Original Article

A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer

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Abstract

The rock-hosted subseafloor crustal aquifer harbors a reservoir of microbial life that may influence global marine biogeochemical cycles. Here we utilized metagenomic libraries of crustal fluid samples from North Pond, located on the flanks of the Mid-Atlantic Ridge, a site with cold, oxic subseafloor fluid circulation within the upper basement to query microbial diversity. Twenty-one samples were collected during a 2-year period to examine potential microbial metabolism and community dynamics. We observed minor changes in the geochemical signatures over the 2 years, yet the microbial community present in the crustal fluids underwent large shifts in the dominant taxonomic groups. An analysis of 195 metagenome-assembled genomes (MAGs) were generated from the data set and revealed a connection between litho- and autotrophic processes, linking carbon fixation to the oxidation of sulfide, sulfur, thiosulfate, hydrogen, and ferrous iron in members of the Proteobacteria, specifically the Alpha-, Gamma- and Zetaproteobacteria, the Epsilonbacteraeota and the Planctomycetes. Despite oxic conditions, analysis of the MAGs indicated that members of the microbial community were poised to exploit hypoxic or anoxic conditions through the use of microaerobic cytochromes, such as cbb3- and bd-type cytochromes, and alternative electron acceptors, like nitrate and sulfate. Temporal and spatial trends from the MAGs revealed a high degree of functional redundancy that did not correlate with the shifting microbial community membership, suggesting functional stability in mediating subseafloor biogeochemical cycles. Collectively, the repeated sampling at multiple sites, together with the successful binning of hundreds of genomes, provides an unprecedented data set for investigation of microbial communities in the cold, oxic crustal aquifer.

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Acknowledgements

We thank the crews of the R/V Merian and ROV Jason, Wolfgang Bach, Peter Girguis Chih-Chiang Hsieh, Ulrike Jaekel, Beate Kraft, Huei-Ting Lin, Beth Orcutt, Keir Becker, Stephanie Carr, and Heiner Villinger for outstanding support in accomplishing our field programs. Ship time was generously provided by the German Science Foundation (DFG). Both Katrina Edwards and James Cowen’s efforts were critical to the field component and success of this project. They are missed immensely. Leslie Murphy and Emily Reddington provided laboratory support at the WM Keck sequencing facility at the Marine Biological Laboratory. This work was supported by NSF OCE1062006 to JAH and NSF OCE1061827 to BTG. The Gordon and Betty Moore Foundation sponsored most of the observatory components at North Pond through grant GBMF1609. The Center for Dark Energy Biosphere Investigations (C-DEBI) (OCE-0939564), a National Science Foundation-funded Science and Technology Centers of Excellence also supported the participation of CGW, JAH and BJT. This is C-DEBI contribution number 395.

Author information

Affiliations

  1. Center for Dark Energy Biosphere Investigations, University of Southern California, Los Angeles, CA, USA

    • Benjamin J Tully
  2. College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK, USA

    • C Geoff Wheat
  3. Department of Oceanography, University of Hawaii, Honolulu, HI, USA

    • Brain T Glazer
  4. Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, USA

    • Julie A Huber
  5. Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    • Julie A Huber

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Competing interests

The authors declare no conflict of interest.

Corresponding authors

Correspondence to Benjamin J Tully or Julie A Huber.

Supplementary information

Supplementary Information accompanies this paper on The ISME Journal website (http://www.nature.com/ismej)