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Microbial population dynamics decouple growth response from environmental nutrient concentration

How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely used Monod model, are generally characterized by a maximum growth rate and a half-...

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Autores principales: Fink, Justus Wilhelm, Held, Noelle A., Manhart, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926246/
https://www.ncbi.nlm.nih.gov/pubmed/36598949
http://dx.doi.org/10.1073/pnas.2207295120
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author Fink, Justus Wilhelm
Held, Noelle A.
Manhart, Michael
author_facet Fink, Justus Wilhelm
Held, Noelle A.
Manhart, Michael
author_sort Fink, Justus Wilhelm
collection PubMed
description How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely used Monod model, are generally characterized by a maximum growth rate and a half-saturation concentration of the resource. What values should we expect for these half-saturation concentrations, and how should they depend on the environmental concentration of the resource? We survey growth response data across a wide range of organisms and resources. We find that the half-saturation concentrations vary across orders of magnitude, even for the same organism and resource. To explain this variation, we develop an evolutionary model to show that demographic fluctuations (genetic drift) can constrain the adaptation of half-saturation concentrations. We find that this effect fundamentally differs depending on the type of population dynamics: Populations undergoing periodic bottlenecks of fixed size will adapt their half-saturation concentrations in proportion to the environmental resource concentrations, but populations undergoing periodic dilutions of fixed size will evolve half-saturation concentrations that are largely decoupled from the environmental concentrations. Our model not only provides testable predictions for laboratory evolution experiments, but it also reveals how an evolved half-saturation concentration may not reflect the organism’s environment. In particular, this explains how organisms in resource-rich environments can still evolve fast growth at low resource concentrations. Altogether, our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits.
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spelling pubmed-99262462023-07-04 Microbial population dynamics decouple growth response from environmental nutrient concentration Fink, Justus Wilhelm Held, Noelle A. Manhart, Michael Proc Natl Acad Sci U S A Biological Sciences How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely used Monod model, are generally characterized by a maximum growth rate and a half-saturation concentration of the resource. What values should we expect for these half-saturation concentrations, and how should they depend on the environmental concentration of the resource? We survey growth response data across a wide range of organisms and resources. We find that the half-saturation concentrations vary across orders of magnitude, even for the same organism and resource. To explain this variation, we develop an evolutionary model to show that demographic fluctuations (genetic drift) can constrain the adaptation of half-saturation concentrations. We find that this effect fundamentally differs depending on the type of population dynamics: Populations undergoing periodic bottlenecks of fixed size will adapt their half-saturation concentrations in proportion to the environmental resource concentrations, but populations undergoing periodic dilutions of fixed size will evolve half-saturation concentrations that are largely decoupled from the environmental concentrations. Our model not only provides testable predictions for laboratory evolution experiments, but it also reveals how an evolved half-saturation concentration may not reflect the organism’s environment. In particular, this explains how organisms in resource-rich environments can still evolve fast growth at low resource concentrations. Altogether, our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits. National Academy of Sciences 2023-01-04 2023-01-10 /pmc/articles/PMC9926246/ /pubmed/36598949 http://dx.doi.org/10.1073/pnas.2207295120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Fink, Justus Wilhelm
Held, Noelle A.
Manhart, Michael
Microbial population dynamics decouple growth response from environmental nutrient concentration
title Microbial population dynamics decouple growth response from environmental nutrient concentration
title_full Microbial population dynamics decouple growth response from environmental nutrient concentration
title_fullStr Microbial population dynamics decouple growth response from environmental nutrient concentration
title_full_unstemmed Microbial population dynamics decouple growth response from environmental nutrient concentration
title_short Microbial population dynamics decouple growth response from environmental nutrient concentration
title_sort microbial population dynamics decouple growth response from environmental nutrient concentration
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926246/
https://www.ncbi.nlm.nih.gov/pubmed/36598949
http://dx.doi.org/10.1073/pnas.2207295120
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