The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification

ABSTRACT More than a century ago, Theodor Escherich isolated the bacterium that was to become Escherichia coli, one of the most studied organisms. Not long after, the strain began an odyssey and landed in many laboratories across the world. As laboratory culture conditions could be responsible for m...

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Autores principales:	M. Desroches, G. Royer, D. Roche, M. Mercier-Darty, D. Vallenet, C. Médigue, K. Bastard, C. Rodriguez, O. Clermont, E. Denamur, J.-W. Decousser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Escherichia coli SPANC tradeoff antibiotic hypersusceptibility collections mutator Microbiology QR1-502
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spelling	oai:doaj.org-article:a8e0664b07a94ab79625eec3449315522021-11-15T15:22:01ZThe Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification10.1128/mSphere.00553-172379-5042https://doaj.org/article/a8e0664b07a94ab79625eec3449315522018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00553-17https://doaj.org/toc/2379-5042ABSTRACT More than a century ago, Theodor Escherich isolated the bacterium that was to become Escherichia coli, one of the most studied organisms. Not long after, the strain began an odyssey and landed in many laboratories across the world. As laboratory culture conditions could be responsible for major changes in bacterial strains, we conducted a genome analysis of isolates of this emblematic strain from different culture collections (England, France, the United States, Germany). Strikingly, many discrepancies between the isolates were observed, as revealed by multilocus sequence typing (MLST), the presence of virulence-associated genes, core genome MLST, and single nucleotide polymorphism/indel analyses. These differences are correlated with the phylogeographic history of the strain and were due to an unprecedented number of mutations in coding DNA repair functions such as mismatch repair (MutL) and oxidized guanine nucleotide pool cleaning (MutT), conferring a specific mutational spectrum and leading to a mutator phenotype. The mutator phenotype was probably acquired during subculturing and corresponded to second-order selection. Furthermore, all of the isolates exhibited hypersusceptibility to antibiotics due to mutations in efflux pump- and porin-encoding genes, as well as a specific mutation in the sigma factor-encoding gene rpoS. These defects reflect a self-preservation and nutritional competence tradeoff allowing survival under the starvation conditions imposed by storage. From a clinical point of view, dealing with such mutator strains can lead microbiologists to draw false conclusions about isolate relatedness and may impact therapeutic effectiveness. IMPORTANCE Mutator phenotypes have been described in laboratory-evolved bacteria, as well as in natural isolates. Several genes can be impacted, each of them being associated with a typical mutational spectrum. By studying one of the oldest strains available, the ancestral Escherich strain, we were able to identify its mutator status leading to tremendous genetic diversity among the isolates from various collections and allowing us to reconstruct the phylogeographic history of the strain. This mutator phenotype was probably acquired during the storage of the strain, promoting adaptation to a specific environment. Other mutations in rpoS and efflux pump- and porin-encoding genes highlight the acclimatization of the strain through self-preservation and nutritional competence regulation. This strain history can be viewed as unintentional experimental evolution in culture collections all over the word since 1885, mimicking the long-term experimental evolution of E. coli of Lenski et al. (O. Tenaillon, J. E. Barrick, N. Ribeck, D. E. Deatherage, J. L. Blanchard, A. Dasgupta, G. C. Wu, S. Wielgoss, S. Cruveiller, C. Médigue, D. Schneider, and R. E. Lenski, Nature 536:165–170, 2016, https://doi.org/10.1038/nature18959) that shares numerous molecular features.M. DesrochesG. RoyerD. RocheM. Mercier-DartyD. VallenetC. MédigueK. BastardC. RodriguezO. ClermontE. DenamurJ.-W. DecousserAmerican Society for MicrobiologyarticleEscherichia coliSPANC tradeoffantibiotic hypersusceptibilitycollectionsmutatorMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli SPANC tradeoff antibiotic hypersusceptibility collections mutator Microbiology QR1-502
spellingShingle	Escherichia coli SPANC tradeoff antibiotic hypersusceptibility collections mutator Microbiology QR1-502 M. Desroches G. Royer D. Roche M. Mercier-Darty D. Vallenet C. Médigue K. Bastard C. Rodriguez O. Clermont E. Denamur J.-W. Decousser The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
description	ABSTRACT More than a century ago, Theodor Escherich isolated the bacterium that was to become Escherichia coli, one of the most studied organisms. Not long after, the strain began an odyssey and landed in many laboratories across the world. As laboratory culture conditions could be responsible for major changes in bacterial strains, we conducted a genome analysis of isolates of this emblematic strain from different culture collections (England, France, the United States, Germany). Strikingly, many discrepancies between the isolates were observed, as revealed by multilocus sequence typing (MLST), the presence of virulence-associated genes, core genome MLST, and single nucleotide polymorphism/indel analyses. These differences are correlated with the phylogeographic history of the strain and were due to an unprecedented number of mutations in coding DNA repair functions such as mismatch repair (MutL) and oxidized guanine nucleotide pool cleaning (MutT), conferring a specific mutational spectrum and leading to a mutator phenotype. The mutator phenotype was probably acquired during subculturing and corresponded to second-order selection. Furthermore, all of the isolates exhibited hypersusceptibility to antibiotics due to mutations in efflux pump- and porin-encoding genes, as well as a specific mutation in the sigma factor-encoding gene rpoS. These defects reflect a self-preservation and nutritional competence tradeoff allowing survival under the starvation conditions imposed by storage. From a clinical point of view, dealing with such mutator strains can lead microbiologists to draw false conclusions about isolate relatedness and may impact therapeutic effectiveness. IMPORTANCE Mutator phenotypes have been described in laboratory-evolved bacteria, as well as in natural isolates. Several genes can be impacted, each of them being associated with a typical mutational spectrum. By studying one of the oldest strains available, the ancestral Escherich strain, we were able to identify its mutator status leading to tremendous genetic diversity among the isolates from various collections and allowing us to reconstruct the phylogeographic history of the strain. This mutator phenotype was probably acquired during the storage of the strain, promoting adaptation to a specific environment. Other mutations in rpoS and efflux pump- and porin-encoding genes highlight the acclimatization of the strain through self-preservation and nutritional competence regulation. This strain history can be viewed as unintentional experimental evolution in culture collections all over the word since 1885, mimicking the long-term experimental evolution of E. coli of Lenski et al. (O. Tenaillon, J. E. Barrick, N. Ribeck, D. E. Deatherage, J. L. Blanchard, A. Dasgupta, G. C. Wu, S. Wielgoss, S. Cruveiller, C. Médigue, D. Schneider, and R. E. Lenski, Nature 536:165–170, 2016, https://doi.org/10.1038/nature18959) that shares numerous molecular features.
format	article
author	M. Desroches G. Royer D. Roche M. Mercier-Darty D. Vallenet C. Médigue K. Bastard C. Rodriguez O. Clermont E. Denamur J.-W. Decousser
author_facet	M. Desroches G. Royer D. Roche M. Mercier-Darty D. Vallenet C. Médigue K. Bastard C. Rodriguez O. Clermont E. Denamur J.-W. Decousser
author_sort	M. Desroches
title	The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
title_short	The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
title_full	The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
title_fullStr	The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
title_full_unstemmed	The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification
title_sort	odyssey of the ancestral escherich strain through culture collections: an example of allopatric diversification
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/a8e0664b07a94ab79625eec344931552
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The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification

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