Conjugative plasmids interact with insertion sequences to shape the horizontal transfer of antimicrobial resistance genes

Che, Ying; Yang, Yu; Xu, Xiaoqing; Břinda, Karel; Polz, Martin F.; Hanage, William P.; Zhang, Tong

doi:10.1073/pnas.2008731118

Cited by 169 publications

(120 citation statements)

References 79 publications

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“…functions and the formation of new mobile genetic elements through plasmid-plasmid recombination (8)(9)(10). Nevertheless, the observed high rates of plasmid coinfection are surprising, given that plasmid acquisition usually disrupts normal cellular function and is often associated with large fitness costs for the host cell (11)(12)(13)(14)(15).…”

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confidence: 99%

Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes

Carrilero

Kottara

Guymer

et al. 2021

mBio

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Plasmids play an important role in bacterial evolution by transferring niche-adaptive functional genes between lineages, thus driving genomic diversification. Bacterial genomes commonly contain multiple, coexisting plasmid replicons, which could fuel adaptation by increasing the range of gene functions available to selection and allowing their recombination. However, plasmid coexistence is difficult to explain because the acquisition of plasmids typically incurs high fitness costs for the host cell. Here, we show that plasmid coexistence was stably maintained without positive selection for plasmid-borne gene functions and was associated with compensatory evolution to reduce fitness costs. In contrast, with positive selection, plasmid coexistence was unstable despite compensatory evolution. Positive selection discriminated between differential fitness benefits of functionally redundant plasmid replicons, retaining only the more beneficial plasmid. These data suggest that while the efficiency of negative selection against plasmid fitness costs declines over time due to compensatory evolution, positive selection to maximize plasmid-derived fitness benefits remains efficient. Our findings help to explain the forces structuring bacterial genomes: coexistence of multiple plasmids in a genome is likely to require either rare positive selection in nature or nonredundancy of accessory gene functions among the coexisting plasmids. IMPORTANCE Bacterial genomes often contain multiple coexisting plasmids that provide important functions like antibiotic resistance. Using lab experiments, we show that such plasmid coexistence within a genome is stable only in environments where the function they encode is useless but is unstable if the function is useful and beneficial for bacterial fitness. Where competing plasmids perform the same useful function, only the most beneficial plasmid is kept by the cell, a process that is similar to competitive exclusion in ecological communities. This process helps explain how bacterial genomes are structured: bacterial genomes expand in size by acquiring multiple plasmids when selection is relaxed but subsequently contract during periods of strong selection for the useful plasmid-encoded function.

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confidence: 99%

Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes

Carrilero

Kottara

Guymer

et al. 2021

mBio

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“…The beta-lactamase gene identified in this study was embedded within the mobile DNA unit without an accompanying insertion sequence element, like the case for Tn 3 [43]. This pattern is atypical for recent widespread AMR genes [44, 45], suggesting an ancient origin for the Tn 6283 -like element with the beta-lactamase gene. As Tn 6945 can have multiple target sites in a single genome, a Tn 6283 -like element may contribute to microbial adaptation to the antimicrobials used at aquaculture sites, with diverse mechanisms beyond mediating the horizontal transmission of AMR genes, such as increasing the resistance level or gene redundancy preceding evolutionary innovation of an AMR gene [46].…”

Section: Discussionmentioning

confidence: 63%

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

Nonaka

Masuda

Yano

2021

Preprint

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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 multi-drug resistant Vibrio alfacsensis strain with an Escherichia coli strain, and then determined the complete genome sequences of the donor strain and multidrug-resistant transconjugants. Sequence analysis revealed a conjugative plasmid of the MOBH family 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 integrative element, designated Tn 6945, harboring a beta-lactamase gene that conferred ampicillin resistance to the host cell. Use of a recA mutant E. coli strain as the recipient yielded a transconjugant showing ampicillin resistance but not multidrug resistance, suggesting the involvement of homologous recombination in plasmid integration into the chromosome. Polymerase chain reaction experiments revealed that Tn 6945 generates a circular copy without generating an empty donor site, suggesting that it moves via a copy-out-paste-in mode, as previously reported for Tn 6283. Transposition of the integrative element into multiple loci in the recipient chromosome increased the resistance level of the transconjugants. Overall, these results suggest that Tn 6283-like copy-out integrative elements and conjugative plasmids additively spread AMR genes among marine bacteria and contribute to the emergence of isolates with high-level resistance through amplification of AMR genes.

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“…Che et al . showed that most ARG genes are located in conjugative plasmids, which -together with Insertion Sequences-play the most important role in mediating the horizontal transfer of ARGs (Che et al, 2021). When the relationship between ARG and ISs were investigated, we did not analyze the location of ARGs which might explain why no significant correlation between the two was observed in our study.…”

Section: Resultsmentioning

confidence: 99%

BacAnt: A Combination Annotation Server for Bacterial DNA Sequences to Identify Antibiotic Resistance Genes, Integrons, and Transposable Elements

Hua

Liang

Deng

et al. 2020

Preprint

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Whole genome sequencing (WGS) of bacteria has become a routine method in diagnostic laboratories. One of the most exciting advantages of WGS is the ability to predict antimicrobial resistance genes (ARGs) and mobile genetic elements (MGEs) in a variety of bacteria, which may allow comprehensive investigations of genetic features but also serve for epidemiological studies. A plethora of softwares have been developed for the detailed annotation of DNA sequences, such as RAST (Rapid Annotation using Subsystem Technology), Resfinder, ISfinder, INTEGRALL and The Transposon Registry. Unfortunately, up to now, a reliable annotation tool of the combination of ARGs and MGEs is not available to researchers, and the generation of genbank files requires much manual input. Here, we present a new webserver which allows the annotation of ARGs, ISs, integron, and transposable elements at the same time. The algorithm generates genbank files automatically, which are compatible with easyfig for comparative genomic analysis.

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Conjugative plasmids interact with insertion sequences to shape the horizontal transfer of antimicrobial resistance genes

Cited by 169 publications

References 79 publications

Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes

Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes

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

BacAnt: A Combination Annotation Server for Bacterial DNA Sequences to Identify Antibiotic Resistance Genes, Integrons, and Transposable Elements

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