Ecological and evolutionary solutions to the plasmid paradox

Brockhurst, Michael A.; Harrison, Ellie

doi:10.1016/j.tim.2021.11.001

Cited by 87 publications

(83 citation statements)

References 94 publications

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“…Plasmid carriage is expected to impose a fitness cost on the host, but plasmid bearing microbes are pervasive in nature [47]. We showed previously that carriage of IncI1-pST26 by S .…”

Section: Discussionmentioning

confidence: 99%

Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance toSalmonellain chickens

Oladeinde

Abdo

Zwirzitz

et al. 2021

Preprint

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Host microbiome homeostasis ensures that gut conditions are unfavorable to an invading pathogen such as Salmonella enterica. Consequently, fostering a 'balanced' gut microbiome through the administration of microbes that can competitively exclude pathogens has gained a lot of attention and use in human and animal medicine. However, little is known on how competitive exclusion affects the transfer of antibiotic resistance. To shed more light on this question, we challenged neonatal broiler chicks raised on reused broiler chicken litter – a complex environment comprising of decomposing pine shavings, feces, uric acid, feathers, and feed, with Salmonella Heidelberg (S. Heidelberg), a model pathogen. We show that chicks raised on reused litter carried lower abundance of Salmonella and harbored a more uniform and diverse microbiome comprising of bacterial species that are known to provide colonization resistance towards Salmonella compared to chicks raised on fresh bedding composed of pine shavings. Additionally, these bacterial species were associated with a lower horizontal transfer of multidrug resistance genes to S. Heidelberg. Using in vitro competition experiments, we confirmed that conjugation between S. Heidelberg and E. coli strains from chicks raised on fresh litter resulted in the acquisition of multidrug resistant plasmids. Contrastingly, bacteriophage-mediated recombination between S. Heidelberg and E. coli strains made the acquisition of plasmid-mediated β-lactamase gene (blaCMY-2)possible. Collectively, this study demonstrates that competitive exclusion can reduce the transfer of antibiotic resistance and provides information on the bacterial species that can be explored for their benefits to reduce antibiotic resistance transfer.

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“…Plasmid carriage is expected to impose a fitness cost on the host, but plasmid bearing microbes are pervasive in nature [47]. We showed previously that carriage of IncI1-pST26 by S .…”

Section: Discussionmentioning

confidence: 99%

Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance toSalmonellain chickens

Oladeinde

Abdo

Zwirzitz

et al. 2021

Preprint

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“…However, long-term bacteria-plasmid co-culture experiments have shown that plasmids can persist for long periods, even in the absence of positive selection [ 87 , 88 ]. This discrepancy between theoretical predictions and experimental observations constitutes “the plasmid paradox” [ 89 – 91 ]. To achieve this higher-than-predicted stability, CPs have evolved multiple mechanisms that promote their persistence at the population level.…”

Section: After Conjugationmentioning

confidence: 99%

“…On the other hand, FinQ, encoded by IncI1 plasmids such as R820a, terminates transcription of the tra operon at multiple sites in a Rho-independent fashion [ 112 ]. Consistent with these FI systems targeting transcription of transfer genes, long-term bacteria-plasmid co-culture experiments demonstrated that down-regulation of transfer genes expression could ameliorate the cost-of-carriage of CPs [ 91 ].…”

Section: After Conjugationmentioning

confidence: 99%

Towards a better understanding of antimicrobial resistance dissemination: what can be learnt from studying model conjugative plasmids?

2022

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Bacteria can evolve rapidly by acquiring new traits such as virulence, metabolic properties, and most importantly, antimicrobial resistance, through horizontal gene transfer (HGT). Multidrug resistance in bacteria, especially in Gram-negative organisms, has become a global public health threat often through the spread of mobile genetic elements. Conjugation represents a major form of HGT and involves the transfer of DNA from a donor bacterium to a recipient by direct contact. Conjugative plasmids, a major vehicle for the dissemination of antimicrobial resistance, are selfish elements capable of mediating their own transmission through conjugation. To spread to and survive in a new bacterial host, conjugative plasmids have evolved mechanisms to circumvent both host defense systems and compete with co-resident plasmids. Such mechanisms have mostly been studied in model plasmids such as the F plasmid, rather than in conjugative plasmids that confer antimicrobial resistance (AMR) in important human pathogens. A better understanding of these mechanisms is crucial for predicting the flow of antimicrobial resistance-conferring conjugative plasmids among bacterial populations and guiding the rational design of strategies to halt the spread of antimicrobial resistance. Here, we review mechanisms employed by conjugative plasmids that promote their transmission and establishment in Gram-negative bacteria, by following the life cycle of conjugative plasmids.

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“…However, in the absence of antibiotics, plasmid-induced physiological alterations frequently lead to a decrease in bacterial fitness, a phenomenon known as plasmid cost 11,12 . This cost can be mitigated over time through compensatory mutations in the plasmid or chromosome [13][14][15] .…”

Section: Introductionmentioning

confidence: 99%

Within-patient evolution of plasmid-mediated antimicrobial resistance

DelaFuente

Toribio-Celestino

Santos-López

et al. 2022

Preprint

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Antibiotic resistance (AMR) in bacteria is a major threat to public health, and one of the key elements in the spread and evolution of AMR in clinical pathogens is the transfer of conjugative plasmids. The drivers of AMR evolution have been extensively studied in vitro, but the evolution of plasmid-mediated AMR in vivo remains poorly explored. Here, we tracked the evolution of the clinically-relevant plasmid pOXA-48, which confers resistance to the last-resort antibiotics carbapenems, in a large collection of enterobacterial clones isolated from the gut of hospitalised patients. Combining genomic and experimental approaches, we first characterized plasmid diversity and the genotypic and phenotypic effects of multiple plasmid mutations on a common genetic background. Second, using cutting-edge genomic editing in wild-type multidrug resistant enterobacteria, we dissected three cases of within-patient plasmid-mediated AMR evolution. Our results revealed, for the first time, compensatory evolution of plasmid-associated fitness cost, as well as the evolution of enhanced plasmid-mediated AMR, in bacteria evolving within the gut of hospitalised patients. Crucially, we observed that the evolution of plasmid-mediated AMR in vivo involves a pivotal trade-off between resistance levels and bacterial fitness. This study highlights the need to develop new evolution-informed approaches to tackle plasmid-mediated AMR dissemination.

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Ecological and evolutionary solutions to the plasmid paradox

Cited by 87 publications

References 94 publications

Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance toSalmonellain chickens

Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance toSalmonellain chickens

Towards a better understanding of antimicrobial resistance dissemination: what can be learnt from studying model conjugative plasmids?

Within-patient evolution of plasmid-mediated antimicrobial resistance

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