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Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community

Microorganisms in nature do not exist in isolation but rather interact with other species in their environment. Some microbes interact via syntrophic associations, in which the metabolic by-products of one species serve as nutrients for another. These associations sustain a variety of natural commun...

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Autores principales: Hamilton, Joshua J., Calixto Contreras, Montserrat, Reed, Jennifer L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4509577/
https://www.ncbi.nlm.nih.gov/pubmed/26147299
http://dx.doi.org/10.1371/journal.pcbi.1004364
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author Hamilton, Joshua J.
Calixto Contreras, Montserrat
Reed, Jennifer L.
author_facet Hamilton, Joshua J.
Calixto Contreras, Montserrat
Reed, Jennifer L.
author_sort Hamilton, Joshua J.
collection PubMed
description Microorganisms in nature do not exist in isolation but rather interact with other species in their environment. Some microbes interact via syntrophic associations, in which the metabolic by-products of one species serve as nutrients for another. These associations sustain a variety of natural communities, including those involved in methanogenesis. In anaerobic syntrophic communities, energy is transferred from one species to another, either through direct contact and exchange of electrons, or through small molecule diffusion. Thermodynamics plays an important role in governing these interactions, as the oxidation reactions carried out by the first community member are only possible because degradation products are consumed by the second community member. This work presents the development and analysis of genome-scale network reconstructions of the bacterium Syntrophobacter fumaroxidans and the methanogenic archaeon Methanospirillum hungatei. The models were used to verify proposed mechanisms of ATP production within each species. We then identified additional constraints and the cellular objective function required to match experimental observations. The thermodynamic S. fumaroxidans model could not explain why S. fumaroxidans does not produce H(2) in monoculture, indicating that current methods might not adequately estimate the thermodynamics, or that other cellular processes (e.g., regulation) play a role. We also developed a thermodynamic coculture model of the association between the organisms. The coculture model correctly predicted the exchange of both H(2) and formate between the two species and suggested conditions under which H(2) and formate produced by S. fumaroxidans would be fully consumed by M. hungatei.
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spelling pubmed-45095772015-07-24 Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community Hamilton, Joshua J. Calixto Contreras, Montserrat Reed, Jennifer L. PLoS Comput Biol Research Article Microorganisms in nature do not exist in isolation but rather interact with other species in their environment. Some microbes interact via syntrophic associations, in which the metabolic by-products of one species serve as nutrients for another. These associations sustain a variety of natural communities, including those involved in methanogenesis. In anaerobic syntrophic communities, energy is transferred from one species to another, either through direct contact and exchange of electrons, or through small molecule diffusion. Thermodynamics plays an important role in governing these interactions, as the oxidation reactions carried out by the first community member are only possible because degradation products are consumed by the second community member. This work presents the development and analysis of genome-scale network reconstructions of the bacterium Syntrophobacter fumaroxidans and the methanogenic archaeon Methanospirillum hungatei. The models were used to verify proposed mechanisms of ATP production within each species. We then identified additional constraints and the cellular objective function required to match experimental observations. The thermodynamic S. fumaroxidans model could not explain why S. fumaroxidans does not produce H(2) in monoculture, indicating that current methods might not adequately estimate the thermodynamics, or that other cellular processes (e.g., regulation) play a role. We also developed a thermodynamic coculture model of the association between the organisms. The coculture model correctly predicted the exchange of both H(2) and formate between the two species and suggested conditions under which H(2) and formate produced by S. fumaroxidans would be fully consumed by M. hungatei. Public Library of Science 2015-07-06 /pmc/articles/PMC4509577/ /pubmed/26147299 http://dx.doi.org/10.1371/journal.pcbi.1004364 Text en © 2015 Hamilton et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
spellingShingle Research Article
Hamilton, Joshua J.
Calixto Contreras, Montserrat
Reed, Jennifer L.
Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title_full Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title_fullStr Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title_full_unstemmed Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title_short Thermodynamics and H(2) Transfer in a Methanogenic, Syntrophic Community
title_sort thermodynamics and h(2) transfer in a methanogenic, syntrophic community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4509577/
https://www.ncbi.nlm.nih.gov/pubmed/26147299
http://dx.doi.org/10.1371/journal.pcbi.1004364
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