H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>

ABSTRACT Hydrogenotrophic methanogenic Archaea require reduced ferredoxin as an anaplerotic source of electrons for methanogenesis. H2 oxidation by the hydrogenase Eha provides these electrons, consistent with an H2 requirement for growth. Here we report the identification of alternative pathways of...

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Autores principales: Kyle C. Costa, Thomas J. Lie, Michael A. Jacobs, John A. Leigh
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:8c1756233a9b4953acf48bd5038ec03e2021-11-15T15:40:28ZH<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>10.1128/mBio.00062-132150-7511https://doaj.org/article/8c1756233a9b4953acf48bd5038ec03e2013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00062-13https://doaj.org/toc/2150-7511ABSTRACT Hydrogenotrophic methanogenic Archaea require reduced ferredoxin as an anaplerotic source of electrons for methanogenesis. H2 oxidation by the hydrogenase Eha provides these electrons, consistent with an H2 requirement for growth. Here we report the identification of alternative pathways of ferredoxin reduction in Methanococcus maripaludis that operate independently of Eha to stimulate methanogenesis. A suppressor mutation that increased expression of the glycolytic enzyme glyceraldehyde-3-phosphate:ferredoxin oxidoreductase resulted in a strain capable of H2-independent ferredoxin reduction and growth with formate as the sole electron donor. In this background, it was possible to eliminate all seven hydrogenases of M. maripaludis. Alternatively, carbon monoxide oxidation by carbon monoxide dehydrogenase could also generate reduced ferredoxin that feeds into methanogenesis. In either case, the reduced ferredoxin generated was inefficient at stimulating methanogenesis, resulting in a slow growth phenotype. As methanogenesis is limited by the availability of reduced ferredoxin under these conditions, other electron donors, such as reduced coenzyme F420, should be abundant. Indeed, when F420-reducing hydrogenase was reintroduced into the hydrogenase-free mutant, the equilibrium of H2 production via an F420-dependent formate:H2 lyase activity shifted markedly toward H2 compared to the wild type. IMPORTANCE Hydrogenotrophic methanogens are thought to require H2 as a substrate for growth and methanogenesis. Here we show alternative pathways in methanogenic metabolism that alleviate this H2 requirement and demonstrate, for the first time, a hydrogenotrophic methanogen that is capable of growth in the complete absence of H2. The demonstration of alternative pathways in methanogenic metabolism suggests that this important group of organisms is metabolically more versatile than previously thought.Kyle C. CostaThomas J. LieMichael A. JacobsJohn A. LeighAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Kyle C. Costa
Thomas J. Lie
Michael A. Jacobs
John A. Leigh
H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
description ABSTRACT Hydrogenotrophic methanogenic Archaea require reduced ferredoxin as an anaplerotic source of electrons for methanogenesis. H2 oxidation by the hydrogenase Eha provides these electrons, consistent with an H2 requirement for growth. Here we report the identification of alternative pathways of ferredoxin reduction in Methanococcus maripaludis that operate independently of Eha to stimulate methanogenesis. A suppressor mutation that increased expression of the glycolytic enzyme glyceraldehyde-3-phosphate:ferredoxin oxidoreductase resulted in a strain capable of H2-independent ferredoxin reduction and growth with formate as the sole electron donor. In this background, it was possible to eliminate all seven hydrogenases of M. maripaludis. Alternatively, carbon monoxide oxidation by carbon monoxide dehydrogenase could also generate reduced ferredoxin that feeds into methanogenesis. In either case, the reduced ferredoxin generated was inefficient at stimulating methanogenesis, resulting in a slow growth phenotype. As methanogenesis is limited by the availability of reduced ferredoxin under these conditions, other electron donors, such as reduced coenzyme F420, should be abundant. Indeed, when F420-reducing hydrogenase was reintroduced into the hydrogenase-free mutant, the equilibrium of H2 production via an F420-dependent formate:H2 lyase activity shifted markedly toward H2 compared to the wild type. IMPORTANCE Hydrogenotrophic methanogens are thought to require H2 as a substrate for growth and methanogenesis. Here we show alternative pathways in methanogenic metabolism that alleviate this H2 requirement and demonstrate, for the first time, a hydrogenotrophic methanogen that is capable of growth in the complete absence of H2. The demonstration of alternative pathways in methanogenic metabolism suggests that this important group of organisms is metabolically more versatile than previously thought.
format article
author Kyle C. Costa
Thomas J. Lie
Michael A. Jacobs
John A. Leigh
author_facet Kyle C. Costa
Thomas J. Lie
Michael A. Jacobs
John A. Leigh
author_sort Kyle C. Costa
title H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
title_short H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
title_full H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
title_fullStr H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
title_full_unstemmed H<sub>2</sub>-Independent Growth of the Hydrogenotrophic Methanogen <named-content content-type="genus-species">Methanococcus maripaludis</named-content>
title_sort h<sub>2</sub>-independent growth of the hydrogenotrophic methanogen <named-content content-type="genus-species">methanococcus maripaludis</named-content>
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/8c1756233a9b4953acf48bd5038ec03e
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