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Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri

View ORCID ProfileAnnette R. Rowe, Shuai Xu, Emily Gardel, Arpita Bose, Peter Girguis, Jan P. Amend, Mohamed Y. El-Naggar
doi: https://doi.org/10.1101/415653
Annette R. Rowe
1Department of Biological Science, University of Cincinnati, Cincinnati, OH
2Department of Physics and Astronomy, University of Southern California, Los Angeles, CA
3Department of Earth Sciences, University of Southern California, Los Angeles, CA
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  • ORCID record for Annette R. Rowe
  • For correspondence: annette.rowe@uc.edu
Shuai Xu
2Department of Physics and Astronomy, University of Southern California, Los Angeles, CA
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Emily Gardel
4Department of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA
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Arpita Bose
4Department of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA
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Peter Girguis
4Department of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA
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Jan P. Amend
3Department of Earth Sciences, University of Southern California, Los Angeles, CA
5Department of Biological Sciences, University of Southern California, Los Angeles, CA
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Mohamed Y. El-Naggar
2Department of Physics and Astronomy, University of Southern California, Los Angeles, CA
5Department of Biological Sciences, University of Southern California, Los Angeles, CA
6Department of Chemistry, University of Southern California, Los Angeles, CA
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Abstract

The Methanosarcinales, a lineage of cytochrome-containing methanogens, have recently been proposed to participate in direct extracellular electron transfer interactions within syntrophic communities. To shed light on this phenomenon, we applied electrochemical techniques to measure electron uptake from cathodes by Methanosarcina barkeri, which is an important model organism that is genetically tractable and utilizes a wide range of substrates for methanogenesis. Here we confirm the ability of M. barkeri to perform electron uptake from cathodes and show that this cathodic current is linked to quantitative increases in methane production. The underlying mechanisms we identified include, but are not limited to, a recently proposed association between cathodes and methanogen-derived extracellular enzymes (e.g. hydrogenases) that can facilitate current generation through the formation of reduced and diffusible methanogenic substrates (e.g. hydrogen). However, after minimizing the contributions of such extracellular enzymes and using a mutant lacking hydrogenases, we observe a lower potential hydrogen-independent pathway that facilitates cathodic activity coupled to methane production in M. barkeri. Our electrochemical measurements of wild-type and mutant strains point to a novel and extracellular-enzyme-free mode of electron uptake able to take up electrons at potentials lower than - 498 mV vs. SHE (over 100 mV more reduced than the observed hydrogenase midpoint potential under these conditions). These results suggest that M. barkeri can perform multiple modes (hydrogenase-mediated and free extracellular enzyme-independent) of electrode interactions on cathodes including a mechanism pointing to a direct interaction, which has significant applied and ecological implications.

Importance Methanogenic Archaea are of fundamental applied and environmental relevance. This is largely due to their activities in a wide range of anaerobic environments, generating gaseous reduced carbon that can be utilized as a fuel source. While the bioenergetics of a wide variety of methanogens has been well studied with respect to soluble substrates, mechanistic understanding of their interaction with solid phase redox active compounds is limited. This work provides insight into solid phase redox interactions in Methanosarcina using electrochemical methods. We highlight a previously undescribed mode of electron uptake from cathodes, that is potentially informative of direct interspecies electron transfer interactions in the Methanosarcinales.

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Posted September 12, 2018.
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Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri
Annette R. Rowe, Shuai Xu, Emily Gardel, Arpita Bose, Peter Girguis, Jan P. Amend, Mohamed Y. El-Naggar
bioRxiv 415653; doi: https://doi.org/10.1101/415653
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Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri
Annette R. Rowe, Shuai Xu, Emily Gardel, Arpita Bose, Peter Girguis, Jan P. Amend, Mohamed Y. El-Naggar
bioRxiv 415653; doi: https://doi.org/10.1101/415653

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