Atypical integrative element with strand-biased circularization activity assists interspecies antimicrobial resistance gene transfer from Vibrio alfacsensis

PLoS One. 2022 Aug 2;17(8):e0271627. doi: 10.1371/journal.pone.0271627. eCollection 2022.

Abstract

The exchange of antimicrobial resistance (AMR) genes between aquaculture and terrestrial microbial populations has emerged as a serious public health concern. However, the nature of the mobile genetic elements in marine bacteria is poorly documented. To gain insight into the genetic mechanisms underlying AMR gene transfer from marine bacteria, we mated a multidrug-resistant Vibrio alfacsensis strain with an Escherichia coli strain, and then determined the complete genome sequences of the donor and the transconjugant strains. Sequence analysis revealed a conjugative multidrug resistance plasmid in the donor strain, which was integrated into the chromosome of the recipient. The plasmid backbone in the transconjugant chromosome was flanked by two copies of a 7.1 kb unclassifiable integrative element harboring a β-lactamase gene. The 7.1 kb element and the previously reported element Tn6283 share four coding sequences, two of which encode the catalytic R-H-R-Y motif of tyrosine recombinases. Polymerase chain reaction and sequencing experiments revealed that these elements generate a circular copy of one specific strand without leaving an empty site on the donor molecule, in contrast to the movement of integron gene cassettes or ICE/IMEs discovered to date. These elements are termed SEs (strand-biased circularizing integrative elements): SE-6945 (the 7.1 kb element) and SE-6283 (Tn6283). The copy number and location of SE-6945 in the chromosome affected the antibiotic resistance levels of the transconjugants. SEs were identified in the genomes of other Vibrio species. Overall, these results suggest that SEs are involved in the spread of AMR genes among marine bacteria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents* / pharmacology
  • Conjugation, Genetic
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli / genetics
  • Gene Transfer, Horizontal
  • Plasmids / genetics
  • Vibrio* / genetics

Substances

  • Anti-Bacterial Agents

Supplementary concepts

  • Vibrio alfacsensis

Associated data

  • figshare/10.6084/m9.figshare.13332467

Grants and funding

This research is supported by JSPS KAKENHI 18K05790 (LN), 22K05790 (LN), research grant from Mishima Kaium Memorial Foundation (HY). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.