Insertion sequence inversions mediated by ectopic recombination between terminal inverted repeats
Transposable elements are widely distributed and diverse in both eukaryotes and prokaryotes, as exemplified by DNA transposons. As a result, they represent a considerable source of genomic variation, for example through ectopic (i.e. non-allelic homologous) recombination events between transposable...
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Published in | PloS one Vol. 5; no. 12; p. e15654 |
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Language | English |
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20.12.2010
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Abstract | Transposable elements are widely distributed and diverse in both eukaryotes and prokaryotes, as exemplified by DNA transposons. As a result, they represent a considerable source of genomic variation, for example through ectopic (i.e. non-allelic homologous) recombination events between transposable element copies, resulting in genomic rearrangements. Ectopic recombination may also take place between homologous sequences located within transposable element sequences. DNA transposons are typically bounded by terminal inverted repeats (TIRs). Ectopic recombination between TIRs is expected to result in DNA transposon inversions. However, such inversions have barely been documented. In this study, we report natural inversions of the most common prokaryotic DNA transposons: insertion sequences (IS). We identified natural TIR-TIR recombination-mediated inversions in 9% of IS insertion loci investigated in Wolbachia bacteria, which suggests that recombination between IS TIRs may be a quite common, albeit largely overlooked, source of genomic diversity in bacteria. We suggest that inversions may impede IS survival and proliferation in the host genome by altering transpositional activity. They may also alter genomic instability by modulating the outcome of ectopic recombination events between IS copies in various orientations. This study represents the first report of TIR-TIR recombination within bacterial IS elements and it thereby uncovers a novel mechanism of structural variation for this class of prokaryotic transposable elements. |
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AbstractList | Transposable elements are widely distributed and diverse in both eukaryotes and prokaryotes, as exemplified by DNA transposons. As a result, they represent a considerable source of genomic variation, for example through ectopic (i.e. non-allelic homologous) recombination events between transposable element copies, resulting in genomic rearrangements. Ectopic recombination may also take place between homologous sequences located within transposable element sequences. DNA transposons are typically bounded by terminal inverted repeats (TIRs). Ectopic recombination between TIRs is expected to result in DNA transposon inversions. However, such inversions have barely been documented. In this study, we report natural inversions of the most common prokaryotic DNA transposons: insertion sequences (IS). We identified natural TIR-TIR recombination-mediated inversions in 9% of IS insertion loci investigated in Wolbachia bacteria, which suggests that recombination between IS TIRs may be a quite common, albeit largely overlooked, source of genomic diversity in bacteria. We suggest that inversions may impede IS survival and proliferation in the host genome by altering transpositional activity. They may also alter genomic instability by modulating the outcome of ectopic recombination events between IS copies in various orientations. This study represents the first report of TIR-TIR recombination within bacterial IS elements and it thereby uncovers a novel mechanism of structural variation for this class of prokaryotic transposable elements. Transposable elements are widely distributed and diverse in both eukaryotes and prokaryotes, as exemplified by DNA transposons. As a result, they represent a considerable source of genomic variation, for example through ectopic (i.e. non-allelic homologous) recombination events between transposable element copies, resulting in genomic rearrangements. Ectopic recombination may also take place between homologous sequences located within transposable element sequences. DNA transposons are typically bounded by terminal inverted repeats (TIRs). Ectopic recombination between TIRs is expected to result in DNA transposon inversions. However, such inversions have barely been documented. In this study, we report natural inversions of the most common prokaryotic DNA transposons: insertion sequences (IS). We identified natural TIR-TIR recombination-mediated inversions in 9% of IS insertion loci investigated in Wolbachia bacteria, which suggests that recombination between IS TIRs may be a quite common, albeit largely overlooked, source of genomic diversity in bacteria. We suggest that inversions may impede IS survival and proliferation in the host genome by altering transpositional activity. They may also alter genomic instability by modulating the outcome of ectopic recombination events between IS copies in various orientations. This study represents the first report of TIR-TIR recombination within bacterial IS elements and it thereby uncovers a novel mechanism of structural variation for this class of prokaryotic transposable elements. |
Audience | Academic |
Author | Cordaux, Richard Ling, Alison |
AuthorAffiliation | Louisiana State University, United States of America Université de Poitiers, CNRS UMR 6556 Ecologie, Evolution, Symbiose, Poitiers, France |
AuthorAffiliation_xml | – name: Université de Poitiers, CNRS UMR 6556 Ecologie, Evolution, Symbiose, Poitiers, France – name: Louisiana State University, United States of America |
Author_xml | – sequence: 1 givenname: Alison surname: Ling fullname: Ling, Alison organization: Université de Poitiers, CNRS UMR 6556 Ecologie, Evolution, Symbiose, Poitiers, France – sequence: 2 givenname: Richard surname: Cordaux fullname: Cordaux, Richard |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21187977$$D View this record in MEDLINE/PubMed https://hal.science/hal-00551569$$DView record in HAL |
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CitedBy_id | crossref_primary_10_1016_j_chom_2021_03_006 crossref_primary_10_1038_s41598_017_13808_z crossref_primary_10_1111_mec_15907 crossref_primary_10_3390_insects15050312 crossref_primary_10_1016_j_meegid_2016_08_030 crossref_primary_10_1016_j_jksuci_2021_11_012 crossref_primary_10_1128_JB_00783_12 |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2010 Public Library of Science 2010 Ling, Cordaux. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Distributed under a Creative Commons Attribution 4.0 International License Ling, Cordaux. 2010 |
Copyright_xml | – notice: COPYRIGHT 2010 Public Library of Science – notice: 2010 Ling, Cordaux. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Distributed under a Creative Commons Attribution 4.0 International License – notice: Ling, Cordaux. 2010 |
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Notes | PMCID: PMC3004938 Conceived and designed the experiments: RC. Analyzed the data: AL RC. Contributed reagents/materials/analysis tools: RC. Wrote the paper: RC. |
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SubjectTerms | Bacteria Base Sequence Biodiversity and Ecology Biology Bordetella Bordetella bronchiseptica Bordetella pertussis Chromosome Inversion Culex pipiens Deoxyribonucleic acid DNA DNA - genetics DNA Transposable Elements Drosophila simulans Environmental Sciences Eukaryotes Evolution Gene sequencing Genome Genomes Genomic Instability Genomics Homologous recombination Homology Insects Insertion Insertion sequences Inversions Molecular Sequence Data Nucleotide sequence Phylogeny Prokaryotes Promoter Regions, Genetic Recombination, Genetic Sequence Homology, Nucleic Acid Sequence Inversion Shigella Stability Terminal Repeat Sequences Transposons Trends Whooping cough Wolbachia Wolbachia - genetics |
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Title | Insertion sequence inversions mediated by ectopic recombination between terminal inverted repeats |
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