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Carbon fixation and energy metabolisms of a subseafloor olivine biofilm

The ISME Journal (2019) | Download Citation

Abstract

Earth’s largest aquifer ecosystem resides in igneous oceanic crust, where chemosynthesis and water-rock reactions provide the carbon and energy that support an active deep biosphere. The Calvin Cycle is the predominant carbon fixation pathway in cool, oxic, crust; however, the energy and carbon metabolisms in the deep thermal basaltic aquifer are poorly understood. Anaerobic carbon fixation pathways such as the Wood-Ljungdahl pathway, which uses hydrogen (H2) and CO2, may be common in thermal aquifers since water-rock reactions can produce H2 in hydrothermal environments and bicarbonate is abundant in seawater. To test this, we reconstructed the metabolisms of eleven bacterial and archaeal metagenome-assembled genomes from an olivine biofilm obtained from a Juan de Fuca Ridge basaltic aquifer. We found that the dominant carbon fixation pathway was the Wood-Ljungdahl pathway, which was present in seven of the eight bacterial genomes. Anaerobic respiration appears to be driven by sulfate reduction, and one bacterial genome contained a complete nitrogen fixation pathway. This study reveals the potential pathways for carbon and energy flux in the deep anoxic thermal aquifer ecosystem, and suggests that ancient H2-based chemolithoautotrophy, which once dominated Earth’s early biosphere, may thus remain one of the dominant metabolisms in the suboceanic aquifer today.

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Data availability

Raw sequence files and draft genomes are publicly available under the Bioproject Number PRJNA264811 (accession #s SDWF00000000, SESU00000000-SESZ00000000, SETA00000000-SETD00000000) on the NCBI website at https://www.ncbi.nlm.nih.gov and at https://figshare.com/articles/olivine_contig-65_fa/7252121.

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Acknowledgements

Metagenome sequencing was made possible by the Deep Carbon Observatory Census of Deep Life supported by the Alfred P. Sloan Foundation and was performed at the Marine Biological Laboratory (Woods Hole, MA, USA). We are grateful for the assistance of Mitch Sogin, Susan Huse, Joseph Vineis, Andrew Voorhis, Sharon Grim, and Hilary Morrison at MBL. Andrew Fisher, C. Geoffrey Wheat, Hans Jannasch, Stefan Sievert, Keir Becker, Mark Nielsen, and the crews of submersible DSRV Alvin and the R/V Atlantis and D/V JOIDES Resolution assisted with flow cell development, deployment, and retrieval. William Rugh contributed to the design of the flow cells. This is a Center for Dark Energy Biosphere Investigations (C-DEBI) contribution.

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Affiliations

  1. Woods Hole Oceanographic Institution, Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, 266 Woods Hole Road, MS #51, Woods Hole, MA, 02543, USA

    • Amy R. Smith
  2. Oregon State University, Corvallis, OR, 97330, USA

    • Brandon Kieft
    • , Ryan Mueller
    • , Martin R. Fisk
    •  & Frederick S. Colwell
  3. Florida State University, Tallahassee, FL, 32306, USA

    • Olivia U. Mason
  4. University of Southern California, Los Angeles, CA, 90089, USA

    • Radu Popa

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The authors declare that they have no conflict of interest.

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Correspondence to Amy R. Smith.

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https://doi.org/10.1038/s41396-019-0385-0