Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities
ABSTRACT Biotic factors that influence the temporal stability of microbial community functioning are an emerging research focus for the control of natural and engineered systems. The discovery of common features within community ensembles that differ in functional stability over time is a starting p...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-06-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01220-22 |
| _version_ | 1827913602069168128 |
|---|---|
| author | Eric R. Moore Dennis Suazo Joany Babilonia Kyana N. Montoya La Verne Gallegos-Graves Sanna Sevanto John Dunbar Michaeline B. N. Albright |
| author_facet | Eric R. Moore Dennis Suazo Joany Babilonia Kyana N. Montoya La Verne Gallegos-Graves Sanna Sevanto John Dunbar Michaeline B. N. Albright |
| author_sort | Eric R. Moore |
| collection | DOAJ |
| description | ABSTRACT Biotic factors that influence the temporal stability of microbial community functioning are an emerging research focus for the control of natural and engineered systems. The discovery of common features within community ensembles that differ in functional stability over time is a starting point to explore biotic factors. We serially propagated a suite of soil microbial communities through five generations of 28-day microcosm incubations to examine microbial community compositional and functional stability during plant litter decomposition. Using dissolved organic carbon (DOC) abundance as a target function, we hypothesized that microbial diversity, compositional stability, and associated changes in interactions would explain the relative stability of the ecosystem function between generations. Communities with initially high DOC abundance tended to converge towards a “low DOC” phenotype within two generations, but across all microcosms, functional stability between generations was highly variable. By splitting communities into two cohorts based on their relative DOC functional stability, we found that compositional shifts, diversity, and interaction network complexity were associated with the stability of DOC abundance between generations. Further, our results showed that legacy effects were important in determining compositional and functional outcomes, and we identified taxa associated with high DOC abundance. In the context of litter decomposition, achieving functionally stable communities is required to utilize soil microbiomes to increase DOC abundance and long-term terrestrial DOC sequestration as one solution to reduce atmospheric carbon dioxide concentrations. Identifying factors that stabilize function for a community of interest may improve the success of microbiome engineering applications. IMPORTANCE Microbial community functioning can be highly dynamic over time. Identifying and understanding biotic factors that control functional stability is of significant interest for natural and engineered communities alike. Using plant litter–decomposing communities as a model system, this study examined the stability of ecosystem function over time following repeated community transfers. By identifying microbial community features that are associated with stable ecosystem functions, microbial communities can be manipulated in ways that promote the consistency and reliability of the desired function, improving outcomes and increasing the utility of microorganisms. |
| first_indexed | 2024-03-13T02:32:16Z |
| format | Article |
| id | doaj.art-82139c8c4993477599620880fbedecb4 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-13T02:32:16Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-82139c8c4993477599620880fbedecb42023-06-29T13:00:40ZengAmerican Society for MicrobiologymSystems2379-50772023-06-018310.1128/msystems.01220-22Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communitiesEric R. Moore0Dennis Suazo1Joany Babilonia2Kyana N. Montoya3La Verne Gallegos-Graves4Sanna Sevanto5John Dunbar6Michaeline B. N. Albright7Bioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USAEarth and Environmental Sciences Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USABioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USAABSTRACT Biotic factors that influence the temporal stability of microbial community functioning are an emerging research focus for the control of natural and engineered systems. The discovery of common features within community ensembles that differ in functional stability over time is a starting point to explore biotic factors. We serially propagated a suite of soil microbial communities through five generations of 28-day microcosm incubations to examine microbial community compositional and functional stability during plant litter decomposition. Using dissolved organic carbon (DOC) abundance as a target function, we hypothesized that microbial diversity, compositional stability, and associated changes in interactions would explain the relative stability of the ecosystem function between generations. Communities with initially high DOC abundance tended to converge towards a “low DOC” phenotype within two generations, but across all microcosms, functional stability between generations was highly variable. By splitting communities into two cohorts based on their relative DOC functional stability, we found that compositional shifts, diversity, and interaction network complexity were associated with the stability of DOC abundance between generations. Further, our results showed that legacy effects were important in determining compositional and functional outcomes, and we identified taxa associated with high DOC abundance. In the context of litter decomposition, achieving functionally stable communities is required to utilize soil microbiomes to increase DOC abundance and long-term terrestrial DOC sequestration as one solution to reduce atmospheric carbon dioxide concentrations. Identifying factors that stabilize function for a community of interest may improve the success of microbiome engineering applications. IMPORTANCE Microbial community functioning can be highly dynamic over time. Identifying and understanding biotic factors that control functional stability is of significant interest for natural and engineered communities alike. Using plant litter–decomposing communities as a model system, this study examined the stability of ecosystem function over time following repeated community transfers. By identifying microbial community features that are associated with stable ecosystem functions, microbial communities can be manipulated in ways that promote the consistency and reliability of the desired function, improving outcomes and increasing the utility of microorganisms.https://journals.asm.org/doi/10.1128/msystems.01220-22bacteriacarbon cyclingfungimicrobial interactionsmicrobiome engineeringserial propagations |
| spellingShingle | Eric R. Moore Dennis Suazo Joany Babilonia Kyana N. Montoya La Verne Gallegos-Graves Sanna Sevanto John Dunbar Michaeline B. N. Albright Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities mSystems bacteria carbon cycling fungi microbial interactions microbiome engineering serial propagations |
| title | Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities |
| title_full | Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities |
| title_fullStr | Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities |
| title_full_unstemmed | Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities |
| title_short | Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities |
| title_sort | drivers of stability and transience in composition functioning links during serial propagation of litter decomposing microbial communities |
| topic | bacteria carbon cycling fungi microbial interactions microbiome engineering serial propagations |
| url | https://journals.asm.org/doi/10.1128/msystems.01220-22 |
| work_keys_str_mv | AT ericrmoore driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT dennissuazo driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT joanybabilonia driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT kyananmontoya driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT lavernegallegosgraves driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT sannasevanto driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT johndunbar driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities AT michaelinebnalbright driversofstabilityandtransienceincompositionfunctioninglinksduringserialpropagationoflitterdecomposingmicrobialcommunities |