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Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities

Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, it would be usef...

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Autores principales: Martinson, Jonathan N. V., Chacón, Jeremy M., Smith, Brian A., Villarreal, Alex R., Hunter, Ryan C., Harcombe, William R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10197568/
https://www.ncbi.nlm.nih.gov/pubmed/37214994
http://dx.doi.org/10.1101/2023.05.08.539835
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author Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
author_facet Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
author_sort Martinson, Jonathan N. V.
collection PubMed
description Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, it would be useful to know if the type of ecological interaction, such as mutualism or competition, changes the average effect of a mutation (i.e., the mean of the distribution of fitness effects). Furthermore, how often does increasing community complexity alter the impact of species interactions on mutant fitness? To address these questions, we created a transposon mutant library in Salmonella enterica and measured the fitness of loss of function mutations in 3,550 genes when grown alone versus competitive co-culture or mutualistic co-culture with Escherichia coli and Methylorubrum extorquens. We found that mutualism reduces the average impact of mutations, while competition had no effect. Additionally, mutant fitness in the 3-species communities can be predicted by averaging the fitness in each 2-species community. Finally, the fitness effects of several knockouts in the mutualistic communities were surprising. We discovered that S. enterica is obtaining a different source of carbon and more vitamins and amino acids than we had expected. Our results suggest that species interactions can predictably impact fitness effect distributions, in turn suggesting that evolution may ultimately be predictable in multi-species communities.
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spelling pubmed-101975682023-05-20 Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities Martinson, Jonathan N. V. Chacón, Jeremy M. Smith, Brian A. Villarreal, Alex R. Hunter, Ryan C. Harcombe, William R. bioRxiv Article Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, it would be useful to know if the type of ecological interaction, such as mutualism or competition, changes the average effect of a mutation (i.e., the mean of the distribution of fitness effects). Furthermore, how often does increasing community complexity alter the impact of species interactions on mutant fitness? To address these questions, we created a transposon mutant library in Salmonella enterica and measured the fitness of loss of function mutations in 3,550 genes when grown alone versus competitive co-culture or mutualistic co-culture with Escherichia coli and Methylorubrum extorquens. We found that mutualism reduces the average impact of mutations, while competition had no effect. Additionally, mutant fitness in the 3-species communities can be predicted by averaging the fitness in each 2-species community. Finally, the fitness effects of several knockouts in the mutualistic communities were surprising. We discovered that S. enterica is obtaining a different source of carbon and more vitamins and amino acids than we had expected. Our results suggest that species interactions can predictably impact fitness effect distributions, in turn suggesting that evolution may ultimately be predictable in multi-species communities. Cold Spring Harbor Laboratory 2023-05-08 /pmc/articles/PMC10197568/ /pubmed/37214994 http://dx.doi.org/10.1101/2023.05.08.539835 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_full Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_fullStr Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_full_unstemmed Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_short Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_sort mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10197568/
https://www.ncbi.nlm.nih.gov/pubmed/37214994
http://dx.doi.org/10.1101/2023.05.08.539835
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