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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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Autores principales: Nonaka, Lisa, Yamamoto, Tatsuya, Maruyama, Fumito, Hirose, Yuu, Onishi, Yuki, Kobayashi, Takeshi, Suzuki, Satoru, Nomura, Nobuhiko, Masuda, Michiaki, Yano, Hirokazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5991714/
https://www.ncbi.nlm.nih.gov/pubmed/29879198
http://dx.doi.org/10.1371/journal.pone.0198613
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author Nonaka, Lisa
Yamamoto, Tatsuya
Maruyama, Fumito
Hirose, Yuu
Onishi, Yuki
Kobayashi, Takeshi
Suzuki, Satoru
Nomura, Nobuhiko
Masuda, Michiaki
Yano, Hirokazu
author_facet Nonaka, Lisa
Yamamoto, Tatsuya
Maruyama, Fumito
Hirose, Yuu
Onishi, Yuki
Kobayashi, Takeshi
Suzuki, Satoru
Nomura, Nobuhiko
Masuda, Michiaki
Yano, Hirokazu
author_sort Nonaka, Lisa
collection PubMed
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 MOB(H) 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.
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spelling pubmed-59917142018-06-16 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 Nonaka, Lisa Yamamoto, Tatsuya Maruyama, Fumito Hirose, Yuu Onishi, Yuki Kobayashi, Takeshi Suzuki, Satoru Nomura, Nobuhiko Masuda, Michiaki Yano, Hirokazu PLoS One Research Article 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 MOB(H) 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. Public Library of Science 2018-06-07 /pmc/articles/PMC5991714/ /pubmed/29879198 http://dx.doi.org/10.1371/journal.pone.0198613 Text en © 2018 Nonaka et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Nonaka, Lisa
Yamamoto, Tatsuya
Maruyama, Fumito
Hirose, Yuu
Onishi, Yuki
Kobayashi, Takeshi
Suzuki, Satoru
Nomura, Nobuhiko
Masuda, Michiaki
Yano, Hirokazu
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 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5991714/
https://www.ncbi.nlm.nih.gov/pubmed/29879198
http://dx.doi.org/10.1371/journal.pone.0198613
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