Belt and braces: Two escape ways to maintainthe cassette reservoir of large chromosomalintegrons

PLOS GENETICS

Egill Richard, Baptiste Darracq, Eloi Littner, Gael A. Millot, Valentin Conte, Thomas Cokelaer, Jan Engelstadter, Eduardo P. C. Rocha, Didier Mazel*, Celine Loot*

Abstract

Integrons are adaptive devices that capture, stockpile, shuffle and express gene cassettes

thereby sampling 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 associated

with a fitness defect. Here, we question the evolutionary sustainability of this apparently

counter selected genetic context. Through experimental evolution, we find that the integrase is rapidly inactivated and that the inverted SCI can recover its original orientation by homologous recombination between two insertion sequences (ISs) present in the array. These two outcomes of SCI inversion restore the normal growth and prevent the loss of cassettes, enabling SCIs to retain their roles as reservoirs of functions. These results illustrate a nice interplay between gene orientation, genome rearrangement, bacterial fitness and demonstrate how integrons can benefit from their embedded ISs.

More information at DOI: https://doi.org/10.1371/journal.pgen.1011231