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Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair

By directed evolution in the laboratory, we previously generated populations of Escherichia coli that exhibit a complex new phenotype, extreme resistance to ionizing radiation (IR). The molecular basis of this extremophile phenotype, involving strain isolates with a 3-4 order of magnitude increase i...

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Autores principales: Byrne, Rose T, Klingele, Audrey J, Cabot, Eric L, Schackwitz, Wendy S, Martin, Jeffrey A, Martin, Joel, Wang, Zhong, Wood, Elizabeth A, Pennacchio, Christa, Pennacchio, Len A, Perna, Nicole T, Battista, John R, Cox, Michael M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3939492/
https://www.ncbi.nlm.nih.gov/pubmed/24596148
http://dx.doi.org/10.7554/eLife.01322
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author Byrne, Rose T
Klingele, Audrey J
Cabot, Eric L
Schackwitz, Wendy S
Martin, Jeffrey A
Martin, Joel
Wang, Zhong
Wood, Elizabeth A
Pennacchio, Christa
Pennacchio, Len A
Perna, Nicole T
Battista, John R
Cox, Michael M
author_facet Byrne, Rose T
Klingele, Audrey J
Cabot, Eric L
Schackwitz, Wendy S
Martin, Jeffrey A
Martin, Joel
Wang, Zhong
Wood, Elizabeth A
Pennacchio, Christa
Pennacchio, Len A
Perna, Nicole T
Battista, John R
Cox, Michael M
author_sort Byrne, Rose T
collection PubMed
description By directed evolution in the laboratory, we previously generated populations of Escherichia coli that exhibit a complex new phenotype, extreme resistance to ionizing radiation (IR). The molecular basis of this extremophile phenotype, involving strain isolates with a 3-4 order of magnitude increase in IR resistance at 3000 Gy, is now addressed. Of 69 mutations identified in one of our most highly adapted isolates, functional experiments demonstrate that the IR resistance phenotype is almost entirely accounted for by only three of these nucleotide changes, in the DNA metabolism genes recA, dnaB, and yfjK. Four additional genetic changes make small but measurable contributions. Whereas multiple contributions to IR resistance are evident in this study, our results highlight a particular adaptation mechanism not adequately considered in studies to date: Genetic innovations involving pre-existing DNA repair functions can play a predominant role in the acquisition of an IR resistance phenotype. DOI: http://dx.doi.org/10.7554/eLife.01322.001
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spelling pubmed-39394922014-03-06 Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair Byrne, Rose T Klingele, Audrey J Cabot, Eric L Schackwitz, Wendy S Martin, Jeffrey A Martin, Joel Wang, Zhong Wood, Elizabeth A Pennacchio, Christa Pennacchio, Len A Perna, Nicole T Battista, John R Cox, Michael M eLife Genes and Chromosomes By directed evolution in the laboratory, we previously generated populations of Escherichia coli that exhibit a complex new phenotype, extreme resistance to ionizing radiation (IR). The molecular basis of this extremophile phenotype, involving strain isolates with a 3-4 order of magnitude increase in IR resistance at 3000 Gy, is now addressed. Of 69 mutations identified in one of our most highly adapted isolates, functional experiments demonstrate that the IR resistance phenotype is almost entirely accounted for by only three of these nucleotide changes, in the DNA metabolism genes recA, dnaB, and yfjK. Four additional genetic changes make small but measurable contributions. Whereas multiple contributions to IR resistance are evident in this study, our results highlight a particular adaptation mechanism not adequately considered in studies to date: Genetic innovations involving pre-existing DNA repair functions can play a predominant role in the acquisition of an IR resistance phenotype. DOI: http://dx.doi.org/10.7554/eLife.01322.001 eLife Sciences Publications, Ltd 2014-03-04 /pmc/articles/PMC3939492/ /pubmed/24596148 http://dx.doi.org/10.7554/eLife.01322 Text en http://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (http://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Genes and Chromosomes
Byrne, Rose T
Klingele, Audrey J
Cabot, Eric L
Schackwitz, Wendy S
Martin, Jeffrey A
Martin, Joel
Wang, Zhong
Wood, Elizabeth A
Pennacchio, Christa
Pennacchio, Len A
Perna, Nicole T
Battista, John R
Cox, Michael M
Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title_full Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title_fullStr Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title_full_unstemmed Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title_short Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair
title_sort evolution of extreme resistance to ionizing radiation via genetic adaptation of dna repair
topic Genes and Chromosomes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3939492/
https://www.ncbi.nlm.nih.gov/pubmed/24596148
http://dx.doi.org/10.7554/eLife.01322
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