Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve Escherichia coli populations have been propagated in a glucose-limited enviro...

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Autores principales:	Colin Raeside, Joël Gaffé, Daniel E. Deatherage, Olivier Tenaillon, Adam M. Briska, Ryan N. Ptashkin, Stéphane Cruveiller, Claudine Médigue, Richard E. Lenski, Jeffrey E. Barrick, Dominique Schneider
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Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
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spelling	oai:doaj.org-article:2a201841c2b941a29ebff170347644bf2021-11-15T15:45:54ZLarge Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.01377-142150-7511https://doaj.org/article/2a201841c2b941a29ebff170347644bf2014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01377-14https://doaj.org/toc/2150-7511ABSTRACT Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve Escherichia coli populations have been propagated in a glucose-limited environment for over 25 years. We used whole-genome mapping (optical mapping) combined with genome sequencing and PCR analysis to identify the large-scale chromosomal rearrangements in clones from each population after 40,000 generations. A total of 110 rearrangement events were detected, including 82 deletions, 19 inversions, and 9 duplications, with lineages having between 5 and 20 events. In three populations, successive rearrangements impacted particular regions. In five populations, rearrangements affected over a third of the chromosome. Most rearrangements involved recombination between insertion sequence (IS) elements, illustrating their importance in mediating genome plasticity. Two lines of evidence suggest that at least some of these rearrangements conferred higher fitness. First, parallel changes were observed across the independent populations, with ~65% of the rearrangements affecting the same loci in at least two populations. For example, the ribose-utilization operon and the manB-cpsG region were deleted in 12 and 10 populations, respectively, suggesting positive selection, and this inference was previously confirmed for the former case. Second, optical maps from clones sampled over time from one population showed that most rearrangements occurred early in the experiment, when fitness was increasing most rapidly. However, some rearrangements likely occur at high frequency and may have simply hitchhiked to fixation. In any case, large-scale rearrangements clearly influenced genomic evolution in these populations. IMPORTANCE Bacterial chromosomes are dynamic structures shaped by long histories of evolution. Among genomic changes, large-scale DNA rearrangements can have important effects on the presence, order, and expression of genes. Whole-genome sequencing that relies on short DNA reads cannot identify all large-scale rearrangements. Therefore, deciphering changes in the overall organization of genomes requires alternative methods, such as optical mapping. We analyzed the longest-running microbial evolution experiment (more than 25 years of evolution in the laboratory) by optical mapping, genome sequencing, and PCR analyses. We found multiple large genome rearrangements in all 12 independently evolving populations. In most cases, it is unclear whether these changes were beneficial themselves or, alternatively, hitchhiked to fixation with other beneficial mutations. In any case, many genome rearrangements accumulated over decades of evolution, providing these populations with genetic plasticity reminiscent of that observed in some pathogenic bacteria.Colin RaesideJoël GafféDaniel E. DeatherageOlivier TenaillonAdam M. BriskaRyan N. PtashkinStéphane CruveillerClaudine MédigueRichard E. LenskiJeffrey E. BarrickDominique SchneiderAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Colin Raeside Joël Gaffé Daniel E. Deatherage Olivier Tenaillon Adam M. Briska Ryan N. Ptashkin Stéphane Cruveiller Claudine Médigue Richard E. Lenski Jeffrey E. Barrick Dominique Schneider Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve Escherichia coli populations have been propagated in a glucose-limited environment for over 25 years. We used whole-genome mapping (optical mapping) combined with genome sequencing and PCR analysis to identify the large-scale chromosomal rearrangements in clones from each population after 40,000 generations. A total of 110 rearrangement events were detected, including 82 deletions, 19 inversions, and 9 duplications, with lineages having between 5 and 20 events. In three populations, successive rearrangements impacted particular regions. In five populations, rearrangements affected over a third of the chromosome. Most rearrangements involved recombination between insertion sequence (IS) elements, illustrating their importance in mediating genome plasticity. Two lines of evidence suggest that at least some of these rearrangements conferred higher fitness. First, parallel changes were observed across the independent populations, with ~65% of the rearrangements affecting the same loci in at least two populations. For example, the ribose-utilization operon and the manB-cpsG region were deleted in 12 and 10 populations, respectively, suggesting positive selection, and this inference was previously confirmed for the former case. Second, optical maps from clones sampled over time from one population showed that most rearrangements occurred early in the experiment, when fitness was increasing most rapidly. However, some rearrangements likely occur at high frequency and may have simply hitchhiked to fixation. In any case, large-scale rearrangements clearly influenced genomic evolution in these populations. IMPORTANCE Bacterial chromosomes are dynamic structures shaped by long histories of evolution. Among genomic changes, large-scale DNA rearrangements can have important effects on the presence, order, and expression of genes. Whole-genome sequencing that relies on short DNA reads cannot identify all large-scale rearrangements. Therefore, deciphering changes in the overall organization of genomes requires alternative methods, such as optical mapping. We analyzed the longest-running microbial evolution experiment (more than 25 years of evolution in the laboratory) by optical mapping, genome sequencing, and PCR analyses. We found multiple large genome rearrangements in all 12 independently evolving populations. In most cases, it is unclear whether these changes were beneficial themselves or, alternatively, hitchhiked to fixation with other beneficial mutations. In any case, many genome rearrangements accumulated over decades of evolution, providing these populations with genetic plasticity reminiscent of that observed in some pathogenic bacteria.
format	article
author	Colin Raeside Joël Gaffé Daniel E. Deatherage Olivier Tenaillon Adam M. Briska Ryan N. Ptashkin Stéphane Cruveiller Claudine Médigue Richard E. Lenski Jeffrey E. Barrick Dominique Schneider
author_facet	Colin Raeside Joël Gaffé Daniel E. Deatherage Olivier Tenaillon Adam M. Briska Ryan N. Ptashkin Stéphane Cruveiller Claudine Médigue Richard E. Lenski Jeffrey E. Barrick Dominique Schneider
author_sort	Colin Raeside
title	Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	large chromosomal rearrangements during a long-term evolution experiment with <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/2a201841c2b941a29ebff170347644bf
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Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>

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