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

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 s...

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Autores principales:	James P J Hall, Rosanna C T Wright, Ellie Harrison, Katie J Muddiman, A Jamie Wood, Steve Paterson, Michael A Brockhurst
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/e7b6d25f6bc941739af7e8d0c266d785
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spelling	oai:doaj.org-article:e7b6d25f6bc941739af7e8d0c266d7852021-12-02T19:54:27ZPlasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.1544-91731545-788510.1371/journal.pbio.3001225https://doaj.org/article/e7b6d25f6bc941739af7e8d0c266d7852021-10-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001225https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Plasmids 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 Pseudomonas fluorescens 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 PFLU4242, 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.James P J HallRosanna C T WrightEllie HarrisonKatie J MuddimanA Jamie WoodSteve PatersonMichael A BrockhurstPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 10, p e3001225 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 James P J Hall Rosanna C T Wright Ellie Harrison Katie J Muddiman A Jamie Wood Steve Paterson Michael A Brockhurst Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
description	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 Pseudomonas fluorescens 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 PFLU4242, 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.
format	article
author	James P J Hall Rosanna C T Wright Ellie Harrison Katie J Muddiman A Jamie Wood Steve Paterson Michael A Brockhurst
author_facet	James P J Hall Rosanna C T Wright Ellie Harrison Katie J Muddiman A Jamie Wood Steve Paterson Michael A Brockhurst
author_sort	James P J Hall
title	Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
title_short	Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
title_full	Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
title_fullStr	Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
title_full_unstemmed	Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
title_sort	plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/e7b6d25f6bc941739af7e8d0c266d785
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Plasmid fitness costs are caused by specific genetic conflicts enabling resolution by compensatory mutation.

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