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Isolation of an autotrophic ammonia-oxidizing marine archaeon

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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Figure 1: Phylogenetic relationships between 16S rRNA sequences from SCM1 and representatives of the marine group 1 Crenarchaeota.
Figure 2: Photomicrographs of SCM1.
Figure 3: Near-stoichiometric conversion of ammonia to nitrite by SCM1.

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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.

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Correspondence to David A. Stahl.

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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.

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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. (DOC 63 kb)

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Könneke, M., Bernhard, A., de la Torre, J. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005). https://doi.org/10.1038/nature03911

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