Systematic transcriptome analysis allows the identification of new type I and type II Toxin/Antitoxin systems located in the superintegron of Vibrio cholerae

Krin, Evelyne; Baharoglu, Zeynep; Sismeiro, Odile; Varet, Hugo; Coppée, Jean‐Yves; Mazel, Didier

doi:10.1016/j.resmic.2022.103997

Cited by 9 publications

(16 citation statements)

References 51 publications

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“…When the expression of the gene pair is stopped, the antitoxin is degraded, resulting in cell death or growth arrest 24 . In V. cholerae N16961, out of the 20 TA systems that have been identified, 19 are concentrated within the SI 23,25 (Fig 5a). We hypothesized that the increased excision of the cassettes encoding TA systems, alongside all the non-expressed cassettes, could be at the origin of the increased growth arrest and cell death observed in the SI Inv strain.…”

Section: Fitness Defect In the Si Inverted Strain Is Largely Explaine...mentioning

confidence: 99%

“…To reduce the number of false positives, we evaluated TASmania's performance on the genome of Vibrio cholerae N16961's secondary chromosome, known to harbor 19 TA systems 23,25 , all located within the SI. We observed that applying an e-value threshold of 10 -3 allowed to keep all the hits corresponding to characterized TA systems (as described by Iqbal and coll.…”

Section: Toxin and Antitoxin Predictionmentioning

confidence: 99%

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Cassette recombination dynamics within chromosomal integrons are regulated by toxin–antitoxin systems

Richard

Darracq

Littner

et al. 2022

Preprint

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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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Section: Fitness Defect In the Si Inverted Strain Is Largely Explaine...mentioning

confidence: 99%

Section: Toxin and Antitoxin Predictionmentioning

confidence: 99%

Cassette recombination dynamics within chromosomal integrons are regulated by toxin–antitoxin systems

Richard

Darracq

Littner

et al. 2022

Preprint

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“…Among the cassettes of SCIs, a distinct type is notable, encoding toxin-antitoxin (TA) systems and containing their own promoter (15)(16)(17)(18). TA systems encode a stable toxin that inhibits an essential cellular process and an unstable antitoxin that counteracts its cognate toxin.…”

Section: Introductionmentioning

confidence: 99%

Cassette recombination dynamics within chromosomal integrons are regulated by toxin-antitoxin systems

Richard,

Darracq,

Littner

et al. 2024

Sci. Adv.

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Integrons are adaptive bacterial devices that rearrange promoter-less gene cassettes into variable ordered arrays under stress conditions, thereby sampling combinatorial phenotypic diversity. Chromosomal integrons often carry hundreds of silent gene cassettes, with integrase-mediated recombination leading to rampant DNA excision and integration, posing a potential threat to genome integrity. How this activity is regulated and controlled, particularly through selective pressures, to maintain such large cassette arrays is unknown. Here, we show a key role of promoter-containing toxin-antitoxin (TA) cassettes as systems that kill the cell when the overall cassette excision rate is too high. These results highlight the importance of TA cassettes regulating the cassette recombination dynamics and provide insight into the evolution and success of integrons in bacterial genomes.

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“…Hence, re-inversion of the SCI brings the attC bs back to their native and less recombinogenic state that is on the leading strand template. The portion of the re-inverted array contains ten non-duplicated TA systems versus only three in the other part (Krin et al, 2023). Indeed, the increased probability of excision of a TA cassette leading to cell death or cell cycle arrest must be a strong selective pressure for the re-inversion of the section of the array that concentrates the most TA cassettes.…”

Section: Discussionmentioning

confidence: 99%

Belt and braces: two escape ways to maintain the cassette reservoir of large chromosomal integrons

Richard,

Darracq,

Littner

et al. 2023

Preprint

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Integrons are powerful adaptive devices that can capture, stockpile, shuffle and express gene cassettes to sample combinatorial phenotypic diversity. Some integrons called sedentary chromosomal integrons (SCIs) can be massive structures containing hundreds of cassettes. Since most of these cassettes are non-expressed, it is not clear how they remain stable over long evolutionary timescales. Recently, it was found that the experimental inversion of the SCI of Vibrio cholerae led to a dramatic increase of the cassette excision rate linked to a fitness defect. Here, we investigate the outcome of such an active SCI through experimental evolution. We find that the integrase is rapidly inactivated. Strikingly, we also find that the inverted SCI can in part recover its original, more stable orientation by homologous recombination between two insertion sequences (ISs) present in the array. These two possible outcomes of SCI inversion both restore the normal growth and prevent the massive and rapid loss of cassettes, enabling SCIs to retain their roles as reservoirs of valuable functions. These results illustrate a nice interplay between gene orientation, genome rearrangement, bacterial fitness and show how integrons can benefit from their embedded ISs.

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Systematic transcriptome analysis allows the identification of new type I and type II Toxin/Antitoxin systems located in the superintegron of Vibrio cholerae

Cited by 9 publications

References 51 publications

Cassette recombination dynamics within chromosomal integrons are regulated by toxin–antitoxin systems

Cassette recombination dynamics within chromosomal integrons are regulated by toxin–antitoxin systems

Cassette recombination dynamics within chromosomal integrons are regulated by toxin-antitoxin systems

Belt and braces: two escape ways to maintain the cassette reservoir of large chromosomal integrons

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