Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species

Kottara, Anastasia; Hall, James P. J.; Harrison, Ellie; Brockhurst, Michael A.

doi:10.1093/femsec/fix172

Cited by 76 publications

(76 citation statements)

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“…The consequent fitness costs can limit plasmid survival because plasmid-bearers will be outcompeted by plasmid-free cells that do not suffer the cost [2]. Beneficial genes carried by the plasmid cannot ensure its long-term persistence, as these genes can recombine onto the chromosome [3, 4]. An important mechanism allowing plasmid survival is compensatory evolution whereby mutations in chromosomal and/or plasmid genes ameliorate fitness costs (e.g.…”

Section: Introductionmentioning

confidence: 99%

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

et al. 2020

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The acquisition of plasmids is often accompanied by fitness costs such that compensatory evolution is required to allow plasmid survival, but it is unclear whether compensatory evolution can be extensive or rapid enough to maintain plasmids when they are very costly. The mercury-resistance plasmid pQBR55 drastically reduced the growth of its host, Pseudomonas fluorescens SBW25, immediately after acquisition, causing a small colony phenotype. However, within 48 h of growth on agar plates we observed restoration of the ancestral large colony morphology, suggesting that compensatory mutations had occurred. Relative fitness of these evolved strains, in lab media and in soil microcosms, varied between replicates, indicating different mutational mechanisms. Using genome sequencing we identified that restoration was associated with chromosomal mutations in either a hypothetical DNA-binding protein PFLU4242, RNA polymerase or the GacA/S two-component system. Targeted deletions in PFLU4242, gacA or gacS recapitulated the ameliorated phenotype upon plasmid acquisition, indicating three distinct mutational pathways to compensation. Our data shows that plasmid compensatory evolution is fast enough to allow survival of a plasmid despite it imposing very high fitness costs upon its host, and indeed may regularly occur during the process of isolating and selecting individual plasmid-containing clones.

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Section: Introductionmentioning

confidence: 99%

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

et al. 2020

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“…The wide range of S α+δ values across phylotypes and conditions confirmed that the plasmid effect is a phylotype and context dependent feature. In fact, population-level studies have repeatedly revealed that plasmid effects are indeed determined by strain-specific factors [42,43]. We identify here, for the first time, individual specific plasmid effect within a complex microbial community.…”

Section: Discussionmentioning

confidence: 60%

Plasmids persist in a microbial community by providing fitness benefit to multiple phylotypes

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Madsen

et al. 2019

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21The current epidemic of antibiotic resistance has been facilitated by the wide and rapid 22 horizontal dissemination of antibiotic resistance genes (ARGs) in microbial communities. 23Indeed, ARGs are often located on plasmids, which can efficiently shuttle genes across diverse 24 taxa. While the existence conditions of plasmids have been extensively studied in a few model 25 bacterial populations, their fate in complex bacterial communities is poorly understood. Here, 26we coupled plasmid transfer assays with serial growth experiments to investigate the 27 persistence of the broad-host-range IncP-1 plasmid pKJK5 in microbial communities derived 28 from a sewage treatment plant. The cultivation conditions combined different nutrient and 29 oxygen levels, and were non-selective and non-conducive for liquid-phase conjugal transfer. 30Following initial transfer, the plasmid persisted in almost all conditions during a 10-day serial 31 growth experiment (equivalent to 60 generations), with a transient transconjugant incidence up 32 to 30%. By combining cell enumeration and sorting with amplicon sequencing, we mapped 33 plasmid fitness effects across taxa of the microbial community. Unexpected plasmid fitness 34 benefits were observed in multiple phylotypes of Aeromonas, Pseudomonas and 35Enterobacteriaceae, which resulted in community-level plasmid persistence. We demonstrate, 36 for the first time, that plasmid fitness effects across community members can be estimated in a 37 high-throughput way without prior isolation. By gaining a fitness benefit when carrying 38 plasmids, members within complex microbial communities might have a hitherto unrecognized 39 potential to maintain plasmids for long-term community-wide access. 40 41 Introduction 42Plasmids -extrachromosomal replicons -can support rapid bacterial adaptation by moving 43 genes between phylogenetically diverse bacteria, a process known as horizontal gene transfer 44[1]. This is particularly important in the case of antibiotic resistance, where acquisition of 45 plasmid-borne antibiotic resistance genes (ARGs) can instantly render a strain impervious to 46 antibiotic treatment [2]. The current global antibiotic resistance crisis has been largely 47 attributed to plasmid mediated ARG dissemination [3]. 48 49Strategies to combat the antibiotic resistance epidemic therefore require an understanding of 50 the mechanisms that underlie plasmid fate in microbial communities. Upon entering a 51 microbial community, a plasmid will only persist if its original or secondary hosts 52 (transconjugants) survive. If it persists, it will constitute a long-term reservoir of auxiliary 53 genes for that community. In fact, persistence of IncP-1 plasmids or their derivatives has 54 recently been observed in ex situ communities like anaerobic sludge microcosms [4] and 55 artificial multi-species system [5] over periods longer than 10 days, as well as in murine gut 56 microbiota experiments [6]. However, by simply interpreting plasmid persistence as the 57 frequency of plasmid ...

