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Phenotypic-dependent variability and the emergence of tolerance in bacterial populations

Ecological and evolutionary dynamics have been historically regarded as unfolding at broadly separated timescales. However, these two types of processes are nowadays well-documented to intersperse much more tightly than traditionally assumed, especially in communities of microorganisms. Advancing th...

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Autores principales: Camacho Mateu, José, Sireci, Matteo, Muñoz, Miguel A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8492070/
https://www.ncbi.nlm.nih.gov/pubmed/34555011
http://dx.doi.org/10.1371/journal.pcbi.1009417
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author Camacho Mateu, José
Sireci, Matteo
Muñoz, Miguel A.
author_facet Camacho Mateu, José
Sireci, Matteo
Muñoz, Miguel A.
author_sort Camacho Mateu, José
collection PubMed
description Ecological and evolutionary dynamics have been historically regarded as unfolding at broadly separated timescales. However, these two types of processes are nowadays well-documented to intersperse much more tightly than traditionally assumed, especially in communities of microorganisms. Advancing the development of mathematical and computational approaches to shed novel light onto eco-evolutionary problems is a challenge of utmost relevance. With this motivation in mind, here we scrutinize recent experimental results showing evidence of rapid evolution of tolerance by lag in bacterial populations that are periodically exposed to antibiotic stress in laboratory conditions. In particular, the distribution of single-cell lag times—i.e., the times that individual bacteria from the community remain in a dormant state to cope with stress—evolves its average value to approximately fit the antibiotic-exposure time. Moreover, the distribution develops right-skewed heavy tails, revealing the presence of individuals with anomalously large lag times. Here, we develop a parsimonious individual-based model mimicking the actual demographic processes of the experimental setup. Individuals are characterized by a single phenotypic trait: their intrinsic lag time, which is transmitted with variation to the progeny. The model—in a version in which the amplitude of phenotypic variations grows with the parent’s lag time—is able to reproduce quite well the key empirical observations. Furthermore, we develop a general mathematical framework allowing us to describe with good accuracy the properties of the stochastic model by means of a macroscopic equation, which generalizes the Crow-Kimura equation in population genetics. Even if the model does not account for all the biological mechanisms (e.g., genetic changes) in a detailed way—i.e., it is a phenomenological one—it sheds light onto the eco-evolutionary dynamics of the problem and can be helpful to design strategies to hinder the emergence of tolerance in bacterial communities. From a broader perspective, this work represents a benchmark for the mathematical framework designed to tackle much more general eco-evolutionary problems, thus paving the road to further research avenues.
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spelling pubmed-84920702021-10-06 Phenotypic-dependent variability and the emergence of tolerance in bacterial populations Camacho Mateu, José Sireci, Matteo Muñoz, Miguel A. PLoS Comput Biol Research Article Ecological and evolutionary dynamics have been historically regarded as unfolding at broadly separated timescales. However, these two types of processes are nowadays well-documented to intersperse much more tightly than traditionally assumed, especially in communities of microorganisms. Advancing the development of mathematical and computational approaches to shed novel light onto eco-evolutionary problems is a challenge of utmost relevance. With this motivation in mind, here we scrutinize recent experimental results showing evidence of rapid evolution of tolerance by lag in bacterial populations that are periodically exposed to antibiotic stress in laboratory conditions. In particular, the distribution of single-cell lag times—i.e., the times that individual bacteria from the community remain in a dormant state to cope with stress—evolves its average value to approximately fit the antibiotic-exposure time. Moreover, the distribution develops right-skewed heavy tails, revealing the presence of individuals with anomalously large lag times. Here, we develop a parsimonious individual-based model mimicking the actual demographic processes of the experimental setup. Individuals are characterized by a single phenotypic trait: their intrinsic lag time, which is transmitted with variation to the progeny. The model—in a version in which the amplitude of phenotypic variations grows with the parent’s lag time—is able to reproduce quite well the key empirical observations. Furthermore, we develop a general mathematical framework allowing us to describe with good accuracy the properties of the stochastic model by means of a macroscopic equation, which generalizes the Crow-Kimura equation in population genetics. Even if the model does not account for all the biological mechanisms (e.g., genetic changes) in a detailed way—i.e., it is a phenomenological one—it sheds light onto the eco-evolutionary dynamics of the problem and can be helpful to design strategies to hinder the emergence of tolerance in bacterial communities. From a broader perspective, this work represents a benchmark for the mathematical framework designed to tackle much more general eco-evolutionary problems, thus paving the road to further research avenues. Public Library of Science 2021-09-23 /pmc/articles/PMC8492070/ /pubmed/34555011 http://dx.doi.org/10.1371/journal.pcbi.1009417 Text en © 2021 Camacho Mateu et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Camacho Mateu, José
Sireci, Matteo
Muñoz, Miguel A.
Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title_full Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title_fullStr Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title_full_unstemmed Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title_short Phenotypic-dependent variability and the emergence of tolerance in bacterial populations
title_sort phenotypic-dependent variability and the emergence of tolerance in bacterial populations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8492070/
https://www.ncbi.nlm.nih.gov/pubmed/34555011
http://dx.doi.org/10.1371/journal.pcbi.1009417
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