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

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          Abstract

          <p class="first" id="d4417315e103">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. </p>

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          Most cited references32

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          Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq.

          Next-generation DNA sequencing (NGS) can be used to reconstruct eco-evolutionary population dynamics and to identify the genetic basis of adaptation in laboratory evolution experiments. Here, we describe how to run the open-source breseq computational pipeline to identify and annotate genetic differences found in whole-genome and whole-population NGS data from haploid microbes where a high-quality reference genome is available. These methods can also be used to analyze mutants isolated in genetic screens and to detect unintended mutations that may occur during strain construction and genome editing.
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            Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations

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              Conjugative plasmids: vessels of the communal gene pool.

              Comparative whole-genome analyses have demonstrated that horizontal gene transfer (HGT) provides a significant contribution to prokaryotic genome innovation. The evolution of specific prokaryotes is therefore tightly linked to the environment in which they live and the communal pool of genes available within that environment. Here we use the term supergenome to describe the set of all genes that a prokaryotic 'individual' can draw on within a particular environmental setting. Conjugative plasmids can be considered particularly successful entities within the communal pool, which have enabled HGT over large taxonomic distances. These plasmids are collections of discrete regions of genes that function as 'backbone modules' to undertake different aspects of overall plasmid maintenance and propagation. Conjugative plasmids often carry suites of 'accessory elements' that contribute adaptive traits to the hosts and, potentially, other resident prokaryotes within specific environmental niches. Insight into the evolution of plasmid modules therefore contributes to our knowledge of gene dissemination and evolution within prokaryotic communities. This communal pool provides the prokaryotes with an important mechanistic framework for obtaining adaptability and functional diversity that alleviates the need for large genomes of specialized 'private genes'.
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                Author and article information

                Journal
                Microbiology
                Microbiology Society
                1350-0872
                1465-2080
                October 15 2019
                Affiliations
                [1 ] Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK
                [2 ] Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK
                [3 ] Department of Evolution, Ecology and Behaviour, University of Liverpool, Crown Street, Liverpool, L69 7ZB, UK
                Article
                10.1099/mic.0.000862
                31613206
                1a9c3057-a185-4f36-aca5-b97fccd9984e
                © 2019
                History

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