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

被引:10
|
作者
Nonaka, Lisa [1 ]
Yamamoto, Tatsuya [2 ]
Maruyama, Fumito [3 ]
Hirose, Yuu [4 ]
Onishi, Yuki [5 ]
Kobayashi, Takeshi [6 ]
Suzuki, Satoru [5 ]
Nomura, Nobuhiko [2 ]
Masuda, Michiaki [1 ]
Yano, Hirokazu [2 ,7 ]
机构
[1] Dokkyo Med Univ, Dept Microbiol, Sch Med, Mibu, Tochigi, Japan
[2] Univ Tsukuba, Fac Life & Environm Sci, Tsukuba, Ibaraki, Japan
[3] Kyoto Univ, Grad Sch Med, Kyoto, Japan
[4] Toyohashi Univ Technol, Dept Environm & Life Sci, Tempaku Ku, Toyohashi, Aichi, Japan
[5] Ehime Univ, Ctr Marine Environm Studies, Matsuyama, Ehime, Japan
[6] Ehime Univ, Grad Sch Med, To On, Ehime, Japan
[7] Tohoku Univ, Grad Sch Life Sci, Aoba Ku, Sendai, Miyagi, Japan
来源
PLOS ONE | 2018年 / 13卷 / 06期
基金
日本科学技术振兴机构;
关键词
CHROMOSOMAL INSERTION; COMPARATIVE GENOMICS; GENES; STRAIN; SITE; DIVERSITY; EXCISION; SEAWATER; NIGRIPULCHRITUDO; RECOMBINATION;
D O I
10.1371/journal.pone.0198613
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The capture of antimicrobial resistance genes (ARGs) by mobile genetic elements (MGEs) plays a critical role in resistance acquisition for human-associated bacteria. Although aqua culture 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 Tn 6283. Molecular genetics analysis suggested a two-step gene transfer model. First, Tn 6283 integrates into the recipient chromosome during suicidal plasmid transfer, followed by homologous recombination between the Tn6283copy in the chromosome and that in the newly transferred pSEA1. Tn 6283 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.
引用
收藏
页数:26
相关论文
共 50 条
  • [21] Non-antibiotic pharmaceuticals promote conjugative plasmid transfer at a community-wide level
    Wang, Yue
    Yu, Zhigang
    Ding, Pengbo
    Lu, Ji
    Kluemper, Uli
    Murray, Aimee K.
    Gaze, William H.
    Guo, Jianhua
    MICROBIOME, 2022, 10 (01)
  • [22] Environmental free radicals efficiently inhibit the conjugative transfer of antibiotic resistance by altering cellular metabolism and plasmid transfer
    Li, Hu
    Song, Ruiying
    Wang, Yangyang
    Zhong, Rongwei
    Wang, Tiecheng
    Jia, Hanzhong
    Zhu, Lingyan
    WATER RESEARCH, 2022, 209
  • [23] Ionic Liquid Facilitates the Conjugative Transfer of Antibiotic Resistance Genes Mediated by Plasmid RP4
    Wang, Qing
    Mao, Daqing
    Luo, Yi
    ENVIRONMENTAL SCIENCE & TECHNOLOGY, 2015, 49 (14) : 8731 - 8740
  • [24] Impact of Redox Conditions on Antibiotic Resistance Conjugative Gene Transfer Frequency and Plasmid Fate in Wastewater Ecosystems
    Jong, Mui-Choo
    Harwood, Colin R.
    Blackburn, Adrian
    Snape, Jason R.
    Graham, David W.
    ENVIRONMENTAL SCIENCE & TECHNOLOGY, 2020, 54 (23) : 14984 - 14993
  • [25] Acquisition and transfer of antibiotic resistance genes in association with conjugative plasmid or class 1 integrons of Acinetobacter baumannii
    Leungtongkam, Udomluk
    Thummeepak, Rapee
    Tasanapak, Kannipa
    Sitthisak, Sutthirat
    PLOS ONE, 2018, 13 (12):
  • [26] Melatonin prevents conjugative transfer of plasmid-mediated antibiotic resistance genes by disrupting proton motive force
    Jia, Yuqian
    Yang, Bingqing
    Shi, Jingru
    Fang, Dan
    Wang, Zhiqiang
    Liu, Yuan
    PHARMACOLOGICAL RESEARCH, 2022, 175
  • [27] Paclitaxel and its derivative facilitate the transmission of plasmid-mediated antibiotic resistance genes through conjugative transfer
    Yang, Bingqing
    Wang, Zhiqiang
    Jia, Yuqian
    Fang, Dan
    Li, Ruichao
    Liu, Yuan
    SCIENCE OF THE TOTAL ENVIRONMENT, 2022, 810
  • [28] A maverick: Environmentally relevant concentrations of nonylphenol attenuate the plasmid-mediated conjugative transfer of antibiotic resistance genes
    Liang, Si-Zhou
    Chang, Ya-Jun
    Semaha, Philip
    Liu, Li-Zhu
    Gao, Yan
    Wang, Zhi
    Zhang, Wei-Guo
    WATER RESEARCH X, 2024, 24
  • [29] Antibiotic resistance conferred by conjugative plasmid in Escherichia coli isolated from community ponds of Kathmandu Valley
    Adhikari, RP
    Kalpana, KC
    Shears, P
    Sharma, AP
    JOURNAL OF HEALTH POPULATION AND NUTRITION, 2000, 18 (01) : 57 - 59
  • [30] Fe-doped TiO2 nanosheet exposure accelerates the spread of antibiotic resistance genes by promoting plasmid-mediated conjugative transfer
    Cheng, Ping
    Wang, Botao
    Ji, Qianyu
    Yuan, Pingping
    Gui, Shixin
    Liang, Shuying
    Li, Lin
    Xu, Hongwei
    Qu, Shaoqi
    JOURNAL OF HAZARDOUS MATERIALS, 2025, 490