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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2014-10-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01377-14 |
| _version_ | 1818856648651833344 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-19T08:27:51Z |
| format | Article |
| id | doaj.art-2a201841c2b941a29ebff170347644bf |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T08:27:51Z |
| publishDate | 2014-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-2a201841c2b941a29ebff170347644bf2022-12-21T20:29:16ZengAmerican Society for MicrobiologymBio2150-75112014-10-015510.1128/mBio.01377-14Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with <named-content content-type="genus-species">Escherichia coli</named-content>Colin Raeside0Joël Gaffé1Daniel E. Deatherage2Olivier Tenaillon3Adam M. Briska4Ryan N. Ptashkin5Stéphane Cruveiller6Claudine Médigue7Richard E. Lenski8Jeffrey E. Barrick9Dominique Schneider10Univ. Grenoble Alpes, Laboratoire Adaptation et Pathogénie des Microorganismes (LAPM), Grenoble, FranceUniv. Grenoble Alpes, Laboratoire Adaptation et Pathogénie des Microorganismes (LAPM), Grenoble, FranceDepartment of Molecular Biosciences, Institute for Cellular and Molecular Biology, Center for Systems and Synthetic Biology, The University of Texas at Austin, Austin, Texas, USAIAME, UMR 1137, INSERM, Paris, FranceOpGen, Inc., Gaithersburg, Maryland, USAOpGen, Inc., Gaithersburg, Maryland, USADirection des Sciences du Vivant, Commissariat à l’energie atomique et aux Energies Alternatives (CEA), Institut de Génomique, Genoscope & CNRS-UMR8030, Évry, FranceDirection des Sciences du Vivant, Commissariat à l’energie atomique et aux Energies Alternatives (CEA), Institut de Génomique, Genoscope & CNRS-UMR8030, Évry, FranceDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USADepartment of Molecular Biosciences, Institute for Cellular and Molecular Biology, Center for Systems and Synthetic Biology, The University of Texas at Austin, Austin, Texas, USAUniv. Grenoble Alpes, Laboratoire Adaptation et Pathogénie des Microorganismes (LAPM), Grenoble, FranceABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.01377-14 |
| spellingShingle | 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> mBio |
| title | 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_short | 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 |
| url | https://journals.asm.org/doi/10.1128/mBio.01377-14 |
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