Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness

ABSTRACT Despite our extensive knowledge of the genetic regulation of heat shock proteins (HSPs), the evolutionary routes that allow bacteria to adaptively tune their HSP levels and corresponding proteostatic robustness have been explored less. In this report, directed evolution experiments using th...

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Autores principales: Julien Mortier, Elisa Gayán, Ronald Van Eyken, Oscar Enrique Torres Montaguth, Ladan Khodaparast, Laleh Khodaparast, Bert Houben, Sebastien Carpentier, Frederic Rousseau, Joost Schymkowitz, Abram Aertsen
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:623a01e2ab7646c0bffe2fbedf4775872021-11-10T18:37:50ZGene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness10.1128/mBio.01129-212150-7511https://doaj.org/article/623a01e2ab7646c0bffe2fbedf4775872021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01129-21https://doaj.org/toc/2150-7511ABSTRACT Despite our extensive knowledge of the genetic regulation of heat shock proteins (HSPs), the evolutionary routes that allow bacteria to adaptively tune their HSP levels and corresponding proteostatic robustness have been explored less. In this report, directed evolution experiments using the Escherichia coli model system unexpectedly revealed that seemingly random single mutations in its tnaA gene can confer significant heat resistance. Closer examination, however, indicated that these mutations create folding-deficient and aggregation-prone TnaA variants that in turn can endogenously and preemptively trigger HSP expression to cause heat resistance. These findings, importantly, demonstrate that even erosive mutations with disruptive effects on protein structure and functionality can still yield true gain-of-function alleles with a selective advantage in adaptive evolution.Julien MortierElisa GayánRonald Van EykenOscar Enrique Torres MontaguthLadan KhodaparastLaleh KhodaparastBert HoubenSebastien CarpentierFrederic RousseauJoost SchymkowitzAbram AertsenAmerican Society for Microbiologyarticleevolutiongeneticsheat resistanceprotein aggregatesMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution DOAJ
collection DOAJ
language EN
topic evolution
genetics
heat resistance
protein aggregates
Microbiology
QR1-502
spellingShingle evolution
genetics
heat resistance
protein aggregates
Microbiology
QR1-502
Julien Mortier
Elisa Gayán
Ronald Van Eyken
Oscar Enrique Torres Montaguth
Ladan Khodaparast
Laleh Khodaparast
Bert Houben
Sebastien Carpentier
Frederic Rousseau
Joost Schymkowitz
Abram Aertsen
Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
description ABSTRACT Despite our extensive knowledge of the genetic regulation of heat shock proteins (HSPs), the evolutionary routes that allow bacteria to adaptively tune their HSP levels and corresponding proteostatic robustness have been explored less. In this report, directed evolution experiments using the Escherichia coli model system unexpectedly revealed that seemingly random single mutations in its tnaA gene can confer significant heat resistance. Closer examination, however, indicated that these mutations create folding-deficient and aggregation-prone TnaA variants that in turn can endogenously and preemptively trigger HSP expression to cause heat resistance. These findings, importantly, demonstrate that even erosive mutations with disruptive effects on protein structure and functionality can still yield true gain-of-function alleles with a selective advantage in adaptive evolution.
format article
author Julien Mortier
Elisa Gayán
Ronald Van Eyken
Oscar Enrique Torres Montaguth
Ladan Khodaparast
Laleh Khodaparast
Bert Houben
Sebastien Carpentier
Frederic Rousseau
Joost Schymkowitz
Abram Aertsen
author_facet Julien Mortier
Elisa Gayán
Ronald Van Eyken
Oscar Enrique Torres Montaguth
Ladan Khodaparast
Laleh Khodaparast
Bert Houben
Sebastien Carpentier
Frederic Rousseau
Joost Schymkowitz
Abram Aertsen
author_sort Julien Mortier
title Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
title_short Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
title_full Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
title_fullStr Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
title_full_unstemmed Gene Erosion Can Lead to Gain-of-Function Alleles That Contribute to Bacterial Fitness
title_sort gene erosion can lead to gain-of-function alleles that contribute to bacterial fitness
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/623a01e2ab7646c0bffe2fbedf477587
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