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A seafloor microbial biome hosted within incipient ferromanganese crusts

Nature Geoscience volume 2, pages 872–876 (2009)Cite this article

Abstract

Exposed rocks at underwater volcanoes and ridges host complex, abundant and diverse microbial communities1,2,3. The volcanic glasses associated with these features constitute one of the most geochemically reactive components of the Earth’s crust. The most commonly held hypothesis is that their oxidation in sea water provides the energy necessary to establish a seafloor biosphere4,5,6,7. However, this hypothesis has yet to be directly tested. Here we used synchrotron-based X-ray microprobe mapping, X-ray absorption spectroscopy and high-resolution scanning and transmission electron microscopy techniques to examine the initial chemical changes that occur as the glassy rims of young pillow basalts are colonized by microbial organisms at Loihi seamount, Hawaii. We found little evidence of basalt dissolution. Instead, microbial biofilms were intimately associated with Fe(III)- and Mn(IV)-oxides that had precipitated from sea water onto the fresh basalt surfaces. These accumulations of secondary minerals probably represent the earliest stages of ferromanganese crust formation. We suggest that fluid-derived energy sources, such as dissolved and particulate Fe(II), Mn(II) and organic matter, may support the microbial communities colonizing seafloor rocks to a greater degree than local rock dissolution.

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Figure 1: Optical and X-ray fluorescence microprobe images of glassy pillow rims collected from three sites at Loihi seamount.
Figure 2: Chemical behaviour of Ti, Fe(II) and Mn within glasses and surface rinds.
Figure 3: High-resolution electron microscopy images of a basalt slab exposed to sea water for one year at Marker 18.

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Acknowledgements

We thank C. Sheehan (OGI) and the crews of the RV Ka’imikai-o-Kanaloa, RV Kilo Moana and Pisces V (Hawaii Undersea Research Lab), RV Thomas G. Thompson (University of Washington) and ROV Jason II (Woods Hole Oceanographic Institution), as well as the principal investigators and collaborators associated with FeMO, the NSF Fe Microbial Observatory at Loihi seamount (MCB-0348668). We also thank C. Hansel at Harvard University for providing reference EXAFS spectra of Fe-bearing model compounds. This work was directly supported by the National Science Foundation grant OCE-0433629 (H.S., B.M.T., A.S.T.), the David and Lucille Packard Foundation (A.S.T.) and a NASA Predoctoral Fellowship (E.J.K.). The synchrotron work was conducted on beamlines 2-3 and 11-2 at the Stanford Synchrotron Radiation Lightsource (SSRL), a national user facility operated by Stanford University on behalf of the Department of Energy, Office of Basic Energy Sciences, through the Structural Molecular Biology Program, supported by DOE Office of Biological and Environmental Research and the National Institutes of Health. The FIB-milling and high-resolution SEM and TEM analyses were conducted at the Environmental Molecular Sciences Laboratory (EMSL), a national scientific user facility at the Pacific Northwest National Laboratory also supported by the DOE Office of Biological and Environmental Research. A. Buxbaum, FEI Corp., also provided valuable technical assistance in the FIB-SEM preparation.

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Authors and Affiliations

  1. Department of Geological Sciences, UCB 399, University of Colorado, Boulder, Colorado 80309-0399, USA

    A. S. Templeton, E. J. Knowles & D. L. Eldridge

  2. Pacific Northwest National Laboratory, Richland, Washington 99354, USA

    B. W. Arey & A. C. Dohnalkova

  3. Stanford Synchrotron Radiation Lightsource, 2575 Sand Hill Road, MS 69, Menlo Park, California 94025, USA

    S. M. Webb

  4. Institute of Geophysics and Planetary Physics, Scripps Institution of Oceanography, University of California, La Jolla, California 92037, USA

    B. E. Bailey & H. Staudigel

  5. Division of Environmental and Biomolecular Systems, Oregon Health & Sciences University, 20000 NW Walker Road, Beaverton, Oregon 97006, USA

    B. M. Tebo

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Contributions

A.S.T., E.J.K., D.L.E., B.E.B., B.M.T. and H.S. all participated in sample planning and collection. A.S.T., E.J.K., D.L.E. and S.M.W. each led aspects of the synchrotron-based X-ray spectroscopy and microprobe mapping data collection and analysis. B.W.A. and A.C.D. conducted the electron microscopy with input from A.S.T. and B.M.T. A.S.T. wrote the manuscript with input from all of the authors.

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Correspondence to A. S. Templeton.

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Templeton, A., Knowles, E., Eldridge, D. et al. A seafloor microbial biome hosted within incipient ferromanganese crusts. Nature Geosci 2, 872–876 (2009). https://doi.org/10.1038/ngeo696

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