Letter | Published:

Isolation of an autotrophic ammonia-oxidizing marine archaeon

Nature volume 437, pages 543546 (22 September 2005) | Download Citation

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Abstract

For years, microbiologists characterized the Archaea as obligate extremophiles that thrive in environments too harsh for other organisms. The limited physiological diversity among cultivated Archaea suggested that these organisms were metabolically constrained to a few environmental niches. For instance, all Crenarchaeota that are currently cultivated are sulphur-metabolizing thermophiles1. However, landmark studies using cultivation-independent methods uncovered vast numbers of Crenarchaeota in cold oxic ocean waters2,3. Subsequent molecular surveys demonstrated the ubiquity of these low-temperature Crenarchaeota in aquatic and terrestrial environments4. The numerical dominance of marine Crenarchaeota—estimated at 1028 cells in the world's oceans5—suggests that they have a major role in global biogeochemical cycles. Indeed, isotopic analyses of marine crenarchaeal lipids suggest that these planktonic Archaea fix inorganic carbon6. Here we report the isolation of a marine crenarchaeote that grows chemolithoautotrophically by aerobically oxidizing ammonia to nitrite—the first observation of nitrification in the Archaea. The autotrophic metabolism of this isolate, and its close phylogenetic relationship to environmental marine crenarchaeal sequences, suggests that nitrifying marine Crenarchaeota may be important to global carbon and nitrogen cycles.

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Acknowledgements

We thank A. R. Blevins, P. M. Berube and N. Pinel for technical assistance, S. Lara for performing electron microscopy and J. F. Heidelberg for assistance navigating the Sargasso Sea metagenome sequence data. We thank the Shedd and Seattle aquariums for samples and J. Hayes for his assistance. This research was supported by National Science Foundation Systematics (D.A.S.), Microbial Observatories (D.A.S. and J.B.W.) and Postdoctoral Fellowship (A.E.B.) programmes.

Author information

Author notes

    • Martin Könneke
    •  & Anne E. Bernhard

    †Present addresses: Institut für Chemie und Biologie des Meeres, Universität Oldenburg, Oldenburg 26111, Germany (M.K.); Department of Biology, Connecticut College, New London, Connecticut 06320, USA (A.E.B.)

    • Martin Könneke
    • , Anne E. Bernhard
    •  & José R. de la Torre

    *These authors contributed equally to this work

Affiliations

  1. Department of Civil and Environmental Engineering, University of Washington, Seattle, Washington 98195, USA

    • Martin Könneke
    • , Anne E. Bernhard
    • , José R. de la Torre
    • , Christopher B. Walker
    •  & David A. Stahl
  2. Woods Hole Oceanographic Institute, Woods Hole, Massachusetts 02543, USA

    • John B. Waterbury

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Competing interests

The sequences described in this manuscript have been deposited in GenBank under accession numbers DQ085097 to DQ085105. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to David A. Stahl.

Supplementary information

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  1. 1.

    Supplementary Notes

    This file contains an alignment of amino acid sequences encoding putative archaeal ammonia monooxygenases. These sequences were used to design oligonucleotide primers for amplification of genes from our isolated crenarchaeote and to demonstrate the high level of sequence conservation among homologous genes recovered from soil and marine crenarchaeal sequences. This file also contains Supplementary Methods and additional references.

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https://doi.org/10.1038/nature03911

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