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Methane formation driven by reactive oxygen species across all living organisms

Author

Listed:
  • Leonard Ernst

    (Heidelberg University
    Max-Planck-Institute for Terrestrial Microbiology
    Heidelberg University)

  • Benedikt Steinfeld

    (Heidelberg University
    Max-Planck-Institute for Terrestrial Microbiology
    Heidelberg University)

  • Uladzimir Barayeu

    (German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance
    Heidelberg University)

  • Thomas Klintzsch

    (Heidelberg University
    Gießen University)

  • Markus Kurth

    (Heidelberg Institute for Theoretical Studies)

  • Dirk Grimm

    (Heidelberg University
    Heidelberg University)

  • Tobias P. Dick

    (German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance
    Heidelberg University)

  • Johannes G. Rebelein

    (Max-Planck-Institute for Terrestrial Microbiology)

  • Ilka B. Bischofs

    (Heidelberg University
    Max-Planck-Institute for Terrestrial Microbiology
    Heidelberg University)

  • Frank Keppler

    (Heidelberg University
    Heidelberg University)

Abstract

Methane (CH4), the most abundant hydrocarbon in the atmosphere, originates largely from biogenic sources1 linked to an increasing number of organisms occurring in oxic and anoxic environments. Traditionally, biogenic CH4 has been regarded as the final product of anoxic decomposition of organic matter by methanogenic archaea. However, plants2,3, fungi4, algae5 and cyanobacteria6 can produce CH4 in the presence of oxygen. Although methanogens are known to produce CH4 enzymatically during anaerobic energy metabolism7, the requirements and pathways for CH4 production by non-methanogenic cells are poorly understood. Here, we demonstrate that CH4 formation by Bacillus subtilis and Escherichia coli is triggered by free iron and reactive oxygen species (ROS), which are generated by metabolic activity and enhanced by oxidative stress. ROS-induced methyl radicals, which are derived from organic compounds containing sulfur- or nitrogen-bonded methyl groups, are key intermediates that ultimately lead to CH4 production. We further show CH4 production by many other model organisms from the Bacteria, Archaea and Eukarya domains, including in several human cell lines. All these organisms respond to inducers of oxidative stress by enhanced CH4 formation. Our results imply that all living cells probably possess a common mechanism of CH4 formation that is based on interactions among ROS, iron and methyl donors, opening new perspectives for understanding biochemical CH4 formation and cycling.

Suggested Citation

  • Leonard Ernst & Benedikt Steinfeld & Uladzimir Barayeu & Thomas Klintzsch & Markus Kurth & Dirk Grimm & Tobias P. Dick & Johannes G. Rebelein & Ilka B. Bischofs & Frank Keppler, 2022. "Methane formation driven by reactive oxygen species across all living organisms," Nature, Nature, vol. 603(7901), pages 482-487, March.
  • Handle: RePEc:nat:nature:v:603:y:2022:i:7901:d:10.1038_s41586-022-04511-9
    DOI: 10.1038/s41586-022-04511-9
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    Citations

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    Cited by:

    1. Kandasamy Senthilraja & Subramanian Venkatesan & Dhandayuthapani Udhaya Nandhini & Manickam Dhasarathan & Balasubramaniam Prabha & Kovilpillai Boomiraj & Shanmugam Mohan Kumar & Kulanthaivel Bhuvanesw, 2023. "Mitigating Methane Emission from the Rice Ecosystem through Organic Amendments," Agriculture, MDPI, vol. 13(5), pages 1-17, May.
    2. 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.
    3. Stefanie Duller & Simone Vrbancic & Łukasz Szydłowski & Alexander Mahnert & Marcus Blohs & Michael Predl & Christina Kumpitsch & Verena Zrim & Christoph Högenauer & Tomasz Kosciolek & Ruth A. Schmitz , 2024. "Targeted isolation of Methanobrevibacter strains from fecal samples expands the cultivated human archaeome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Jan N. Arx & Abiel T. Kidane & Miriam Philippi & Wiebke Mohr & Gaute Lavik & Sina Schorn & Marcel M. M. Kuypers & Jana Milucka, 2023. "Methylphosphonate-driven methane formation and its link to primary production in the oligotrophic North Atlantic," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. César Ordóñez & Tonya DelSontro & Timon Langenegger & Daphne Donis & Ena L. Suarez & Daniel F. McGinnis, 2023. "Evaluation of the methane paradox in four adjacent pre-alpine lakes across a trophic gradient," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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