Nitrite-driven anaerobic methane oxidation by oxygenic bacteria

Katharina F. Ettwig (), Margaret K. Butler, Denis Le Paslier, Eric Pelletier, Sophie Mangenot, Marcel M. M. Kuypers, Frank Schreiber, Bas E. Dutilh, Johannes Zedelius, Dirk de Beer, Jolein Gloerich, Hans J. C. T. Wessels, Theo van Alen, Francisca Luesken, Ming L. Wu, Katinka T. van de Pas-Schoonen, Huub J. M. Op den Camp, Eva M. Janssen-Megens, Kees-Jan Francoijs, Henk Stunnenberg, Jean Weissenbach, Mike S. M. Jetten and Marc Strous ()
Additional contact information
Katharina F. Ettwig: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Margaret K. Butler: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Denis Le Paslier: CEA Genoscope,
Eric Pelletier: CEA Genoscope,
Sophie Mangenot: CEA Genoscope,
Marcel M. M. Kuypers: Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
Frank Schreiber: Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
Bas E. Dutilh: Radboud University Nijmegen Medical Centre, Centre for Molecular and Biomolecular Informatics, Nijmegen Centre for Molecular Life Sciences, Geert Grooteplein 28,
Johannes Zedelius: Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
Dirk de Beer: Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
Jolein Gloerich: Radboud University Nijmegen Medical Centre, Nijmegen Proteomics Facility, Laboratory of Genetic, Endocrine and Metabolic Diseases, Geert Grooteplein-Zuid 10
Hans J. C. T. Wessels: Radboud University Nijmegen Medical Centre, Nijmegen Proteomics Facility, Laboratory of Genetic, Endocrine and Metabolic Diseases, Geert Grooteplein-Zuid 10
Theo van Alen: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Francisca Luesken: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Ming L. Wu: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Katinka T. van de Pas-Schoonen: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Huub J. M. Op den Camp: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Eva M. Janssen-Megens: Radboud University Nijmegen, Nijmegen Centre for Molecular Life Sciences, Geert Grooteplein-Zuid 26, 6525 GA, Nijmegen, The Netherlands
Kees-Jan Francoijs: Radboud University Nijmegen, Nijmegen Centre for Molecular Life Sciences, Geert Grooteplein-Zuid 26, 6525 GA, Nijmegen, The Netherlands
Henk Stunnenberg: Radboud University Nijmegen, Nijmegen Centre for Molecular Life Sciences, Geert Grooteplein-Zuid 26, 6525 GA, Nijmegen, The Netherlands
Jean Weissenbach: CEA Genoscope,
Mike S. M. Jetten: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands
Marc Strous: Radboud University Nijmegen, IWWR, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands

Nature, 2010, vol. 464, issue 7288, 543-548

Abstract: Abstract Only three biological pathways are known to produce oxygen: photosynthesis, chlorate respiration and the detoxification of reactive oxygen species. Here we present evidence for a fourth pathway, possibly of considerable geochemical and evolutionary importance. The pathway was discovered after metagenomic sequencing of an enrichment culture that couples anaerobic oxidation of methane with the reduction of nitrite to dinitrogen. The complete genome of the dominant bacterium, named ‘Candidatus Methylomirabilis oxyfera’, was assembled. This apparently anaerobic, denitrifying bacterium encoded, transcribed and expressed the well-established aerobic pathway for methane oxidation, whereas it lacked known genes for dinitrogen production. Subsequent isotopic labelling indicated that ‘M. oxyfera’ bypassed the denitrification intermediate nitrous oxide by the conversion of two nitric oxide molecules to dinitrogen and oxygen, which was used to oxidize methane. These results extend our understanding of hydrocarbon degradation under anoxic conditions and explain the biochemical mechanism of a poorly understood freshwater methane sink. Because nitrogen oxides were already present on early Earth, our finding opens up the possibility that oxygen was available to microbial metabolism before the evolution of oxygenic photosynthesis.

Date: 2010
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DOI: 10.1038/nature08883

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