected under the extreme conditions encountered in the subsurface biosphere of hydrothermal vent systems, and do not correlate clearly with any environmental variables investigated (i.e., pH, temperature, and H2S, NO3 −, NH4 + concentrations).

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Acknowledgments

The authors wish to thank James Holden, Bill Chadwick, the officer and crew of the R/V Atlantis and R/V Thomas G. Thompson and the Jason and Alvin submersible teams. We specially thank Steven J. Hallam for sharing laboratory space and commenting on a previous version of the manuscript. Kevin Roe analyzed fluids for pH, H2S, dissolved silica, and ammonia on board. Hoang-My Christensen analyzed fluids for Mg and other cations and anions in 2009. We thank Elena Zaikova for laboratory assistance and Dr. Juergen Ehlting and Alyse Hawley for sharing laboratory material and space. The Couchsurfing community is thanked for providing accommodation to A.B.. during laboratory analysis at the University of British Columbia (Vancouver). This work was funded through an NSERC (Natural Sciences and Engineering Research Council of Canada) graduate fellowship and a Rix Family fellowship to A.B.., and by an NSERC Discovery grant and British Columbia Leadership Chair to S.K.J. The research cruises were funded by the US National Oceanic and Atmospheric Administration, Pacific Marine Environmental Laboratory and by the National Science Foundation.

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  1. Annie Bourbonnais

    Present address: School for Marine Science and Technology (SMAST), University of Massachusetts Dartmouth, New Bedford, MA, 02744-1221, USA

Authors and Affiliations

  1. School of Earth and Ocean Sciences, University of Victoria, Victoria, BC, V8P 5C2, Canada

    Annie Bourbonnais & S. Kim Juniper

  2. Joint Institute for the Study of the Atmosphere and Ocean, University of Washington, Seattle, WA, 98105-5672, USA

    David A. Butterfield

  3. Pacific Marine Environmental Laboratory, National Oceanic and Atmospheric Administration, Seattle, WA, 98115, USA

    David A. Butterfield

  4. School of Oceanography and Astrobiology, University of Washington, Seattle, WA, 98195-7940, USA

    Rika E. Anderson

  5. Department of Environmental Sciences, University of Basel, 4056, Basel, Switzerland

    Moritz F. Lehmann

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Bourbonnais, A., Juniper, S.K., Butterfield, D.A. et al. Diversity and abundance of Bacteria and nirS-encoding denitrifiers associated with the Juan de Fuca Ridge hydrothermal system. Ann Microbiol 64, 1691–1705 (2014). https://doi.org/10.1007/s13213-014-0813-3

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