Operon formation by insertion sequence IS3 in Escherichia coli

Abstract

Operons are a hallmark of the genomic and regulatory architecture of prokaryotes. However, the mechanism by which two genes placed far apart gradually come close and form operons remains to be elucidated. Here, we propose a new model of the origin of operons: Mobile genetic elements called insertion sequences can facilitate the formation of operons by consecutive insertion-deletion-excision reactions. This mechanism barely leaves traces of insertion sequences and is difficult to detect in evolution in nature. We performed, to the best of our knowledge, the first experimental demonstration of operon formation, as a proof of concept. The insertion sequence IS3 and the insertion sequence excision enhancer are genes found in a broad range of bacterial species. We introduced these genes into insertion sequence-less Escherichia coli and found that, supporting our hypothesis, the activity of the two genes altered the expression of genes surrounding IS3, closed a 2.7 kilobase pair gap between a pair of genes, and formed new operons. This study shows how insertion sequences can facilitate the rapid formation of operons through locally increasing the structural mutation rates and highlights how coevolution with mobile elements may shape the organization of prokaryotic genomes and gene regulation.

Beyond to the Stable: Role of the Insertion Sequences as Epidemiological Descriptors in Corynebacterium striatum

“…The adaptation and evolution of C. striatum can be explained by the insertion sequences. In Escherichia coli , it has been suggested that IS could be associated with the genome evolution, fitness, and the formation of new operons ( Gaffé et al, 2011 ; Consuegra et al, 2021 ; Kanai et al, 2021 ). This raises the question if the presence of IS would explain the transition of C. striatum lineages from normal microbiota to the generation of pathogenic lineages, and whether it would also be related to the role of the environment in the evolution of its pathogenicity.…”