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MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans

Methanogens are a diverse group of Archaea that couple energy conservation to the production of methane gas. While most methanogens have no alternate mode of energy conservation, strains like Methanosarcina acetivorans are known to also conserve energy by dissimilatory metal reduction (DSMR) in the...

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Autores principales: Gupta, Dinesh, Chen, Keying, Elliott, Sean J., Nayak, Dipti D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10153276/
https://www.ncbi.nlm.nih.gov/pubmed/37131651
http://dx.doi.org/10.1101/2023.04.20.537704
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author Gupta, Dinesh
Chen, Keying
Elliott, Sean J.
Nayak, Dipti D.
author_facet Gupta, Dinesh
Chen, Keying
Elliott, Sean J.
Nayak, Dipti D.
author_sort Gupta, Dinesh
collection PubMed
description Methanogens are a diverse group of Archaea that couple energy conservation to the production of methane gas. While most methanogens have no alternate mode of energy conservation, strains like Methanosarcina acetivorans are known to also conserve energy by dissimilatory metal reduction (DSMR) in the presence of soluble ferric iron or iron-containing minerals. The ecological ramifications of energy conservation decoupled from methane production in methanogens are substantial, yet the molecular details are poorly understood. In this work, we conducted in vitro and in vivo studies with a multiheme c-type cytochrome (MHC), called MmcA, to establish its role during methanogenesis and DSMR in M. acetivorans. MmcA purified from M. acetivorans can donate electrons to methanophenazine, a membrane-bound electron carrier, to facilitate methanogenesis. In addition, MmcA can also reduce Fe(III) and the humic acid analog anthraquinone-2,6-disulfonate (AQDS) during DSMR. Furthermore, mutants lacking mmcA have slower Fe(III) reduction rates. The redox reactivities of MmcA are consistent with the electrochemical data where MmcA displays reversible redox features ranging from −100 to −450 mV versus SHE. MmcA is prevalent in members of the Order Methanosarcinales but does not belong to a known family of MHCs linked to extracellular electron transfer, bioinformatically, and instead forms a distinct clade that is closely related to octaheme tetrathionate reductases. Taken together, this study shows that MmcA is widespread in methanogens with cytochromes where it acts as an electron conduit to support a variety of energy conservation strategies that extend beyond methanogenesis.
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spelling pubmed-101532762023-05-03 MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans Gupta, Dinesh Chen, Keying Elliott, Sean J. Nayak, Dipti D. bioRxiv Article Methanogens are a diverse group of Archaea that couple energy conservation to the production of methane gas. While most methanogens have no alternate mode of energy conservation, strains like Methanosarcina acetivorans are known to also conserve energy by dissimilatory metal reduction (DSMR) in the presence of soluble ferric iron or iron-containing minerals. The ecological ramifications of energy conservation decoupled from methane production in methanogens are substantial, yet the molecular details are poorly understood. In this work, we conducted in vitro and in vivo studies with a multiheme c-type cytochrome (MHC), called MmcA, to establish its role during methanogenesis and DSMR in M. acetivorans. MmcA purified from M. acetivorans can donate electrons to methanophenazine, a membrane-bound electron carrier, to facilitate methanogenesis. In addition, MmcA can also reduce Fe(III) and the humic acid analog anthraquinone-2,6-disulfonate (AQDS) during DSMR. Furthermore, mutants lacking mmcA have slower Fe(III) reduction rates. The redox reactivities of MmcA are consistent with the electrochemical data where MmcA displays reversible redox features ranging from −100 to −450 mV versus SHE. MmcA is prevalent in members of the Order Methanosarcinales but does not belong to a known family of MHCs linked to extracellular electron transfer, bioinformatically, and instead forms a distinct clade that is closely related to octaheme tetrathionate reductases. Taken together, this study shows that MmcA is widespread in methanogens with cytochromes where it acts as an electron conduit to support a variety of energy conservation strategies that extend beyond methanogenesis. Cold Spring Harbor Laboratory 2023-04-20 /pmc/articles/PMC10153276/ /pubmed/37131651 http://dx.doi.org/10.1101/2023.04.20.537704 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Gupta, Dinesh
Chen, Keying
Elliott, Sean J.
Nayak, Dipti D.
MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title_full MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title_fullStr MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title_full_unstemmed MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title_short MmcA is an electron conduit that facilitates both intracellular and extracellular electron transport in Methanosarcina acetivorans
title_sort mmca is an electron conduit that facilitates both intracellular and extracellular electron transport in methanosarcina acetivorans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10153276/
https://www.ncbi.nlm.nih.gov/pubmed/37131651
http://dx.doi.org/10.1101/2023.04.20.537704
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