Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse Escherichia coli Lineages

Dunn, Steven; Carrilero, Laura; Brockhurst, Michael A.; McNally, Alan

doi:10.1128/msystems.00083-21

Cited by 30 publications

(41 citation statements)

References 38 publications

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“…First, it is rarely confirmed that the plasmid-carrying transconjugants have not acquired other chromosomal mutations that may alter chromosomal transcription independently of the plasmid. This could be determined by curing the plasmid and confirming that transcription returns to wild-type levels, or by genome sequencing the transconjugant to confirm no additional mutations are present [ 28 ]. More studies with these additional controls would be valuable.…”

Section: What Is the ‘Omic’ Footprint Of Plasmid Acquisition Upon The Host Cell?mentioning

confidence: 99%

“…carbohydrate, energy, amino acid), with the direction of regulation often varying among bacterium–plasmid pairings, sometimes for the same functional group of genes [ 20 ]. An interesting example where a consistent effect is observed across diverse host strains is the plasmid pLL35, which causes the upregulation of bacterial anaerobic metabolism genes in phylogenetically diverse E. coli backgrounds [ 28 ]. Although the effect on bacterial growth is unknown, it is possible that by shifting the host cell from aerobic towards anaerobic metabolism, the plasmid may potentiate gut colonization, and thereby promote the fitness of both the bacterium and the plasmid in this niche.…”

Section: Linking Altered Expression Of Bacterial Functions To Plasmid Fitnessmentioning

confidence: 99%

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Why do plasmids manipulate the expression of bacterial phenotypes?

Billane

Harrison

Cameron

et al. 2021

Phil. Trans. R. Soc. B

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Conjugative plasmids play an important role in bacterial evolution by transferring niche-adaptive traits between lineages, thus driving adaptation and genome diversification. It is increasingly clear, however, that in addition to this evolutionary role, plasmids also manipulate the expression of a broad range of bacterial phenotypes. In this review, we argue that the effects that plasmids have on the expression of bacterial phenotypes may often represent plasmid adaptations, rather than mere deleterious side effects. We begin by summarizing findings from untargeted omics analyses, which give a picture of the global effects of plasmid acquisition on host cells. Thereafter, because many plasmids are capable of both vertical and horizontal transmission, we distinguish plasmid-mediated phenotypic effects into two main classes based upon their potential fitness benefit to plasmids: (i) those that promote the competitiveness of the host cell in a given niche and thereby increase plasmid vertical transmission, and (ii) those that promote plasmid conjugation and thereby increase plasmid horizontal transmission. Far from being mere vehicles for gene exchange, we propose that plasmids often act as sophisticated genetic parasites capable of manipulating their bacterial hosts for their own benefit. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.

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Section: What Is the ‘Omic’ Footprint Of Plasmid Acquisition Upon The Host Cell?mentioning

confidence: 99%

Section: Linking Altered Expression Of Bacterial Functions To Plasmid Fitnessmentioning

confidence: 99%

Why do plasmids manipulate the expression of bacterial phenotypes?

Billane

Harrison

Cameron

et al. 2021

Phil. Trans. R. Soc. B

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show abstract

“…Plasmid persistence is generally expected to depend on the balance of growth costs (how plasmids affect bacterial population growth) and transfer rates (typically by conjugation) and, to a lesser extent given many natural plasmids carry addiction systems, segregational loss (Stewart and Levin, 1977; Levin et al ., 1979; Finbarr, 1995; Ponciano et al ., 2007; San Millán et al ., 2014). Past work showed growth costs (Alonso-del Valle et al ., 2021; Dunn et al ., 2021), transfer rates (Lopatkin et al ., 2017; Sheppard et al ., 2020) and segregational loss (De Gelder et al ., 2007) can vary depending on the bacterium-plasmid combination. This variability may therefore be central to predicting the long-term stability of plasmids (over hundreds of generations and in the absence of antibiotics).…”

Section: Introductionmentioning

confidence: 99%

Host-specific plasmid evolution explains the variable spread of clinical antibiotic-resistance plasmids

Benz

Hall

2022

Preprint

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Antibiotic resistance encoded on plasmids is a pressing global health problem. Predicting which plasmids spread/decline in the long term remains a huge challenge, even though some key parameters influencing plasmid stability have been identified, such as plasmid growth costs and horizontal transfer rates. Here, we show these parameters evolve in a strain-specific way among clinical plasmids/bacteria, and this occurs rapidly enough to alter the relative likelihoods of different bacterium-plasmid combinations spreading/declining. We used experiments with Escherichia coli and antibiotic-resistance plasmids isolated from patients, paired with a mathematical model, to show long-term plasmid stability (beyond antibiotic exposure) was better explained by evolutionary changes in plasmid-stability traits than by initial variation among bacterium-plasmid combinations. Evolutionary trajectories were specific to particular bacterium-plasmid combinations. Genome sequencing and genetic manipulation helped explain this, revealing epistatic (here, strain-dependent) effects of key genetic changes affecting horizontal plasmid transfer. Several genetic changes involved mobile elements and pathogenicity islands. Rapid strain-specific evolution can thus outweigh ancestral phenotypes as a predictor of plasmid stability. Accounting for strain-specific plasmid evolution in natural populations could improve our ability to anticipate and manage successful bacterium-plasmid combinations.

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“…Ancestral WGS data are available under Bioproject Accession number PRJNA667580, and are described in (Dunn et al, 2021).…”

Section: Genomics and Bioinformaticsmentioning

confidence: 99%

“…Evolved plasmid-carrier clones were tested for their ability to conjugate pLL35 into an E. coli J53 recipient strain as previously described (Dunn et al 2021). Conjugation positive strains are demoted with "+" and conjugation deficient strains are denoted with "-".…”

Section: Table S3 | Conjugational Abilities Of Evolved Clonesmentioning

confidence: 99%

Evolutionary responses to acquiring a multidrug resistance plasmid are dominated by metabolic functions across diverse Escherichia coli lineages

Carrilero

Dunn

McNally

et al. 2022

Preprint

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Multidrug resistance (MDR) plasmids drive the spread of antibiotic resistance between bacterial lineages. The immediate impact of MDR plasmid acquisition on fitness and cellular processes varies among bacterial lineages, but how the evolutionary processes enabling the genomic integration of MDR plasmids vary is less well understood, particularly in clinical pathogens. Using diverse Escherichia coli lineages experimentally evolved for ~700 generations, we show that the evolutionary response to gaining the MDR plasmid pLL35 was dominated by chromosomal mutations affecting metabolic and regulatory functions, with both strain-specific and shared mutational targets. The expression of several of these functions, such as anaerobic metabolism, is known to be altered upon acquisition of pLL35. Interactions with resident mobile genetic elements, notably several IS-elements, potentiated parallel mutations, including insertions upstream of hns that were associated with its upregulation and the downregulation of the plasmid-encoded extended-spectrum beta-lactamase gene. Plasmid parallel mutations targeted conjugation-related genes, whose expression was also commonly downregulated in evolved clones. Beyond their role in horizontal gene transfer, plasmids can be an important selective force shaping the evolution of bacterial chromosomes and core cellular functions.

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Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse Escherichia coli Lineages

Cited by 30 publications

References 38 publications

Why do plasmids manipulate the expression of bacterial phenotypes?

Why do plasmids manipulate the expression of bacterial phenotypes?

Host-specific plasmid evolution explains the variable spread of clinical antibiotic-resistance plasmids

Evolutionary responses to acquiring a multidrug resistance plasmid are dominated by metabolic functions across diverse Escherichia coli lineages

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