Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate.
The capture of antimicrobial resistance genes (ARGs) by mobile genetic elements (MGEs) plays a critical role in resistance acquisition for human-associated bacteria. Although aquaculture environments are recognized as important reservoirs of ARGs, intra- and intercellular mobility of MGEs discovered...
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| _version_ | 1849766420180631552 |
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| author | Lisa Nonaka Tatsuya Yamamoto Fumito Maruyama Yuu Hirose Yuki Onishi Takeshi Kobayashi Satoru Suzuki Nobuhiko Nomura Michiaki Masuda Hirokazu Yano |
| author_facet | Lisa Nonaka Tatsuya Yamamoto Fumito Maruyama Yuu Hirose Yuki Onishi Takeshi Kobayashi Satoru Suzuki Nobuhiko Nomura Michiaki Masuda Hirokazu Yano |
| author_sort | Lisa Nonaka |
| collection | DOAJ |
| description | The capture of antimicrobial resistance genes (ARGs) by mobile genetic elements (MGEs) plays a critical role in resistance acquisition for human-associated bacteria. Although aquaculture environments are recognized as important reservoirs of ARGs, intra- and intercellular mobility of MGEs discovered in marine organisms is poorly characterized. Here, we show a new pattern of interspecies ARGs transfer involving a 'non-conjugative' integrative element. To identify active MGEs in a Vibrio ponticus isolate, we conducted whole-genome sequencing of a transconjugant obtained by mating between Escherichia coli and Vibrio ponticus. This revealed integration of a plasmid (designated pSEA1) into the chromosome, consisting of a self-transmissible plasmid backbone of the MOBH group, ARGs, and a 13.8-kb integrative element Tn6283. Molecular genetics analysis suggested a two-step gene transfer model. First, Tn6283 integrates into the recipient chromosome during suicidal plasmid transfer, followed by homologous recombination between the Tn6283 copy in the chromosome and that in the newly transferred pSEA1. Tn6283 is unusual among integrative elements in that it apparently does not encode transfer function and its excision barely generates unoccupied donor sites. Thus, its movement is analogous to the transposition of insertion sequences rather than to that of canonical integrative and conjugative elements. Overall, this study reveals the presence of a previously unrecognized type of MGE in a marine organism, highlighting diversity in the mode of interspecies gene transfer. |
| format | Article |
| id | doaj-art-b8b30f25637d40cf86e410760340978e |
| institution | DOAJ |
| issn | 1932-6203 |
| language | English |
| publishDate | 2018-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj-art-b8b30f25637d40cf86e410760340978e2025-08-20T03:04:35ZengPublic Library of Science (PLoS)PLoS ONE1932-62032018-01-01136e019861310.1371/journal.pone.0198613Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate.Lisa NonakaTatsuya YamamotoFumito MaruyamaYuu HiroseYuki OnishiTakeshi KobayashiSatoru SuzukiNobuhiko NomuraMichiaki MasudaHirokazu YanoThe capture of antimicrobial resistance genes (ARGs) by mobile genetic elements (MGEs) plays a critical role in resistance acquisition for human-associated bacteria. Although aquaculture environments are recognized as important reservoirs of ARGs, intra- and intercellular mobility of MGEs discovered in marine organisms is poorly characterized. Here, we show a new pattern of interspecies ARGs transfer involving a 'non-conjugative' integrative element. To identify active MGEs in a Vibrio ponticus isolate, we conducted whole-genome sequencing of a transconjugant obtained by mating between Escherichia coli and Vibrio ponticus. This revealed integration of a plasmid (designated pSEA1) into the chromosome, consisting of a self-transmissible plasmid backbone of the MOBH group, ARGs, and a 13.8-kb integrative element Tn6283. Molecular genetics analysis suggested a two-step gene transfer model. First, Tn6283 integrates into the recipient chromosome during suicidal plasmid transfer, followed by homologous recombination between the Tn6283 copy in the chromosome and that in the newly transferred pSEA1. Tn6283 is unusual among integrative elements in that it apparently does not encode transfer function and its excision barely generates unoccupied donor sites. Thus, its movement is analogous to the transposition of insertion sequences rather than to that of canonical integrative and conjugative elements. Overall, this study reveals the presence of a previously unrecognized type of MGE in a marine organism, highlighting diversity in the mode of interspecies gene transfer.https://storage.googleapis.com/plos-corpus-prod/10.1371/journal.pone.0198613/1/pone.0198613.pdf?X-Goog-Algorithm=GOOG4-RSA-SHA256&X-Goog-Credential=wombat-sa%40plos-prod.iam.gserviceaccount.com%2F20210221%2Fauto%2Fstorage%2Fgoog4_request&X-Goog-Date=20210221T142159Z&X-Goog-Expires=3600&X-Goog-SignedHeaders=host&X-Goog-Signature=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 |
| spellingShingle | Lisa Nonaka Tatsuya Yamamoto Fumito Maruyama Yuu Hirose Yuki Onishi Takeshi Kobayashi Satoru Suzuki Nobuhiko Nomura Michiaki Masuda Hirokazu Yano Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. PLoS ONE |
| title | Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. |
| title_full | Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. |
| title_fullStr | Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. |
| title_full_unstemmed | Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. |
| title_short | Interplay of a non-conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture Vibrio isolate. |
| title_sort | interplay of a non conjugative integrative element and a conjugative plasmid in the spread of antibiotic resistance via suicidal plasmid transfer from an aquaculture vibrio isolate |
| url | https://storage.googleapis.com/plos-corpus-prod/10.1371/journal.pone.0198613/1/pone.0198613.pdf?X-Goog-Algorithm=GOOG4-RSA-SHA256&X-Goog-Credential=wombat-sa%40plos-prod.iam.gserviceaccount.com%2F20210221%2Fauto%2Fstorage%2Fgoog4_request&X-Goog-Date=20210221T142159Z&X-Goog-Expires=3600&X-Goog-SignedHeaders=host&X-Goog-Signature=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 |
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