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

Xueqin Zhang, Georgina H. Joyce, Andy O. Leu, Jing Zhao, Hesamoddin Rabiee, Bernardino Virdis, Gene W. Tyson, Zhiguo Yuan, Simon J. McIlroy and Shihu Hu ()
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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
Hesamoddin Rabiee: University of Queensland
Bernardino Virdis: University of Queensland
Gene W. Tyson: Queensland University of Technology (QUT), Translational Research Institute
Zhiguo Yuan: University of Queensland
Simon J. McIlroy: Queensland University of Technology (QUT), Translational Research Institute
Shihu Hu: University of Queensland

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41847-w

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