Horizontal transfer of genomic islands (GEIs), that is, chromosomal regions encoding functions that can be advantageous for the host, plays a key role in bacterial evolution, but their mechanisms of transfer remained elusive for a long time. Recent data suggest that numerous GEIs belong to noncanonical classes of mobile genetic elements (MGEs) that can transfer by conjugation. Among them, the integrative and conjugative elements encode their own excision, conjugative transfer, and integration, whereas the integrative mobilizable elements are autonomous for excision and integration but require the conjugation machinery of helper elements to transfer. Others can self-transfer but require the recombination machinery of the recipient cell to integrate. All these MGEs evolve by acquisition, deletion, or exchange of modules, that is, groups of genes involved in the same function. Moreover, composite GEIs can result from the insertion of a MGE within another or from the site-specific integration of an incoming MGE into one of the recombination sites flanking a resident GEI (tandem accretion). Tandem accretion enables the cis-conjugative mobilization of highly degenerated and nonautonomous GEIs, the cis-mobilizable elements. All these mechanisms contribute to the plasticity and complex evolution of GEIs and explain the highly diverse tableau revealed by more and more genome comparisons.
Integrative and conjugative elements (ICEs), also called conjugative transposons, are genomic islands that excise, self-transfer by conjugation, and integrate in the genome of the recipient bacterium. The current investigation shows the intraspecies conjugative transfer of the first described ICEs in Streptococcus thermophilus, ICESt1 and ICESt3. Mitomycin C, a DNA-damaging agent, derepresses ICESt3 conjugative transfer almost 25-fold. The ICESt3 host range was determined using various members of the Firmicutes as recipients. Whereas numerous ICESt3 transconjugants of Streptococcus pyogenes and Enterococcus faecalis were recovered, only one transconjugant of Lactococcus lactis was obtained. The newly incoming ICEs, except the one from L. lactis, are site-specifically integrated into the 3 end of the fda gene and are still able to excise in these transconjugants. Furthermore, ICESt3 was retransferred from E. faecalis to S. thermophilus. Recombinant plasmids carrying different parts of the ICESt1 recombination module were used to show that the integrase gene is required for the site-specific integration and excision of the ICEs, whereas the excisionase gene is required for the site-specific excision only.Horizontal transfer of genomic islands plays a key role in bacterial evolution, leading to the acquisition of advantageous functions or to major modifications of the bacterial way of life (37, 38). However, the mechanism of their transfer and integration remains generally unknown. Recent in silico analyses revealed that numerous genomic islands could be integrative and conjugative elements (ICEs) or elements deriving from them (18,30,62,67) The ICEs, also called conjugative transposons, were defined as elements which encode their own excision, their transfer by conjugation, and their integration in a replicon of the recipient cell, whatever their specificity and their mechanism of integration and conjugation (18). Most of the ICEs encode a putative integrase belonging to the tyrosine recombinase family. This enzyme, generally associated with an excisionase, catalyzes the recombination between identical sequences carried by the attL and attR recombination sites flanking the element. This event leads to the excision of a circular form of the ICE harboring an attI site, resulting from the recombination between attL and attR sites, and to a chromosome carrying an empty attB site. After conjugative transfer, most of the ICEs integrate by site-specific recombination between identical sequences carried by the attI site and the attB site. The attB sites are generally located in the
SummaryGenomic islands, flanked by attachment sites, devoid of conjugation and recombination modules and related to the integrative and conjugative element (ICE) ICESt3, were previously found in Streptococcus thermophilus. Here, we show that ICESt3 transfers to a recipient harbouring a similar engineered genomic island, CIMEL3catR3, and integrates by site-specific recombination into its attachment sites, leading to their accretion. The resulting composite island can excise, showing that ICESt3 mobilizes CIMEL3catR3 in cis. ICESt3, CIMEL3catR3 and the whole composite element can transfer from the strain harbouring the composite structure. The ICESt3 transfer to a recipient bearing CIMEL3catR3 can also lead to retromobilization, i.e. its capture by the donor. This is the first demonstration of specific conjugative mobilization of a genomic island in cis and the first report of ICEmediated retromobilization. CIMEL3catR3 would be the prototype of a novel class of non-autonomous mobile elements (CIMEs: CIs mobilizable elements), which hijack the recombination and conjugation machinery of related ICEs to excise, transfer and integrate. Few genome analyses have shown that CIMEs could be widespread and have revealed internal repeats that could result from accretions in numerous genomic islands, suggesting that accretion and cis mobilization have a key role in evolution of genomic islands.
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