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A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group.

ABSTRACT: Integrons facilitate the evolution of complex phenotypes by physical and transcriptional linkage of genes. They can be categorized as chromosomal integrons (CIs) or mobile resistance integrons (MRIs). The significance of MRIs for the problem of multiple antibiotic resistance is well established. CIs are more widespread, but their only demonstrated significance is as a reservoir of gene cassettes for MRIs. In characterizing CIs associated with Pseudomonas, we discovered a subfamily of insertion sequences, termed the IS1111-attC group, that insert into the recombination sites of gene cassettes (attC site) by site-specific recombination. IS1111-attC elements appear to have recently spread from Pseudomonas species to clinical class 1 integrons. Such elements are expected to significantly impact integrons. To explore this further, we examined CIs in 24 strains representing multiple levels of evolutionary divergence within the genus Pseudomonas. Cassette arrays frequently had a degenerated "footprint" of an IS1111-attC group element at their terminus and in three cases were occupied by multiple functional IS1111-attC elements. Within Pseudomonas spp. the IS-integron interaction appears to follow an evolutionarily rapid cycle of infection, expansion, and extinction. The final outcome is extinction of the IS element and modification of the right-hand boundary of the integron. This system represents an unusual example of convergent evolution whereby heterologous families of site-specific recombinases of distinct genetic elements have adopted the same target site. The interactions described here represent a model for evolutionary processes that offer insights to a number of aspects of the biology of integrons and other mosaic genetic elements.

SUBMITTER: Tetu SG

PROVIDER: S-EPMC2447020 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group.

Tetu Sasha G SG Holmes Andrew J AJ

Journal of bacteriology 20080516 14

Integrons facilitate the evolution of complex phenotypes by physical and transcriptional linkage of genes. They can be categorized as chromosomal integrons (CIs) or mobile resistance integrons (MRIs). The significance of MRIs for the problem of multiple antibiotic resistance is well established. CIs are more widespread, but their only demonstrated significance is as a reservoir of gene cassettes for MRIs. In characterizing CIs associated with Pseudomonas, we discovered a subfamily of insertion s ...[more]

PMID: 18487340

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Project description:BACKGROUND:Integrons are genetic elements able to integrate and disseminate genes as cassettes by a site-specific recombination mechanism. These elements contain a gene coding for an integrase that carries out recombination by interacting with two different target sites; the attI site in cis with the integrase and the palindromic attC site of a gene cassette. Integron integrases (IntIs) bind specifically to the bottom strand of attC sites. The extrahelical bases resulting from folding of attC bottom strands are important for the recognition by integrases. These enzymes are directly involved in the accumulation and formation of new cassette arrangements in the variable region of integrons. Thus, it is important to better understand interactions between IntIs and their substrates. RESULTS:We compared the ability of five IntIs to carry out excision of several cassettes flanked by different attC sites. The results showed that for most cassettes, IntI1 was the most active integrase. However, IntI2*179E and SonIntIA could easily excise cassettes containing the attCdfrA1 site located upstream, whereas IntI1 and IntI3 had only a weak excision activity for these cassettes. Analysis of the secondary structure adopted by the bottom strand of attCdfrA1 has shown that the identity of the extrahelical bases and the distance between them (A-N7-8-C) differ from those of attCs contained in the cassettes most easily excisable by IntI1 (T-N6-G). We used the attCdfrA1 site upstream of the sat2 gene cassette as a template and varied the identity and spacing between the extrahelical bases in order to determine how these modifications influence the ability of IntI1, IntI2*179E, IntI3 and SonIntIA to excise cassettes. Our results show that IntI1 is more efficient in cassette excision using T-N6-G or T-N6-C attCs while IntI3 recognizes only a limited range of attCs. IntI2*179E and SonIntIA are more tolerant of changes to the identity and spacing of extrahelical bases. CONCLUSIONS:This study provides new insights into the factors that influence the efficiency of cassette excision by integron integrases. It also suggests that IntI2 and SonIntIA have an evolutionary path that is different from IntI1 and IntI3, in their ability to recognize and excise cassettes.

Dataset Information

A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group.

Publications

A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group.

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