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Back flux during anaerobic oxidation of butane support archaea-mediated alkanogenesis

Author

Listed:
  • Song-Can Chen

    (University of Vienna
    Zhejiang University)

  • Sheng Chen

    (Beijing Normal University)

  • Niculina Musat

    (Aarhus University)

  • Steffen Kümmel

    (Helmholtz Centre for Environmental Research – UFZ)

  • Jiaheng Ji

    (Helmholtz Centre for Environmental Research – UFZ)

  • Marie Braad Lund

    (Aarhus University)

  • Alexis Gilbert

    (Tokyo Institute of Technology)

  • Oliver J. Lechtenfeld

    (Helmholtz Centre for Environmental Research – UFZ)

  • Hans-Hermann Richnow

    (Helmholtz Centre for Environmental Research – UFZ)

  • Florin Musat

    (Aarhus University
    Babeş-Bolyai University)

Abstract

Microbial formation and oxidation of volatile alkanes in anoxic environments significantly impacts biogeochemical cycles on Earth. The discovery of archaea oxidizing volatile alkanes via deeply branching methyl-coenzyme M reductase variants, dubbed alkyl-CoM reductases (ACR), prompted the hypothesis of archaea-catalysed alkane formation in nature (alkanogenesis). A combination of metabolic modelling, anaerobic physiology assays, and isotope labeling of Candidatus Syntrophoarchaeum archaea catalyzing the anaerobic oxidation of butane (AOB) show a back flux of CO2 to butane, demonstrating reversibility of the entire AOB pathway. Back fluxes correlate with thermodynamics and kinetics of the archaeal catabolic system. AOB reversibility supports a biological formation of butane, and generally of higher volatile alkanes, helping to explain the presence of isotopically light alkanes and deeply branching ACR genes in sedimentary basins isolated from gas reservoirs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53932-9
    DOI: 10.1038/s41467-024-53932-9
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    References listed on IDEAS

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    1. Gunter Wegener & Viola Krukenberg & Dietmar Riedel & Halina E. Tegetmeyer & Antje Boetius, 2015. "Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria," Nature, Nature, vol. 526(7574), pages 587-590, October.
    2. Song-Can Chen & Niculina Musat & Oliver J. Lechtenfeld & Heidrun Paschke & Matthias Schmidt & Nedal Said & Denny Popp & Federica Calabrese & Hryhoriy Stryhanyuk & Ulrike Jaekel & Yong-Guan Zhu & Saman, 2019. "Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep," Nature, Nature, vol. 568(7750), pages 108-111, April.
    3. Olaf Kniemeyer & Florin Musat & Stefan M. Sievert & Katrin Knittel & Heinz Wilkes & Martin Blumenberg & Walter Michaelis & Arno Classen & Carsten Bolm & Samantha B. Joye & Friedrich Widdel, 2007. "Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria," Nature, Nature, vol. 449(7164), pages 898-901, October.
    4. 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.
    5. Zhuo Zhou & Cui-jing Zhang & Peng-fei Liu & Lin Fu & Rafael Laso-Pérez & Lu Yang & Li-ping Bai & Jiang Li & Min Yang & Jun-zhang Lin & Wei-dong Wang & Gunter Wegener & Meng Li & Lei Cheng, 2022. "Non-syntrophic methanogenic hydrocarbon degradation by an archaeal species," Nature, Nature, vol. 601(7892), pages 257-262, January.
    6. Elad Noor & Hulda S Haraldsdóttir & Ron Milo & Ronan M T Fleming, 2013. "Consistent Estimation of Gibbs Energy Using Component Contributions," PLOS Computational Biology, Public Library of Science, vol. 9(7), pages 1-11, July.
    7. Silvan Scheller & Meike Goenrich & Reinhard Boecher & Rudolf K. Thauer & Bernhard Jaun, 2010. "The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane," Nature, Nature, vol. 465(7298), pages 606-608, June.
    8. Zheng-Shuang Hua & Yu-Lin Wang & Paul N. Evans & Yan-Ni Qu & Kian Mau Goh & Yang-Zhi Rao & Yan-Ling Qi & Yu-Xian Li & Min-Jun Huang & Jian-Yu Jiao & Ya-Ting Chen & Yan-Ping Mao & Wen-Sheng Shu & Wael , 2019. "Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    9. 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.
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