Originally published as Genetics Published Articles Ahead of Print on February 2, 2009.

Genetics, Vol. 181, 1557-1566, April 2009, Copyright © 2009
doi:10.1534/genetics.108.095190

The Decay of the Chromosomally Encoded ccdO157 Toxin–Antitoxin System in the Escherichia coli Species

Natacha Mine, Julien Guglielmini, Myriam Wilbaux and Laurence Van Melderen1

Laboratoire de Génétique et Physiologie Bactérienne, Institut de Biologie et Médecine Moléculaires, Faculté des Sciences, Université Libre de Bruxelles, 6041 Gosselies, Belgium

1 Corresponding author: Laboratoire de Génétique et Physiologie Bactérienne, Institut de Biologie et Médecine Moléculaires, Faculté des Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, B:6041 Gosselies, Belgium.
E-mail: lvmelder{at}ulb.ac.be

The origin and the evolution of toxin–antitoxin (TA) systems remain to be uncovered. TA systems are abundant in bacterial chromosomes and are thought to be part of the flexible genome that originates from horizontal gene transfer. To gain insight into TA system evolution, we analyzed the distribution of the chromosomally encoded ccdO157 system in 395 natural isolates of Escherichia coli. It was discovered in the E. coli O157:H7 strain in which it constitutes a genomic islet between two core genes (folA and apaH). Our study revealed that the folA–apaH intergenic region is plastic and subject to insertion of foreign DNA. It could be composed (i) of a repetitive extragenic palindromic (REP) sequence, (ii) of the ccdO157 system or subtle variants of it, (iii) of a large DNA piece that contained a ccdAO157 antitoxin remnant in association with ORFs of unknown function, or (iv) of a variant of it containing an insertion sequence in the ccdAO157 remnant. Sequence analysis and functional tests of the ccdO157 variants revealed that 69% of the variants were composed of an active toxin and antitoxin, 29% were composed of an active antitoxin and an inactive toxin, and in 2% of the cases both ORFs were inactive. Molecular evolution analysis showed that ccdBO157 is under neutral evolution, suggesting that this system is devoid of any biological role in the E. coli species.