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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.

References

  1. Burggraf, S., Huber, H. & Stetter, K. O. Reclassification of the crenarchaeal orders and families in accordance with 16S rRNA sequence data. Int. J. Syst. Bacteriol. 47, 657–660 (1997)

    CAS  Article  Google Scholar 

  2. Fuhrman, J. A., McCallum, K. & Davis, A. A. Novel major archaebacterial group from marine plankton. Nature 356, 148–149 (1992)

    ADS  CAS  Article  Google Scholar 

  3. DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992)

    ADS  CAS  Article  Google Scholar 

  4. Dawson, S. C., Pace, N. R. & DeLong, E. F. Phylogenetic and ecological perspectives on uncultured Crenarchaeota and Korarchaeota. In The Prokaryotes—An Evolving Electronic Resource for the Microbiological Community 3rd edn (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) http://link.springer-ny.com/link/service/books/10125/ release 3.3 (Springer, New York, 2000)

    Google Scholar 

  5. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)

    ADS  CAS  Article  Google Scholar 

  6. Pearson, A., McNichol, A. P., Benitez-Nelson, B. C., Hayes, J. M. & Eglinton, T. I. Origins of lipid biomarkers in Santa Monica Basin surface sediment: A case study using compound-specific Δ14C analysis. Geochim. Cosmochim. Acta 65, 3123–3137 (2001)

    ADS  CAS  Article  Google Scholar 

  7. Wuchter, C., Schouten, S., Boschker, H. T. & Sinninghe Damste, J. S. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol. Lett. 219, 203–207 (2003)

    CAS  Article  Google Scholar 

  8. Ouverney, C. C. & Fuhrman, J. A. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66, 4829–4833 (2000)

    CAS  Article  Google Scholar 

  9. Bock, E. & Wagner, M. Oxidation of inorganic nitrogen compounds as an energy source. In The Prokaryotes—An Evolving Electronic Resource for the Microbiological Community 3rd edn (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) http://link.springer-ny.com/link/service/books/10125/ release 3.7 (Springer, New York, 2001)

    Google Scholar 

  10. Hovanec, T. A. & DeLong, E. F. Comparative analysis of nitrifying bacteria associated with freshwater and marine aquaria. Appl. Environ. Microbiol. 62, 2888–2896 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)

    ADS  CAS  Article  Google Scholar 

  12. Preston, C. M., Wu, K. Y., Molinski, T. F. & DeLong, E. F. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl Acad. Sci. USA 93, 6241–6246 (1996)

    ADS  CAS  Article  Google Scholar 

  13. Béjà, O. et al. Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces. Appl. Environ. Microbiol. 68, 335–345 (2002)

    Article  Google Scholar 

  14. Treusch, A. H. et al. Characterization of large-insert DNA libraries from soil for environmental genomic studies of Archaea. Environ. Microbiol. 6, 970–980 (2004)

    CAS  Article  Google Scholar 

  15. DeLong, E. F., Taylor, L. T., Marsh, T. L. & Preston, C. M. Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl. Environ. Microbiol. 65, 5554–5563 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Capone, D. G. in Microbial Ecology of the Oceans (ed. Kirchman, D. L.) 455–493 (Wiley, New York, 2000)

    Google Scholar 

  17. Ducklow, H. in Microbial Ecology of the Oceans (ed. Kirchman, D. L.) 85–120 (Wiley, New York, 2000)

    Google Scholar 

  18. Hügler, M., Huber, H., Stetter, K. O. & Fuchs, G. Autotrophic CO2 fixation pathways in archaea (Crenarchaeota). Arch. Microbiol. 179, 160–173 (2003)

    Article  Google Scholar 

  19. Menendez, C. et al. Presence of acetyl-coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J. Bacteriol. 181, 1088–1098 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Wada, E. & Hattori, A. Nitrite metabolism in the euphotic layer of the central North Pacific Ocean. Limnol. Oceanogr. 16, 766–772 (1971)

    ADS  CAS  Article  Google Scholar 

  21. Barns, S. M., Delwiche, C. F., Palmer, J. D. & Pace, N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl Acad. Sci. USA 93, 9188–9193 (1996)

    ADS  CAS  Article  Google Scholar 

  22. Pearson, A. et al. Nonmarine crenarchaeol in Nevada hot springs. Appl. Environ. Microbiol. 70, 5229–5237 (2004)

    CAS  Article  Google Scholar 

  23. Widdel, F. & Bak, F. in The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Application 2nd edn (eds Ballows, A., Trüper, H. G., Dworkin, M., Harder, W. & Schleifer, K.-H.) 3352–3378 (Springer, New York, 1992)

    Google Scholar 

  24. Lane, D. J. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) 115–175 (Wiley, New York, 1991)

    Google Scholar 

  25. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004)

    CAS  Article  Google Scholar 

  26. Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods) (version 4.0 beta 10) http://paup.csit.fsu.edu/index.html (Sinauer, Sunderland, 2003)

  27. Stickland, J. D. H. & Parsons, T. R. A Practical Handbook of Seawater Analysis (Fisheries Research Board of Canada, Ottawa, 1972)

    Google Scholar 

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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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