Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation



Hall, James PJ ORCID: 0000-0002-4896-4592, Wright, Rosanna CT, Harrison, Ellie, Muddiman, Katie J, Wood, A Jamie, Paterson, Steve ORCID: 0000-0002-1307-2981 and Brockhurst, Michael A
(2021) Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation. PLOS Biology, 19 (10). e3001225-e3001225.

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Abstract

<jats:p>Plasmids play an important role in bacterial genome evolution by transferring genes between lineages. Fitness costs associated with plasmid carriage are expected to be a barrier to gene exchange, but the causes of plasmid fitness costs are poorly understood. Single compensatory mutations are often sufficient to completely ameliorate plasmid fitness costs, suggesting that such costs are caused by specific genetic conflicts rather than generic properties of plasmids, such as their size, metabolic burden, or gene expression level. By combining the results of experimental evolution with genetics and transcriptomics, we show here that fitness costs of 2 divergent large plasmids in <jats:italic>Pseudomonas fluorescens</jats:italic> are caused by inducing maladaptive expression of a chromosomal tailocin toxin operon. Mutations in single genes unrelated to the toxin operon, and located on either the chromosome or the plasmid, ameliorated the disruption associated with plasmid carriage. We identify one of these compensatory loci, the chromosomal gene <jats:italic>PFLU4242</jats:italic>, as the key mediator of the fitness costs of both plasmids, with the other compensatory loci either reducing expression of this gene or mitigating its deleterious effects by up-regulating a putative plasmid-borne ParAB operon. The chromosomal mobile genetic element Tn6291, which uses plasmids for transmission, remained up-regulated even in compensated strains, suggesting that mobile genetic elements communicate through pathways independent of general physiological disruption. Plasmid fitness costs caused by specific genetic conflicts are unlikely to act as a long-term barrier to horizontal gene transfer (HGT) due to their propensity for amelioration by single compensatory mutations, helping to explain why plasmids are so common in bacterial genomes.</jats:p>

Item Type: Article
Uncontrolled Keywords: Chromosomes, Bacterial, Pseudomonas fluorescens, Evolution, Molecular, Transcription, Genetic, Gene Expression Regulation, Bacterial, Up-Regulation, Conjugation, Genetic, Mutation, Plasmids, Models, Biological, Genetic Fitness
Divisions: Faculty of Health and Life Sciences
Faculty of Health and Life Sciences > Institute of Infection, Veterinary and Ecological Sciences
Depositing User: Symplectic Admin
Date Deposited: 02 Nov 2021 10:56
Last Modified: 18 Jan 2023 21:25
DOI: 10.1371/journal.pbio.3001225
Open Access URL: http://doi.org/10.1371/journal.pbio.3001225
Related URLs:
URI: https://livrepository.liverpool.ac.uk/id/eprint/3142485