Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient
Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for a...
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| Published in: | Frontiers in microbiology Vol. 11; p. 796 |
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| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
Frontiers Research Foundation
15.05.2020
Frontiers Media S.A |
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| ISSN: | 1664-302X, 1664-302X |
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| Abstract | Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions.Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions. |
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| AbstractList | Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions. Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partiallyand fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions. Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions.Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions. |
| Author | Hough, Moira Dorrepaal, Ellen Klepac-Ceraj, Vanja McClure, Amelia Saleska, Scott Rich, Virginia Bolduc, Benjamin |
| AuthorAffiliation | 4 Climate Impacts Research Centre, Umeå University , Umeå , Sweden 2 Department of Biological Sciences, Wellesley College , Wellesley, MA , United States 1 Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ , United States 3 Department of Microbiology, College of Arts and Sciences, The Ohio State University , Columbus, OH , United States |
| AuthorAffiliation_xml | – name: 1 Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ , United States – name: 2 Department of Biological Sciences, Wellesley College , Wellesley, MA , United States – name: 4 Climate Impacts Research Centre, Umeå University , Umeå , Sweden – name: 3 Department of Microbiology, College of Arts and Sciences, The Ohio State University , Columbus, OH , United States |
| Author_xml | – sequence: 1 givenname: Moira surname: Hough fullname: Hough, Moira – sequence: 2 givenname: Amelia surname: McClure fullname: McClure, Amelia – sequence: 3 givenname: Benjamin surname: Bolduc fullname: Bolduc, Benjamin – sequence: 4 givenname: Ellen surname: Dorrepaal fullname: Dorrepaal, Ellen – sequence: 5 givenname: Scott surname: Saleska fullname: Saleska, Scott – sequence: 6 givenname: Vanja surname: Klepac-Ceraj fullname: Klepac-Ceraj, Vanja – sequence: 7 givenname: Virginia surname: Rich fullname: Rich, Virginia |
| BackLink | https://www.osti.gov/biblio/1618929$$D View this record in Osti.gov https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-172852$$DView record from Swedish Publication Index (Umeå universitet) |
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| Copyright | Copyright © 2020 Hough, McClure, Bolduc, Dorrepaal, Saleska, Klepac-Ceraj and Rich. Copyright © 2020 Hough, McClure, Bolduc, Dorrepaal, Saleska, Klepac-Ceraj and Rich. 2020 Hough, McClure, Bolduc, Dorrepaal, Saleska, Klepac-Ceraj and Rich |
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| SubjectTerms | BASIC BIOLOGICAL SCIENCES climate feedbacks IsoGenie Project keystone species microbial community assembly Microbiology permafrost thaw plant-microbial interactions Stordalen Mire |
| Title | Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient |
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