Thermodynamics and H2 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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Published in | PLoS computational biology Vol. 11; no. 7; p. e1004364 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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01.07.2015
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Abstract | 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 H2 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 H2 and formate between the two species and suggested conditions under which H2 and formate produced by S. fumaroxidans would be fully consumed by M. hungatei. |
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AbstractList | 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
.
Natural and engineered microbial communities can contain up to hundreds of interacting microbes. These interactions may be positive, negative, or neutral, as well as obligate or facultative. Syntrophy is an obligate, positive interaction, in which one species lives off the metabolic by-products of another. Syntrophic associations play an important role in sustaining a variety of natural communities, including those involved in the breakdown and conversion of short-chain fatty acids (e.g., propionate) to methane. In many syntrophic communities, electrons are transferred from one species to the other through small molecule diffusion. In this work, we expand the study of a two-member syntrophic, methanogenic community through the development and analysis of computational models for both species: the bacterium
Syntrophobacter fumaroxidans
and the methanogenic archaeon
Methanospirillum hungatei
. These models were used to analyze energy conservation mechanisms within each species, as well as small molecule exchange between the two organisms in coculture. The coculture model correctly predicted the exchange of both H
2
and formate between the two species and suggested conditions under which these molecules would be fully metabolized within the 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 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 H2 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 H2 and formate between the two species and suggested conditions under which H2 and formate produced by S. fumaroxidans would be fully consumed by M. hungatei. |
Author | Calixto Contreras, Montserrat Reed, Jennifer L Hamilton, Joshua J |
AuthorAffiliation | Department of Chemical and Biological Engineering, University of Wisconsin-Madison, Madison, Wisconsin, United States of America The Pennsylvania State University, UNITED STATES |
AuthorAffiliation_xml | – name: The Pennsylvania State University, UNITED STATES – name: Department of Chemical and Biological Engineering, University of Wisconsin-Madison, Madison, Wisconsin, United States of America |
Author_xml | – sequence: 1 givenname: Joshua J surname: Hamilton fullname: Hamilton, Joshua J organization: Department of Chemical and Biological Engineering, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – sequence: 2 givenname: Montserrat surname: Calixto Contreras fullname: Calixto Contreras, Montserrat organization: Department of Chemical and Biological Engineering, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – sequence: 3 givenname: Jennifer L surname: Reed fullname: Reed, Jennifer L organization: Department of Chemical and Biological Engineering, University of Wisconsin-Madison, Madison, Wisconsin, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26147299$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JJH JLR. Performed the experiments: JJH MCC. Analyzed the data: JJH JLR. Wrote the paper: JJH JLR. The authors have declared that no competing interests exist. |
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SubjectTerms | Computer Simulation Deltaproteobacteria - metabolism Energy Transfer - physiology Hydrogen - metabolism Methane - metabolism Methanospirillum - metabolism Microbial Consortia - physiology Models, Biological Symbiosis - physiology Thermodynamics |
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Title | Thermodynamics and H2 Transfer in a Methanogenic, Syntrophic Community |
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