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Plasmid stability is enhanced by higher-frequency pulses of positive selection.

ABSTRACT: Plasmids accelerate bacterial adaptation by sharing ecologically important traits between lineages. However, explaining plasmid stability in bacterial populations is challenging owing to their associated costs. Previous theoretical and experimental studies suggest that pulsed positive selection may explain plasmid stability by favouring gene mobility and promoting compensatory evolution to ameliorate plasmid cost. Here we test how the frequency of pulsed positive selection affected the dynamics of a mercury-resistance plasmid, pQBR103, in experimental populations of Pseudomonas fluorescens SBW25. Plasmid dynamics varied according to the frequency of Hg2+ positive selection: in the absence of Hg2+ plasmids declined to low frequency, whereas pulses of Hg2+ selection allowed plasmids to sweep to high prevalence. Compensatory evolution to ameliorate the cost of plasmid carriage was widespread across the entire range of Hg2+ selection regimes, including both constant and pulsed Hg2+ selection. Consistent with theoretical predictions, gene mobility via conjugation appeared to play a greater role in promoting plasmid stability under low-frequency pulses of Hg2+ selection. However, upon removal of Hg2+ selection, plasmids which had evolved under low-frequency pulse selective regimes declined over time. Our findings suggest that temporally variable selection environments, such as those created during antibiotic treatments, may help to explain the stability of mobile plasmid-encoded resistance.

SUBMITTER: Stevenson C

PROVIDER: S-EPMC5784203 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Plasmid stability is enhanced by higher-frequency pulses of positive selection.

Stevenson Cagla C Hall James P J JPJ Brockhurst Michael A MA Harrison Ellie E

Proceedings. Biological sciences 20180101 1870

Plasmids accelerate bacterial adaptation by sharing ecologically important traits between lineages. However, explaining plasmid stability in bacterial populations is challenging owing to their associated costs. Previous theoretical and experimental studies suggest that pulsed positive selection may explain plasmid stability by favouring gene mobility and promoting compensatory evolution to ameliorate plasmid cost. Here we test how the frequency of pulsed positive selection affected the dynamics ...[more]

PMID: 29321301

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Project description: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.

Project description:Collembola are a basal group of Hexapoda renowned for both unique morphological characters and significant ecological roles. However, a robust and plausible phylogenetic relationship between its deeply divergent lineages has yet to be achieved. We carried out a mitophylogenomic study based on a so far the most comprehensive mitochondrial genome dataset. Our data matrix contained mitogenomes of 31 species from almost all major families of all four orders, with 16 mitogenomes newly sequenced and annotated. We compared the linear arrangements of genes along mitochondria across species. Then we conducted 13 analyses each under a different combination of character coding, partitioning scheme and heterotachy models, and assessed their performance in phylogenetic inference. Several hypothetical tree topologies were also tested. Mitogenomic structure comparison revealed that most species share the same gene order of putative ancestral pancrustacean pattern, while seven species from Onychiuridae, Poduridae and Symphypleona bear different levels of gene rearrangements, indicating phylogenetic signals. Tomoceroidea was robustly recovered for the first time in the presence of all its families and subfamilies. Monophyly of Onychiuroidea was supported using unpartitioned models alleviating LBA. Paronellidae was revealed polyphyletic with two subfamilies inserted independently into Entomobryidae. Although Entomobryomorpha has not been well supported, more than half of the analyses obtained convincing topologies by placing Tomoceroidea within or near remaining Entomobryomorpha. The relationship between elongate-shaped and spherical-shaped collembolans still remained ambiguous, but Neelipleona tend to occupy the basal position in most trees. This study showed that mitochondrial genomes could provide important information for reconstructing the relationships among Collembola when suitable analytical approaches are implemented. Of all the data refining and model selecting schemes used in this study, the combination of nucleotide sequences, partitioning model and exclusion of third codon positions performed better in generating more reliable tree topology and higher node supports than others.

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Plasmid stability is enhanced by higher-frequency pulses of positive selection.

Publications

Plasmid stability is enhanced by higher-frequency pulses of positive selection.

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