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Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep

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  • Song-Can Chen

    (Helmholtz Centre for Environmental Research – UFZ
    Chinese Academy of Sciences)

  • Niculina Musat

    (Helmholtz Centre for Environmental Research – UFZ)

  • Oliver J. Lechtenfeld

    (Helmholtz Centre for Environmental Research – UFZ)

  • Heidrun Paschke

    (Helmholtz Centre for Environmental Research – UFZ)

  • Matthias Schmidt

    (Helmholtz Centre for Environmental Research – UFZ)

  • Nedal Said

    (Helmholtz Centre for Environmental Research – UFZ)

  • Denny Popp

    (Helmholtz Centre for Environmental Research – UFZ)

  • Federica Calabrese

    (Helmholtz Centre for Environmental Research – UFZ)

  • Hryhoriy Stryhanyuk

    (Helmholtz Centre for Environmental Research – UFZ)

  • Ulrike Jaekel

    (Max Planck Institute for Marine Microbiology
    The Research Council of Norway)

  • Yong-Guan Zhu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Samantha B. Joye

    (University of Georgia)

  • Hans-Hermann Richnow

    (Helmholtz Centre for Environmental Research – UFZ)

  • Friedrich Widdel

    (Max Planck Institute for Marine Microbiology)

  • Florin Musat

    (Helmholtz Centre for Environmental Research – UFZ
    Max Planck Institute for Marine Microbiology)

Abstract

Ethane is the second most abundant component of natural gas in addition to methane, and—similar to methane—is chemically unreactive. The biological consumption of ethane under anoxic conditions was suggested by geochemical profiles at marine hydrocarbon seeps1–3, and through ethane-dependent sulfate reduction in slurries4–7. Nevertheless, the microorganisms and reactions that catalyse this process have to date remained unknown8. Here we describe ethane-oxidizing archaea that were obtained by specific enrichment over ten years, and analyse these archaea using phylogeny-based fluorescence analyses, proteogenomics and metabolite studies. The co-culture, which oxidized ethane completely while reducing sulfate to sulfide, was dominated by an archaeon that we name ‘Candidatus Argoarchaeum ethanivorans’; other members were sulfate-reducing Deltaproteobacteria. The genome of Ca. Argoarchaeum contains all of the genes that are necessary for a functional methyl-coenzyme M reductase, and all subunits were detected in protein extracts. Accordingly, ethyl-coenzyme M (ethyl-CoM) was identified as an intermediate by liquid chromatography–tandem mass spectrometry. This indicated that Ca. Argoarchaeum initiates ethane oxidation by ethyl-CoM formation, analogous to the recently described butane activation by ‘Candidatus Syntrophoarchaeum’9. Proteogenomics further suggests that oxidation of intermediary acetyl-CoA to CO2 occurs through the oxidative Wood–Ljungdahl pathway. The identification of an archaeon that uses ethane (C2H6) fills a gap in our knowledge of microorganisms that specifically oxidize members of the homologous alkane series (CnH2n+2) without oxygen. Detection of phylogenetic and functional gene markers related to those of Ca. Argoarchaeum at deep-sea gas seeps10–12 suggests that archaea that are able to oxidize ethane through ethyl-CoM are widespread members of the local communities fostered by venting gaseous alkanes around these seeps.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:568:y:2019:i:7750:d:10.1038_s41586-019-1063-0
    DOI: 10.1038/s41586-019-1063-0
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    Citations

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    Cited by:

    1. Olivier N. Lemaire & Gunter Wegener & Tristan Wagner, 2024. "Ethane-oxidising archaea couple CO2 generation to F420 reduction," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Tiantian Yu & Lin Fu & Yinzhao Wang & Yijing Dong & Yifan Chen & Gunter Wegener & Lei Cheng & Fengping Wang, 2024. "Thermophilic Hadarchaeota grow on long-chain alkanes in syntrophy with methanogens," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. 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.
    4. Koudai Taguchi & Alexis Gilbert & Barbara Sherwood Lollar & Thomas Giunta & Christopher J. Boreham & Qi Liu & Juske Horita & Yuichiro Ueno, 2022. "Low 13C-13C abundances in abiotic ethane," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Xiyang Dong & Chuwen Zhang & Yongyi Peng & Hong-Xi Zhang & Ling-Dong Shi & Guangshan Wei & Casey R. J. Hubert & Yong Wang & Chris Greening, 2022. "Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. 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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