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Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host.

ABSTRACT: Plasmids are autonomously replicating sequences that help cells adapt to diverse stresses. Theta plasmids are the most frequent plasmid class in enterobacteria. They co-opt two host replication mechanisms: replication at oriC, a DnaA-dependent pathway leading to replisome assembly (theta class A), and replication fork restart, a PriA-dependent pathway leading to primosome assembly through primer extension and D-loop formation (theta classes B, C, and D). To ensure autonomy from the host's replication and to facilitate copy number regulation, theta plasmids have unique mechanisms of replication initiation at the plasmid origin of replication (ori). Tight plasmid copy number regulation is essential because of the major and direct impact plasmid gene dosage has on gene expression. The timing of plasmid replication and segregation are also critical for optimizing plasmid gene expression. Therefore, we propose that plasmid replication needs to be understood in its biological context, where complex origins of replication (redundant origins, mosaic and cointegrated replicons), plasmid segregation, and toxin-antitoxin systems are often present. Highlighting their tight functional integration with ori function, we show that both partition and toxin-antitoxin systems tend to be encoded in close physical proximity to the ori in a large collection of Escherichia coli plasmids. We also propose that adaptation of plasmids to their host optimizes their contribution to the host's fitness while restricting access to broad genetic diversity, and we argue that this trade-off between adaptation to host and access to genetic diversity is likely a determinant factor shaping the distribution of replicons in populations of enterobacteria.

SUBMITTER: Kim JW

PROVIDER: S-EPMC7724965 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host.

Kim Jay W JW Bugata Vega V Cortés-Cortés Gerardo G Quevedo-Martínez Giselle G Camps Manel M

EcoSal Plus 20201101 1

Plasmids are autonomously replicating sequences that help cells adapt to diverse stresses. Theta plasmids are the most frequent plasmid class in enterobacteria. They co-opt two host replication mechanisms: replication at <i>oriC</i>, a DnaA-dependent pathway leading to replisome assembly (theta class A), and replication fork restart, a PriA-dependent pathway leading to primosome assembly through primer extension and D-loop formation (theta classes B, C, and D). To ensure autonomy from the host's ...[more]

PMID: 33210586

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Project description:UnlabelledPromiscuous plasmids replicate in a wide range of bacteria and therefore play a key role in the dissemination of various host-beneficial traits, including antibiotic resistance. Despite the medical relevance, little is known about the evolutionary dynamics through which drug resistance plasmids adapt to new hosts and thereby persist in the absence of antibiotics. We previously showed that the incompatibility group P-1 (IncP-1) minireplicon pMS0506 drastically improved its stability in novel host Shewanella oneidensis MR-1 after 1,000 generations under antibiotic selection for the plasmid. The only mutations found were those affecting the N terminus of the plasmid replication initiation protein TrfA1. Our aim in this study was to gain insight into the dynamics of plasmid evolution. Changes in stability and genotype frequencies of pMS0506 were monitored in evolving populations of MR-1 (pMS0506). Genotypes were determined by sequencing trfA1 amplicons from individual clones and by 454 pyrosequencing of whole plasmids from entire populations. Stability of pMS0506 drastically improved by generation 200. Many evolved plasmid genotypes with point mutations as well as in-frame and frameshift deletions and duplications in trfA1 were observed in all lineages with both sequencing methods. Strikingly, multiple genotypes were simultaneously present at high frequencies (>10%) in each population. Their relative abundances changed over time, but after 1,000 generations only one or two genotypes dominated the populations. This suggests that hosts with different plasmid genotypes were competing with each other, thus affecting the evolutionary trajectory. Plasmids can thus rapidly improve their stability, and clonal interference plays a significant role in plasmid-host adaptation dynamics.ImportancePromiscuous plasmids play an important role in the spread of antibiotic resistance and many other traits between closely and distantly related bacteria. However, little is known about the dynamics by which these broad-host-range antibiotic resistance plasmids adapt to novel bacteria and thereby become more persistent, even in the absence of antibiotics. In this study, we show that after no more than 200 generations of growth in the presence of antibiotics, a plasmid that was initially poorly maintained in a novel bacterial host evolved to become drastically more persistent in the absence of antibiotics. In each of the evolving populations, an unexpectedly large number of bacterial variants arose with distinct mutations in the plasmid's replication initiation protein. Our results suggest that clonal interference, characterized by competition between variant clones in a population, plays a major role in the evolution of the persistence of drug resistance.

Dataset Information

Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host.

Publications

Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host.

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