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“…The change in error bars is indicative of ongoing adaptation to the mixed culture conditions but, interestingly, I found no significant change in the number of pGW155B borne by R-cells during the competition ( Figure 2B, Mann-Whitney U-test p = 0.1 and ranksum= 15 for 3 replicates). Now, the cost of plasmid carriage is commonly measured using fitness [11,13,14,31,33] and this metric relies on growth rate [26,27]. How well does fitness predict the outcome of this competition?…”

Section: Resultsmentioning

confidence: 99%

“…So, here I asked what cost do microbes pay in each phase of microbial growth. The Malthusian parameter, metric widely used to estimate microbial and tumour growth rates [11,14,[26][27][28][29][30][31][32][33], could-in principle-reflect differences in lag, cell density during the stationary phase or, indeed, in growth rate [26]. But it cannot inform which trait is sensitive, and what cost they pay.…”

Section: Introductionmentioning

confidence: 99%

Plasmid carriage and the unorthodox use of fitness in microbial evolution

Reding

2019

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Microbes without plasmids divide faster than those harbouring them. Microbiolo-6 gists rely on this difference in growth rate between both types to foresee whether 7 a plasmid will be maintained, or else purged by the host to avoid extinction. Here 8 I report that plasmids change multiple life-history traits, and I demonstrate that 9 growth rate alone can be a bad predictor for plasmid maintenance. Pairwise com-10 petition experiments between two constructs of Escherichia coli-one of which car-11 ries a plasmid-revealed that harbouring plasmids can also increase yield and delay 12 growth (lag). Crucially, yield engaged in a trade-off with growth rate. The plasmid 13 borne by one construct (R), non-transmissible and with a tetracycline-resistance 14 gene, reduced its host's growth rate by 20%. However, given this trade-off, R 15 outgrew its sensitive counterpart (S) in the absence of tetracycline when the com-16 petition favoured yield over growth rate. Trade-offs like this can challenge the 17 application of concepts that depend on carriage costs: R-mutants with additional 18 copies of the plasmid exploited this trade-off, and were selected for in tetracycline 19concentrations below the so-called 'minimal selective concentration'-the lowest an-20 timicrobial concentration thought to select for resistant mutants. My data suggests 21 that carriage costs interfere with multiple traits. Whether plasmids are costly to 22 maintain will therefore depend on the relationship between them, and which is un-23 der strongest selection. It also demonstrates that each trait reports different drug 24 sensitivity, exposing new opportunities for therapy design. 26Plasmids are independent genetic elements that complement the chromosome of prokaryotes 1,2 27 and eukaryotes 3 alike. They can benefit cells harbouring them-notoriously in the form of 28 resistance to antibiotics-but the metabolic costs associated with their upkeep can reduce the 29 host's growth rate 2,4 . Clinicians and evolutionary biologists exploit the sensitivity of growth rate 30 to plasmid carriage, using pairwise competition experiments to estimate the costs of plasmid 31 maintenance 5-8 and whether a plasmid will be maintained through time. Their conclusion is 32 straightforward: microbes without plasmids multiply faster in environments where plasmids are 33 not beneficial, and overthrow microbes harbouring them 4,7 . 34Plasmids will therefore be preserved when the benefits they provide outweigh the reduction 35 in growth rate that they impose. Bacteria, however, can maintain plasmids that have no evident 36 benefit-despite reducing their growth rate 2,[9][10][11] . So, where is the hidden benefit? Plasmids are 37 2 known to reduce the host's growth rate, but the metabolic alterations that plasmids introduce 38 are unclear [12][13][14][15] . Here I asked whether growth rate is the only life-history trait that is sensitive 39 to plasmid carriage, and it is not. I analysed the growth dynamics of two identical constructs 16 40 of Escherichia coli, one of which ...

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Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species

Cited by 76 publications

References 44 publications

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

Plasmids persist in a microbial community by providing fitness benefit to multiple phylotypes

Plasmid carriage and the unorthodox use of fitness in microbial evolution

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