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Synthetic Methane-Consuming Communities from a Natural Lake Sediment

The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood. Synthetic microbial communities provide reduced-complexity models that allow an examination of ecological theories under defined and con...

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Autores principales: Yu, Zheng, Groom, Joseph, Zheng, Yue, Chistoserdova, Ludmila, Huang, Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6650549/
https://www.ncbi.nlm.nih.gov/pubmed/31337718
http://dx.doi.org/10.1128/mBio.01072-19
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author Yu, Zheng
Groom, Joseph
Zheng, Yue
Chistoserdova, Ludmila
Huang, Jing
author_facet Yu, Zheng
Groom, Joseph
Zheng, Yue
Chistoserdova, Ludmila
Huang, Jing
author_sort Yu, Zheng
collection PubMed
description The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood. Synthetic microbial communities provide reduced-complexity models that allow an examination of ecological theories under defined and controlled conditions. In this study, we applied a multiphasic approach to study synthetic methane-oxidizing communities and species interactions as proxies to the natural communities. Our results confirm that, under selective pressures, natural-sediment communities of high complexity simplify rapidly, selecting for several major functional guilds, the major partners in methane oxidation being the Methylococcaceae methanotrophs and the Methylophilaceae methylotrophs, along with minor but persistent partners, members of Burkholderiales and Flavobacteriales. As a proof of concept, we established minimalist synthetic communities that were representative of the four functional guilds to demonstrate the dependency of the non-methane-utilizing species on the methanotrophs as the primary carbon-providing species. We observed that in communities consisting of multiple representatives of the key guilds, members of the same guild appeared to compete for resources. For example, when two methanotrophs of the same family were present, the two expressed similar key methanotrophy pathways and responded similarly to changing environmental conditions, suggesting that they perform a similar keystone function in situ. Similar observations were made for the Methylophilaceae. However, differences were noted in the expression of auxiliary and unique genes among strains of the same functional guild, reflecting differential adaptation and suggesting mechanisms for competition. At the same time, differences were also noted in the performances of partners with specific metabolic schemes. For example, a mutant of Methylotenera mobilis impaired in nitrate utilization behaved as a more efficient cooperator in methane consumption, suggesting that the loss of function may lead to changes in communal behavior. Overall, we demonstrate the robust nature of synthetic communities built of native lake sediment strains and their utility in addressing important ecological questions while using a simplified model.
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spelling pubmed-66505492019-08-06 Synthetic Methane-Consuming Communities from a Natural Lake Sediment Yu, Zheng Groom, Joseph Zheng, Yue Chistoserdova, Ludmila Huang, Jing mBio Research Article The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood. Synthetic microbial communities provide reduced-complexity models that allow an examination of ecological theories under defined and controlled conditions. In this study, we applied a multiphasic approach to study synthetic methane-oxidizing communities and species interactions as proxies to the natural communities. Our results confirm that, under selective pressures, natural-sediment communities of high complexity simplify rapidly, selecting for several major functional guilds, the major partners in methane oxidation being the Methylococcaceae methanotrophs and the Methylophilaceae methylotrophs, along with minor but persistent partners, members of Burkholderiales and Flavobacteriales. As a proof of concept, we established minimalist synthetic communities that were representative of the four functional guilds to demonstrate the dependency of the non-methane-utilizing species on the methanotrophs as the primary carbon-providing species. We observed that in communities consisting of multiple representatives of the key guilds, members of the same guild appeared to compete for resources. For example, when two methanotrophs of the same family were present, the two expressed similar key methanotrophy pathways and responded similarly to changing environmental conditions, suggesting that they perform a similar keystone function in situ. Similar observations were made for the Methylophilaceae. However, differences were noted in the expression of auxiliary and unique genes among strains of the same functional guild, reflecting differential adaptation and suggesting mechanisms for competition. At the same time, differences were also noted in the performances of partners with specific metabolic schemes. For example, a mutant of Methylotenera mobilis impaired in nitrate utilization behaved as a more efficient cooperator in methane consumption, suggesting that the loss of function may lead to changes in communal behavior. Overall, we demonstrate the robust nature of synthetic communities built of native lake sediment strains and their utility in addressing important ecological questions while using a simplified model. American Society for Microbiology 2019-07-23 /pmc/articles/PMC6650549/ /pubmed/31337718 http://dx.doi.org/10.1128/mBio.01072-19 Text en Copyright © 2019 Yu et al. https://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 (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Yu, Zheng
Groom, Joseph
Zheng, Yue
Chistoserdova, Ludmila
Huang, Jing
Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title_full Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title_fullStr Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title_full_unstemmed Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title_short Synthetic Methane-Consuming Communities from a Natural Lake Sediment
title_sort synthetic methane-consuming communities from a natural lake sediment
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6650549/
https://www.ncbi.nlm.nih.gov/pubmed/31337718
http://dx.doi.org/10.1128/mBio.01072-19
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