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Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community

Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the...

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Autores principales: Barber, Jake N., Nicholson, Luke C., Woods, Laura C., Judd, Louise M., Sezmis, Aysha L., Hawkey, Jane, Holt, Kathryn E., McDonald, Michael J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9039033/
https://www.ncbi.nlm.nih.gov/pubmed/35066567
http://dx.doi.org/10.1038/s41396-022-01191-1
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author Barber, Jake N.
Nicholson, Luke C.
Woods, Laura C.
Judd, Louise M.
Sezmis, Aysha L.
Hawkey, Jane
Holt, Kathryn E.
McDonald, Michael J.
author_facet Barber, Jake N.
Nicholson, Luke C.
Woods, Laura C.
Judd, Louise M.
Sezmis, Aysha L.
Hawkey, Jane
Holt, Kathryn E.
McDonald, Michael J.
author_sort Barber, Jake N.
collection PubMed
description Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the stability and function of the emergent community. Here we study experimental cultures of a simple, ecologically stable community of Saccharomyces cerevisiae and Lactobacillus plantarum, in order to understand how the presence or absence of a species impacts coexistence over evolutionary timescales. We found that evolution in coculture led to drastically altered evolutionary outcomes for L. plantarum, but not S. cerevisiae. Both monoculture- and co-culture-evolved L. plantarum evolved dozens of mutations over 925 generations of evolution, but only L. plantarum that had evolved in isolation from S. cerevisiae lost the capacity to coexist with S. cerevisiae. We find that the evolutionary loss of ecological stability corresponds with fitness differences between monoculture-evolved L. plantarum and S. cerevisiae and genetic changes that repeatedly evolve across the replicate populations of L. plantarum. This work shows how coevolution within a community can prevent destabilising evolution in individual species, thereby preserving ecological diversity and stability, despite rapid adaptation.
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spelling pubmed-90390332022-04-28 Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community Barber, Jake N. Nicholson, Luke C. Woods, Laura C. Judd, Louise M. Sezmis, Aysha L. Hawkey, Jane Holt, Kathryn E. McDonald, Michael J. ISME J Article Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the stability and function of the emergent community. Here we study experimental cultures of a simple, ecologically stable community of Saccharomyces cerevisiae and Lactobacillus plantarum, in order to understand how the presence or absence of a species impacts coexistence over evolutionary timescales. We found that evolution in coculture led to drastically altered evolutionary outcomes for L. plantarum, but not S. cerevisiae. Both monoculture- and co-culture-evolved L. plantarum evolved dozens of mutations over 925 generations of evolution, but only L. plantarum that had evolved in isolation from S. cerevisiae lost the capacity to coexist with S. cerevisiae. We find that the evolutionary loss of ecological stability corresponds with fitness differences between monoculture-evolved L. plantarum and S. cerevisiae and genetic changes that repeatedly evolve across the replicate populations of L. plantarum. This work shows how coevolution within a community can prevent destabilising evolution in individual species, thereby preserving ecological diversity and stability, despite rapid adaptation. Nature Publishing Group UK 2022-01-22 2022-05 /pmc/articles/PMC9039033/ /pubmed/35066567 http://dx.doi.org/10.1038/s41396-022-01191-1 Text en © Crown 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Barber, Jake N.
Nicholson, Luke C.
Woods, Laura C.
Judd, Louise M.
Sezmis, Aysha L.
Hawkey, Jane
Holt, Kathryn E.
McDonald, Michael J.
Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title_full Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title_fullStr Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title_full_unstemmed Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title_short Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
title_sort species interactions constrain adaptation and preserve ecological stability in an experimental microbial community
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9039033/
https://www.ncbi.nlm.nih.gov/pubmed/35066567
http://dx.doi.org/10.1038/s41396-022-01191-1
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