Genetic drivers of chromosomal integron stability

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Richard, Egill | Darracq, Baptiste | Littner, Eloi | Vit, Claire | Whiteway, Clémence | Bos, Julia | Fournes, Florian | Garriss, Geneviève | Conte, Valentin | Lapaillerie, Delphine | Parissi, Vincent | Rousset, François | Skovgaard, Ole | Bikard, David | Rocha, Eduardo, P C | Mazel, Didier | Loot, Céline

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The integron is a bacterial recombination system that allows acquisition, stockpiling and expression of promoterless genes embedded in cassettes. Some integrons, like the one found in the second chromosome of Vibrio cholerae, can be particularly massive and contain hundreds of non-expressed cassettes. It is unclear how such genetic structures can be stabilized in bacterial genomes. Here, we reveal that the orientation of integrons toward replication within bacterial chromosomes is essential to their stability. Indeed, we show that upon inversion of the V. cholerae chromosomal integron, its plasticity is dramatically increased. This correlates with a strong growth defect which we show is mostly due to the excision of a particular type of cassettes bearing their own promoter and encoding toxin-antitoxin systems. This so called "abortive excision" of toxin-antitoxin systems can prevent the inversion of chromosomal integrons and the associated extensive loss of cassettes. Our analysis of the available sedentary chromosomal integrons in genome database show a robust correlation between the size of the cassette array and the number of toxin-antitoxin cassettes. This study thus provides a striking example of the relationship between genome organization, genome stability, and an emerging property of toxin-antitoxin systems.

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