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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Nature Portfolio
2021
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oai:doaj.org-article:e12831b700494fe4a6382dd00152f3d62021-12-02T13:30:12ZOptimal proteome allocation and the temperature dependence of microbial growth laws10.1038/s41540-021-00172-y2056-7189https://doaj.org/article/e12831b700494fe4a6382dd00152f3d62021-03-01T00:00:00Zhttps://doi.org/10.1038/s41540-021-00172-yhttps://doaj.org/toc/2056-7189Abstract 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.Francis MairetJean-Luc GouzéHidde de JongNature PortfolioarticleBiology (General)QH301-705.5ENnpj Systems Biology and Applications, Vol 7, Iss 1, Pp 1-11 (2021) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Francis Mairet Jean-Luc Gouzé Hidde de Jong Optimal proteome allocation and the temperature dependence of microbial growth laws |
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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. |
format |
article |
author |
Francis Mairet Jean-Luc Gouzé Hidde de Jong |
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 Portfolio |
publishDate |
2021 |
url |
https://doaj.org/article/e12831b700494fe4a6382dd00152f3d6 |
work_keys_str_mv |
AT francismairet optimalproteomeallocationandthetemperaturedependenceofmicrobialgrowthlaws AT jeanlucgouze optimalproteomeallocationandthetemperaturedependenceofmicrobialgrowthlaws AT hiddedejong optimalproteomeallocationandthetemperaturedependenceofmicrobialgrowthlaws |
_version_ |
1718392946758254592 |