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

• Published in: PloS one Vol. 13; no. 6; p. e0198613
• Main Authors: Nonaka, Lisa, Yamamoto, Tatsuya, Maruyama, Fumito, Hirose, Yuu, Onishi, Yuki, Kobayashi, Takeshi, Suzuki, Satoru, Nomura, Nobuhiko, Masuda, Michiaki, Yano, Hirokazu
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 07-06-2018; Public Library of Science (PLoS)
• Subjects: Analysis; Antibiotic resistance; Antibiotics; Antimicrobial resistance; Aquaculture; Aquaculture industry; Aquatic Organisms - drug effects; Aquatic Organisms - genetics; Aquatic Organisms - physiology; Biodiversity; Biology and Life Sciences; Chromosomes; Drug Resistance, Bacterial - genetics; E coli; Environmental science; Environmental studies; Escherichia coli - drug effects; Escherichia coli - genetics; Escherichia coli - physiology; Gene sequencing; Gene transfer; Gene Transfer, Horizontal; Genes; Genetic aspects; Genetics; Genomes; Homologous recombination; Homology; Insertion; Insertion sequences; Life sciences; Marine organisms; Medicine; Microbial drug resistance; Mobile genetic elements; Molecular chains; Plasmids; R Factors - genetics; Research and Analysis Methods; Suicidal behavior; Transfer functions; Transposition; Vibrio; Vibrio - drug effects; Vibrio - genetics; Vibrio - physiology; Vibrio cholerae; Waterborne diseases; Whole Genome Sequencing; United States > US; Japan
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0198613

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.