Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis

Abstract Complex regulatory programs control cell adaptation to environmental changes by setting condition‐specific proteomes. In balanced growth, bacterial protein abundances depend on the dilution rate, transcript abundances and transcript‐specific translation efficiencies. We revisited the curren...

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Main Authors: Olivier Borkowski, Anne Goelzer, Marc Schaffer, Magali Calabre, Ulrike Mäder, Stéphane Aymerich, Matthieu Jules, Vincent Fromion
Format: Article
Language:English
Published: Springer Nature 2016-05-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20156608
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author Olivier Borkowski
Anne Goelzer
Marc Schaffer
Magali Calabre
Ulrike Mäder
Stéphane Aymerich
Matthieu Jules
Vincent Fromion
author_facet Olivier Borkowski
Anne Goelzer
Marc Schaffer
Magali Calabre
Ulrike Mäder
Stéphane Aymerich
Matthieu Jules
Vincent Fromion
author_sort Olivier Borkowski
collection DOAJ
description Abstract Complex regulatory programs control cell adaptation to environmental changes by setting condition‐specific proteomes. In balanced growth, bacterial protein abundances depend on the dilution rate, transcript abundances and transcript‐specific translation efficiencies. We revisited the current theory claiming the invariance of bacterial translation efficiency. By integrating genome‐wide transcriptome datasets and datasets from a library of synthetic gfp‐reporter fusions, we demonstrated that translation efficiencies in Bacillus subtilis decreased up to fourfold from slow to fast growth. The translation initiation regions elicited a growth rate‐dependent, differential production of proteins without regulators, hence revealing a unique, hard‐coded, growth rate‐dependent mode of regulation. We combined model‐based data analyses of transcript and protein abundances genome‐wide and revealed that this global regulation is extensively used in B. subtilis. We eventually developed a knowledge‐based, three‐step translation initiation model, experimentally challenged the model predictions and proposed that a growth rate‐dependent drop in free ribosome abundance accounted for the differential protein production.
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spelling doaj.art-d59fef70fd714eb08d535f88d57ba3c02024-04-02T19:10:38ZengSpringer NatureMolecular Systems Biology1744-42922016-05-01125n/an/a10.15252/msb.20156608Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilisOlivier Borkowski0Anne Goelzer1Marc Schaffer2Magali Calabre3Ulrike Mäder4Stéphane Aymerich5Matthieu Jules6Vincent Fromion7Micalis Institute INRA AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceMaIAGE INRA Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceInterfaculty Institute for Genetics and Functional Genomics University Medicine Greifswald Greifswald GermanyMicalis Institute INRA AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceInterfaculty Institute for Genetics and Functional Genomics University Medicine Greifswald Greifswald GermanyMicalis Institute INRA AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceMicalis Institute INRA AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceMaIAGE INRA Université Paris‐Saclay Jouy‐en‐Josas F78350 FranceAbstract Complex regulatory programs control cell adaptation to environmental changes by setting condition‐specific proteomes. In balanced growth, bacterial protein abundances depend on the dilution rate, transcript abundances and transcript‐specific translation efficiencies. We revisited the current theory claiming the invariance of bacterial translation efficiency. By integrating genome‐wide transcriptome datasets and datasets from a library of synthetic gfp‐reporter fusions, we demonstrated that translation efficiencies in Bacillus subtilis decreased up to fourfold from slow to fast growth. The translation initiation regions elicited a growth rate‐dependent, differential production of proteins without regulators, hence revealing a unique, hard‐coded, growth rate‐dependent mode of regulation. We combined model‐based data analyses of transcript and protein abundances genome‐wide and revealed that this global regulation is extensively used in B. subtilis. We eventually developed a knowledge‐based, three‐step translation initiation model, experimentally challenged the model predictions and proposed that a growth rate‐dependent drop in free ribosome abundance accounted for the differential protein production.https://doi.org/10.15252/msb.20156608Bacillus subtilisglobal regulationgrowth rateprotein productiontranslation efficiency
spellingShingle Olivier Borkowski
Anne Goelzer
Marc Schaffer
Magali Calabre
Ulrike Mäder
Stéphane Aymerich
Matthieu Jules
Vincent Fromion
Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
Molecular Systems Biology
Bacillus subtilis
global regulation
growth rate
protein production
translation efficiency
title Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
title_full Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
title_fullStr Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
title_full_unstemmed Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
title_short Translation elicits a growth rate‐dependent, genome‐wide, differential protein production in Bacillus subtilis
title_sort translation elicits a growth rate dependent genome wide differential protein production in bacillus subtilis
topic Bacillus subtilis
global regulation
growth rate
protein production
translation efficiency
url https://doi.org/10.15252/msb.20156608
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