Stabilizing microbial communities by looped mass transfer
- Building and changing a microbiome at will and maintaining it over hundreds of generations has so far proven challenging. Despite best efforts, complex microbiomes appear to be susceptible to large stochastic fluctuations. Current capabilities to assemble and control stable complex microbiomes are limited. Here, we propose a looped mass transfer design that stabilizes microbiomes over long periods of time. Five local microbiomes were continuously grown in parallel for over 114 generations and connected by a loop to a regional pool. Mass transfer rates were altered and microbiome dynamics were monitored using quantitative high-throughput flow cytometry and taxonomic sequencing of whole communities and sorted subcommunities. Increased mass transfer rates reduced local and temporal variation in microbiome assembly, did not affect functions, and overcame stochasticity, with all microbiomes exhibiting high constancy and increasing resistance. Mass transfer synchronized the structures of the five local microbiomes and nestedness of certainBuilding and changing a microbiome at will and maintaining it over hundreds of generations has so far proven challenging. Despite best efforts, complex microbiomes appear to be susceptible to large stochastic fluctuations. Current capabilities to assemble and control stable complex microbiomes are limited. Here, we propose a looped mass transfer design that stabilizes microbiomes over long periods of time. Five local microbiomes were continuously grown in parallel for over 114 generations and connected by a loop to a regional pool. Mass transfer rates were altered and microbiome dynamics were monitored using quantitative high-throughput flow cytometry and taxonomic sequencing of whole communities and sorted subcommunities. Increased mass transfer rates reduced local and temporal variation in microbiome assembly, did not affect functions, and overcame stochasticity, with all microbiomes exhibiting high constancy and increasing resistance. Mass transfer synchronized the structures of the five local microbiomes and nestedness of certain cell types was eminent. Mass transfer increased cell number and thus decreased net growth rates mu'. Subsets of cells that did not show net growth mu'SCx were rescued by the regional pool R and thus remained part of the microbiome. The loop in mass transfer ensured the survival of cells that would otherwise go extinct, even if they did not grow in all local microbiomes or grew more slowly than the actual dilution rate D would allow. The rescue effect, known from metacommunity theory, was the main stabilizing mechanism leading to synchrony and survival of subcommunities, despite differences in cell physiological properties, including growth rates.…
Author details: | Shuang LiORCiD, Nafi'u AbdulkadirORCiD, Florian Schattenberg, Ulisses Nunes da RochaORCiD, Volker GrimmORCiDGND, Susann MüllerORCiDGND, Zishu LiuORCiDGND |
---|---|
DOI: | https://doi.org/10.1073/pnas.2117814119 |
ISSN: | 0027-8424 |
ISSN: | 1091-6490 |
Pubmed ID: | https://pubmed.ncbi.nlm.nih.gov/35446625 |
Title of parent work (English): | Proceedings of the National Academy of Sciences of the United States of America : PNAS |
Publisher: | National Acad. of Sciences |
Place of publishing: | Washington |
Publication type: | Article |
Language: | English |
Date of first publication: | 2022/04/21 |
Publication year: | 2022 |
Release date: | 2024/02/21 |
Tag: | community cytometry; metacommunity assembly; microbial; microbial ecology; single-cell analytics; stability |
Volume: | 119 |
Issue: | 17 |
Article number: | e2117814119 |
Number of pages: | 11 |
Funding institution: | European Regional Development Funds (EFRE-Europe Funds Saxony); [100192205]; Helmholtz Association, Helmholtz-Centre for Environmental; Research - UFZ; Chinese Scholarship Council; Petroleum Technology; Development Fund; German Academic Exchange Service [57401043] |
Organizational units: | Mathematisch-Naturwissenschaftliche Fakultät / Institut für Umweltwissenschaften und Geographie |
DDC classification: | 5 Naturwissenschaften und Mathematik / 55 Geowissenschaften, Geologie / 550 Geowissenschaften |
Peer review: | Referiert |
License (German): | CC-BY - Namensnennung 4.0 International |