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ISME J. 2018 Dec;12(12):3014-3024. doi: 10.1038/s41396-018-0224-8. Epub 2018 Aug 10.

Integrative analysis of fitness and metabolic effects of plasmids in Pseudomonas aeruginosa PAO1.

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Department of Zoology, University of Oxford, Oxford, OX2 6GG, UK.
Department of Microbiology, Hospital Universitario Ramon y Cajal (IRYCIS) and Network Research Centre for Epidemiology and Public Health (CIBERESP), 28034, Madrid, Spain.
Department of Zoology, University of Oxford, Oxford, OX2 6GG, UK.
Department of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057, Zurich, Switzerland.
Swiss Institute of Bioinformatics, Quartier Sorge-Bâtiment Génopode, 1015, Lausanne, Switzerland.
Department of Zoology, University of Oxford, Oxford, OX2 6GG, UK.
Chemistry Research Laboratory, University of Oxford, Oxford, OX1 3TA, UK.
Leicester Institute of Structural and Chemical Biology and Department of Chemistry, University of Leicester, Leicester, LE1 7RH, UK.


Horizontal gene transfer (HGT) mediated by the spread of plasmids fuels evolution in prokaryotes. Although plasmids provide bacteria with new adaptive genes, they also produce physiological alterations that often translate into a reduction in bacterial fitness. The fitness costs associated with plasmids represent an important limit to plasmid maintenance in bacterial communities, but their molecular origins remain largely unknown. In this work, we combine phenomics, transcriptomics and metabolomics to study the fitness effects produced by a collection of diverse plasmids in the opportunistic pathogen Pseudomonas aeruginosa PAO1. Using this approach, we scan the physiological changes imposed by plasmids and test the generality of some main mechanisms that have been proposed to explain the cost of HGT, including increased biosynthetic burden, reduced translational efficiency, and impaired chromosomal replication. Our results suggest that the fitness effects of plasmids have a complex origin, since none of these mechanisms could individually provide a general explanation for the cost of plasmid carriage. Interestingly, our results also showed that plasmids alter the expression of a common set of metabolic genes in PAO1, and produce convergent changes in host cell metabolism. These surprising results suggest that there is a common metabolic response to plasmids in P. aeruginosa PAO1.

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