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Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’

Author

Listed:
  • Xueqin Zhang

    (University of Queensland)

  • Georgina H. Joyce

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Andy O. Leu

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Jing Zhao

    (University of Queensland
    The University of Queensland)

  • Hesamoddin Rabiee

    (University of Queensland
    The University of Queensland
    University of Southern Queensland)

  • Bernardino Virdis

    (University of Queensland)

  • Gene W. Tyson

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Zhiguo Yuan

    (University of Queensland
    City University of Hong Kong)

  • Simon J. McIlroy

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Shihu Hu

    (University of Queensland)

Abstract

Anaerobic methanotrophic archaea (ANME) carry out anaerobic oxidation of methane, thus playing a crucial role in the methane cycle. Previous genomic evidence indicates that multi-heme c-type cytochromes (MHCs) may facilitate the extracellular electron transfer (EET) from ANME to different electron sinks. Here, we provide experimental evidence supporting cytochrome-mediated EET for the reduction of metals and electrodes by ‘Candidatus Methanoperedens nitroreducens’, an ANME acclimated to nitrate reduction. Ferrous iron-targeted fluorescent assays, metatranscriptomics, and single-cell imaging suggest that ‘Ca. M. nitroreducens’ uses surface-localized redox-active cytochromes for metal reduction. Electrochemical and Raman spectroscopic analyses also support the involvement of c-type cytochrome-mediated EET for electrode reduction. Furthermore, several genes encoding menaquinone cytochrome type-c oxidoreductases and extracellular MHCs are differentially expressed when different electron acceptors are used.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41847-w
    DOI: 10.1038/s41467-023-41847-w
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    References listed on IDEAS

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    1. 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.
    2. 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.
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    4. 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.
    5. 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.
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    1. 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.
    2. Song-Can Chen & Sheng Chen & Niculina Musat & Steffen Kümmel & Jiaheng Ji & Marie Braad Lund & Alexis Gilbert & Oliver J. Lechtenfeld & Hans-Hermann Richnow & Florin Musat, 2024. "Back flux during anaerobic oxidation of butane support archaea-mediated alkanogenesis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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