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Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Author

Listed:
  • Heleen T. Ouboter

    (Radboud University)

  • Rob Mesman

    (Radboud University)

  • Tom Sleutels

    (European Centre of Excellence for Sustainable Water Technology
    University of Groningen)

  • Jelle Postma

    (Radboud University)

  • Martijn Wissink

    (Radboud University)

  • Mike S. M. Jetten

    (Radboud University)

  • Annemiek Ter Heijne

    (Wageningen University & Research)

  • Tom Berben

    (Radboud University)

  • Cornelia U. Welte

    (Radboud University)

Abstract

Anaerobic methanotrophic (ANME) archaea are environmentally important, uncultivated microorganisms that oxidize the potent greenhouse gas methane. During methane oxidation, ANME archaea engage in extracellular electron transfer (EET) with other microbes, metal oxides, and electrodes through unclear mechanisms. Here, we cultivate ANME-2d archaea (‘Ca. Methanoperedens’) in bioelectrochemical systems and observe strong methane-dependent current (91–93% of total current) associated with high enrichment of ‘Ca. Methanoperedens’ on the anode (up to 82% of the community), as determined by metagenomics and transmission electron microscopy. Electrochemical and metatranscriptomic analyses suggest that the EET mechanism is similar at various electrode potentials, with the possible involvement of an uncharacterized short-range electron transport protein complex and OmcZ nanowires.

Suggested Citation

  • Heleen T. Ouboter & Rob Mesman & Tom Sleutels & Jelle Postma & Martijn Wissink & Mike S. M. Jetten & Annemiek Ter Heijne & Tom Berben & Cornelia U. Welte, 2024. "Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45758-2
    DOI: 10.1038/s41467-024-45758-2
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    1. Yangqi Gu & Vishok Srikanth & Aldo I. Salazar-Morales & Ruchi Jain & J. Patrick O’Brien & Sophia M. Yi & Rajesh Kumar Soni & Fadel A. Samatey & Sibel Ebru Yalcin & Nikhil S. Malvankar, 2021. "Structure of Geobacter pili reveals secretory rather than nanowire behaviour," Nature, Nature, vol. 597(7876), pages 430-434, September.
    2. Michael J. McAnulty & Venkata G. Poosarla & Kyoung-Yeol Kim & Ricardo Jasso-Chávez & Bruce E. Logan & Thomas K. Wood, 2017. "Electricity from methane by reversing methanogenesis," Nature Communications, Nature, vol. 8(1), pages 1-8, August.
    3. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Erratum: Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 501(7468), pages 578-578, September.
    4. Antje Boetius & Katrin Ravenschlag & Carsten J. Schubert & Dirk Rickert & Friedrich Widdel & Armin Gieseke & Rudolf Amann & Bo Barker Jørgensen & Ursula Witte & Olaf Pfannkuche, 2000. "A marine microbial consortium apparently mediating anaerobic oxidation of methane," Nature, Nature, vol. 407(6804), pages 623-626, October.
    5. Peter Menzel & Kim Lee Ng & Anders Krogh, 2016. "Fast and sensitive taxonomic classification for metagenomics with Kaiju," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
    6. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 500(7464), pages 567-570, August.
    7. Xueqin Zhang & Georgina H. Joyce & Andy O. Leu & Jing Zhao & Hesamoddin Rabiee & Bernardino Virdis & Gene W. Tyson & Zhiguo Yuan & Simon J. McIlroy & Shihu Hu, 2023. "Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Shawn E. McGlynn & Grayson L. Chadwick & Christopher P. Kempes & Victoria J. Orphan, 2015. "Single cell activity reveals direct electron transfer in methanotrophic consortia," Nature, Nature, vol. 526(7574), pages 531-535, October.
    9. Kai-Uwe Hinrichs & John M. Hayes & Sean P. Sylva & Peter G. Brewer & Edward F. DeLong, 1999. "Methane-consuming archaebacteria in marine sediments," Nature, Nature, vol. 398(6730), pages 802-805, April.
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