Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains

Different strains of a microorganism growing in the same environment display a wide variety of growth rates and growth yields. We developed a coarse-grained model to test the hypothesis that different resource allocation strategies, corresponding to different compositions of the proteome, can accoun...

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Main Authors: Valentina Baldazzi, Delphine Ropers, Jean-Luc Gouzé, Tomas Gedeon, Hidde de Jong
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/79815
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author Valentina Baldazzi
Delphine Ropers
Jean-Luc Gouzé
Tomas Gedeon
Hidde de Jong
author_facet Valentina Baldazzi
Delphine Ropers
Jean-Luc Gouzé
Tomas Gedeon
Hidde de Jong
author_sort Valentina Baldazzi
collection DOAJ
description Different strains of a microorganism growing in the same environment display a wide variety of growth rates and growth yields. We developed a coarse-grained model to test the hypothesis that different resource allocation strategies, corresponding to different compositions of the proteome, can account for the observed rate-yield variability. The model predictions were verified by means of a database of hundreds of published rate-yield and uptake-secretion phenotypes of Escherichia coli strains grown in standard laboratory conditions. We found a very good quantitative agreement between the range of predicted and observed growth rates, growth yields, and glucose uptake and acetate secretion rates. These results support the hypothesis that resource allocation is a major explanatory factor of the observed variability of growth rates and growth yields across different bacterial strains. An interesting prediction of our model, supported by the experimental data, is that high growth rates are not necessarily accompanied by low growth yields. The resource allocation strategies enabling high-rate, high-yield growth of E. coli lead to a higher saturation of enzymes and ribosomes, and thus to a more efficient utilization of proteomic resources. Our model thus contributes to a fundamental understanding of the quantitative relationship between rate and yield in E. coli and other microorganisms. It may also be useful for the rapid screening of strains in metabolic engineering and synthetic biology.
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spelling doaj.art-e866ecd2e5444415b5d4b9a187062e8a2023-06-15T13:55:36ZengeLife Sciences Publications LtdeLife2050-084X2023-05-011210.7554/eLife.79815Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strainsValentina Baldazzi0https://orcid.org/0000-0001-9734-9759Delphine Ropers1https://orcid.org/0000-0003-2659-3003Jean-Luc Gouzé2Tomas Gedeon3Hidde de Jong4https://orcid.org/0000-0002-2226-650XUniversité Côte d’Azur, Inria, INRAE, CNRS, Sorbonne Université, Sophia Antipolis, France; Université Côte d’Azur, INRAE, CNRS, Institut Sophia-Agrobiotech, Sophia Antipolis, FranceUniversité Grenoble Alpes, Inria, Grenoble, FranceUniversité Côte d’Azur, Inria, INRAE, CNRS, Sorbonne Université, Sophia Antipolis, FranceMontana State University, Bozeman, United StatesUniversité Grenoble Alpes, Inria, Grenoble, FranceDifferent strains of a microorganism growing in the same environment display a wide variety of growth rates and growth yields. We developed a coarse-grained model to test the hypothesis that different resource allocation strategies, corresponding to different compositions of the proteome, can account for the observed rate-yield variability. The model predictions were verified by means of a database of hundreds of published rate-yield and uptake-secretion phenotypes of Escherichia coli strains grown in standard laboratory conditions. We found a very good quantitative agreement between the range of predicted and observed growth rates, growth yields, and glucose uptake and acetate secretion rates. These results support the hypothesis that resource allocation is a major explanatory factor of the observed variability of growth rates and growth yields across different bacterial strains. An interesting prediction of our model, supported by the experimental data, is that high growth rates are not necessarily accompanied by low growth yields. The resource allocation strategies enabling high-rate, high-yield growth of E. coli lead to a higher saturation of enzymes and ribosomes, and thus to a more efficient utilization of proteomic resources. Our model thus contributes to a fundamental understanding of the quantitative relationship between rate and yield in E. coli and other microorganisms. It may also be useful for the rapid screening of strains in metabolic engineering and synthetic biology.https://elifesciences.org/articles/79815resource allocationgrowth rategrowth yieldbacterial physiologymetabolic regulationEscherichia coli
spellingShingle Valentina Baldazzi
Delphine Ropers
Jean-Luc Gouzé
Tomas Gedeon
Hidde de Jong
Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
eLife
resource allocation
growth rate
growth yield
bacterial physiology
metabolic regulation
Escherichia coli
title Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
title_full Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
title_fullStr Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
title_full_unstemmed Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
title_short Resource allocation accounts for the large variability of rate-yield phenotypes across bacterial strains
title_sort resource allocation accounts for the large variability of rate yield phenotypes across bacterial strains
topic resource allocation
growth rate
growth yield
bacterial physiology
metabolic regulation
Escherichia coli
url https://elifesciences.org/articles/79815
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AT jeanlucgouze resourceallocationaccountsforthelargevariabilityofrateyieldphenotypesacrossbacterialstrains
AT tomasgedeon resourceallocationaccountsforthelargevariabilityofrateyieldphenotypesacrossbacterialstrains
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