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A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea
Heterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor. The ancient origin is consistent with the widespread occurrence of genes encoding putative HdrABC homologs in metabolically diverse prokaryotes...
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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American Society for Microbiology
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5296606/ https://www.ncbi.nlm.nih.gov/pubmed/28174314 http://dx.doi.org/10.1128/mBio.02285-16 |
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author | Yan, Zhen Wang, Mingyu Ferry, James G. |
author_facet | Yan, Zhen Wang, Mingyu Ferry, James G. |
author_sort | Yan, Zhen |
collection | PubMed |
description | Heterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor. The ancient origin is consistent with the widespread occurrence of genes encoding putative HdrABC homologs in metabolically diverse prokaryotes predicting diverse physiological functions; however, only one HdrABC has been characterized and that was from a narrow metabolic group of obligate CO(2)-reducing methanogenic anaerobes (methanogens) from the domain Archaea. Here we report the biochemical characterization of an HdrABC homolog (HdrA2B2C2) from the acetate-utilizing methanogen Methanosarcina acetivorans with unusual properties structurally and functionally distinct from the only other HdrABC characterized. Homologs of the HdrA2B2C2 archetype are present in phylogenetically and metabolically diverse species from the domains Bacteria and Archaea. The expression of the individual HdrA2, HdrB2, and HdrB2C2 enzymes in Escherichia coli, and reconstitution of an active HdrA2B2C2 complex, revealed an intersubunit electron transport pathway dependent on ferredoxin or coenzyme F(420) (F(420)H(2)) as an electron donor. Remarkably, HdrA2B2C2 couples the previously unknown endergonic oxidation of F(420)H(2) and reduction of ferredoxin with the exergonic oxidation of F(420)H(2) and reduction of the heterodisulfide of coenzyme M and coenzyme B (CoMS-SCoB). The unique electron bifurcation predicts a role for HdrA2B2C2 in Fe(III)-dependent anaerobic methane oxidation (ANME) by M. acetivorans and uncultured species from ANME environments. HdrA2B2C2, ubiquitous in acetotrophic methanogens, was shown to participate in electron transfer during acetotrophic growth of M. acetivorans and proposed to be essential for growth in the environment when acetate is limiting. |
format | Online Article Text |
id | pubmed-5296606 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-52966062017-02-13 A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea Yan, Zhen Wang, Mingyu Ferry, James G. mBio Research Article Heterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor. The ancient origin is consistent with the widespread occurrence of genes encoding putative HdrABC homologs in metabolically diverse prokaryotes predicting diverse physiological functions; however, only one HdrABC has been characterized and that was from a narrow metabolic group of obligate CO(2)-reducing methanogenic anaerobes (methanogens) from the domain Archaea. Here we report the biochemical characterization of an HdrABC homolog (HdrA2B2C2) from the acetate-utilizing methanogen Methanosarcina acetivorans with unusual properties structurally and functionally distinct from the only other HdrABC characterized. Homologs of the HdrA2B2C2 archetype are present in phylogenetically and metabolically diverse species from the domains Bacteria and Archaea. The expression of the individual HdrA2, HdrB2, and HdrB2C2 enzymes in Escherichia coli, and reconstitution of an active HdrA2B2C2 complex, revealed an intersubunit electron transport pathway dependent on ferredoxin or coenzyme F(420) (F(420)H(2)) as an electron donor. Remarkably, HdrA2B2C2 couples the previously unknown endergonic oxidation of F(420)H(2) and reduction of ferredoxin with the exergonic oxidation of F(420)H(2) and reduction of the heterodisulfide of coenzyme M and coenzyme B (CoMS-SCoB). The unique electron bifurcation predicts a role for HdrA2B2C2 in Fe(III)-dependent anaerobic methane oxidation (ANME) by M. acetivorans and uncultured species from ANME environments. HdrA2B2C2, ubiquitous in acetotrophic methanogens, was shown to participate in electron transfer during acetotrophic growth of M. acetivorans and proposed to be essential for growth in the environment when acetate is limiting. American Society for Microbiology 2017-02-07 /pmc/articles/PMC5296606/ /pubmed/28174314 http://dx.doi.org/10.1128/mBio.02285-16 Text en Copyright © 2017 Yan et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Yan, Zhen Wang, Mingyu Ferry, James G. A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title | A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title_full | A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title_fullStr | A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title_full_unstemmed | A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title_short | A Ferredoxin- and F(420)H(2)-Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea |
title_sort | ferredoxin- and f(420)h(2)-dependent, electron-bifurcating, heterodisulfide reductase with homologs in the domains bacteria and archaea |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5296606/ https://www.ncbi.nlm.nih.gov/pubmed/28174314 http://dx.doi.org/10.1128/mBio.02285-16 |
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