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Nitrite-driven anaerobic methane oxidation by oxygenic bacteria

Author

Listed:
  • 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
    Present address: Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, 4072, Australia.)

  • Denis Le Paslier

    (CEA Genoscope,
    CNRS-UMR 8030, 2 rue Gaston Crémieux,
    Université d’Evry Val d’Essonne, Boulevard François Mitterrand CP 5706, 91057 Evry, France)

  • Eric Pelletier

    (CEA Genoscope,
    CNRS-UMR 8030, 2 rue Gaston Crémieux,
    Université d’Evry Val d’Essonne, Boulevard François Mitterrand CP 5706, 91057 Evry, France)

  • 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,
    CNRS-UMR 8030, 2 rue Gaston Crémieux,
    Université d’Evry Val d’Essonne, Boulevard François Mitterrand CP 5706, 91057 Evry, France)

  • 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
    Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
    Centre for Biotechnology, University of Bielefeld, Postfach 10 01 31, D-33501 Bielefeld, Germany)

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.

Suggested Citation

  • 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 Gloe, 2010. "Nitrite-driven anaerobic methane oxidation by oxygenic bacteria," Nature, Nature, vol. 464(7288), pages 543-548, March.
  • Handle: RePEc:nat:nature:v:464:y:2010:i:7288:d:10.1038_nature08883
    DOI: 10.1038/nature08883
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    Citations

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    Cited by:

    1. Leonard Ernst & Uladzimir Barayeu & Jonas Hädeler & Tobias P. Dick & Judith M. Klatt & Frank Keppler & Johannes G. Rebelein, 2023. "Methane formation driven by light and heat prior to the origin of life and beyond," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Luyao Kang & Yutong Song & Rachel Mackelprang & Dianye Zhang & Shuqi Qin & Leiyi Chen & Linwei Wu & Yunfeng Peng & Yuanhe Yang, 2024. "Metagenomic insights into microbial community structure and metabolism in alpine permafrost on the Tibetan Plateau," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. He, Yanying & Li, Yiming & Li, Xuecheng & Liu, Yingrui & Wang, Yufen & Guo, Haixiao & Hou, Jiaqi & Zhu, Tingting & Liu, Yiwen, 2023. "Net-zero greenhouse gas emission from wastewater treatment: Mechanisms, opportunities and perspectives," Renewable and Sustainable Energy Reviews, Elsevier, vol. 184(C).
    4. Maktabifard, Mojtaba & Al-Hazmi, Hussein E. & Szulc, Paulina & Mousavizadegan, Mohammad & Xu, Xianbao & Zaborowska, Ewa & Li, Xiang & Mąkinia, Jacek, 2023. "Net-zero carbon condition in wastewater treatment plants: A systematic review of mitigation strategies and challenges," Renewable and Sustainable Energy Reviews, Elsevier, vol. 185(C).
    5. Mengxiong Wu & Jie Li & Andy O. Leu & Dirk V. Erler & Terra Stark & Gene W. Tyson & Zhiguo Yuan & Simon J. McIlroy & Jianhua Guo, 2022. "Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Sina Schorn & Jon S. Graf & Sten Littmann & Philipp F. Hach & Gaute Lavik & Daan R. Speth & Carsten J. Schubert & Marcel M. M. Kuypers & Jana Milucka, 2024. "Persistent activity of aerobic methane-oxidizing bacteria in anoxic lake waters due to metabolic versatility," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Kang-Hua Chen & Jiao Feng & Paul L. E. Bodelier & Ziming Yang & Qiaoyun Huang & Manuel Delgado-Baquerizo & Peng Cai & Wenfeng Tan & Yu-Rong Liu, 2024. "Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Jared L. Wilmoth, 2021. "Redox Heterogeneity Entangles Soil and Climate Interactions," Sustainability, MDPI, vol. 13(18), pages 1-14, September.
    9. J. M. Beman & S. M. Vargas & J. M. Wilson & E. Perez-Coronel & J. S. Karolewski & S. Vazquez & A. Yu & A. E. Cairo & M. E. White & I. Koester & L. I. Aluwihare & S. D. Wankel, 2021. "Substantial oxygen consumption by aerobic nitrite oxidation in oceanic oxygen minimum zones," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    10. Samuel Imisi Awala & Joo-Han Gwak & Yongman Kim & Man-Young Jung & Peter F. Dunfield & Michael Wagner & Sung-Keun Rhee, 2024. "Nitrous oxide respiration in acidophilic methanotrophs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Yue Zheng & Huan Wang & Yan Liu & Peiyu Liu & Baoli Zhu & Yanning Zheng & Jinhua Li & Ludmila Chistoserdova & Zhiyong Jason Ren & Feng Zhao, 2024. "Electrochemically coupled CH4 and CO2 consumption driven by microbial processes," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    12. S. Emil Ruff & Pauline Humez & Isabella Hrabe Angelis & Muhe Diao & Michael Nightingale & Sara Cho & Liam Connors & Olukayode O. Kuloyo & Alan Seltzer & Samuel Bowman & Scott D. Wankel & Cynthia N. Mc, 2023. "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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