Optimal proteome allocation and the temperature dependence of microbial growth laws

Abstract Although the effect of temperature on microbial growth has been widely studied, the role of proteome allocation in bringing about temperature-induced changes remains elusive. To tackle this problem, we propose a coarse-grained model of microbial growth, including the processes of temperatur...

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Main Authors: Francis Mairet, Jean-Luc Gouzé, Hidde de Jong
Format: Article
Language:English
Published: Nature Publishing Group 2021-03-01
Series:npj Systems Biology and Applications
Online Access:https://doi.org/10.1038/s41540-021-00172-y
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spelling doaj-e12831b700494fe4a6382dd00152f3d62021-03-11T12:46:09ZengNature Publishing Groupnpj Systems Biology and Applications2056-71892021-03-017111110.1038/s41540-021-00172-yOptimal proteome allocation and the temperature dependence of microbial growth lawsFrancis Mairet0Jean-Luc Gouzé1Hidde de Jong2Ifremer, Physiology and Biotechnology of Algae laboratoryUniversité Côte d’Azur, Inria, INRAE, CNRS, Sorbonne Université, Biocore teamUniversité Grenoble Alpes, InriaAbstract Although the effect of temperature on microbial growth has been widely studied, the role of proteome allocation in bringing about temperature-induced changes remains elusive. To tackle this problem, we propose a coarse-grained model of microbial growth, including the processes of temperature-sensitive protein unfolding and chaperone-assisted (re)folding. We determine the proteome sector allocation that maximizes balanced growth rate as a function of nutrient limitation and temperature. Calibrated with quantitative proteomic data for Escherichia coli, the model allows us to clarify general principles of temperature-dependent proteome allocation and formulate generalized growth laws. The same activation energy for metabolic enzymes and ribosomes leads to an Arrhenius increase in growth rate at constant proteome composition over a large range of temperatures, whereas at extreme temperatures resources are diverted away from growth to chaperone-mediated stress responses. Our approach points at risks and possible remedies for the use of ribosome content to characterize complex ecosystems with temperature variation.https://doi.org/10.1038/s41540-021-00172-y
collection DOAJ
language English
format Article
sources DOAJ
author Francis Mairet
Jean-Luc Gouzé
Hidde de Jong
spellingShingle Francis Mairet
Jean-Luc Gouzé
Hidde de Jong
Optimal proteome allocation and the temperature dependence of microbial growth laws
npj Systems Biology and Applications
author_facet Francis Mairet
Jean-Luc Gouzé
Hidde de Jong
author_sort Francis Mairet
title Optimal proteome allocation and the temperature dependence of microbial growth laws
title_short Optimal proteome allocation and the temperature dependence of microbial growth laws
title_full Optimal proteome allocation and the temperature dependence of microbial growth laws
title_fullStr Optimal proteome allocation and the temperature dependence of microbial growth laws
title_full_unstemmed Optimal proteome allocation and the temperature dependence of microbial growth laws
title_sort optimal proteome allocation and the temperature dependence of microbial growth laws
publisher Nature Publishing Group
series npj Systems Biology and Applications
issn 2056-7189
publishDate 2021-03-01
description Abstract Although the effect of temperature on microbial growth has been widely studied, the role of proteome allocation in bringing about temperature-induced changes remains elusive. To tackle this problem, we propose a coarse-grained model of microbial growth, including the processes of temperature-sensitive protein unfolding and chaperone-assisted (re)folding. We determine the proteome sector allocation that maximizes balanced growth rate as a function of nutrient limitation and temperature. Calibrated with quantitative proteomic data for Escherichia coli, the model allows us to clarify general principles of temperature-dependent proteome allocation and formulate generalized growth laws. The same activation energy for metabolic enzymes and ribosomes leads to an Arrhenius increase in growth rate at constant proteome composition over a large range of temperatures, whereas at extreme temperatures resources are diverted away from growth to chaperone-mediated stress responses. Our approach points at risks and possible remedies for the use of ribosome content to characterize complex ecosystems with temperature variation.
url https://doi.org/10.1038/s41540-021-00172-y
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