The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation

The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation.

Guglielmini J, Quintais L, Garcillán-Barcia MP, de la Cruz F, Rocha EPC (2011)

PLoS Genet 7(8): e1002222. doi:10.1371/journal.pgen.100222210.1371/journal.pgen.1002222

Scheme of some essential interactions in the process of ICEs movement.

The integration/excision reaction (1) occurs by recombination across two recombination sites (yellow squares) located at the termini of the inserted element. As a result, a circular (most commonly non-replicating) DNA molecule is produced. Conjugation (2) is carried out by mobility systems. The relaxase (red circle) cleaves a specific site within oriT, and this step starts conjugation. The DNA strand that contains the relaxase protein covalently bound to its 5′-end is displaced by an ongoing conjugative DNA replication process (dotted lines). The relaxase interacts with the T4CP (green oval) and then with other components of the T4SS (blue rectangle). As a result, the relaxase-DNA complex is transported to the recipient cell [13]. Since ICEs are supposed not to replicate autonomously, the process terminates necessarily by integration of the transferred DNA circle in the recipient chromosome.

Horizontal gene transfer shapes the genomes of prokaryotes by allowing rapid acquisition of novel adaptive functions. Conjugation allows the broadest range and the highest gene transfer input per transfer event. While conjugative plasmids have been studied for decades, the number and diversity of integrative conjugative elements (ICE) in prokaryotes remained unknown. We defined a large set of protein profiles of the conjugation machinery to scan over 1,000 genomes of prokaryotes. We found 682 putative conjugative systems among all major phylogenetic clades and showed that ICEs are the most abundant conjugative elements in prokaryotes. Nearly half of the genomes contain a type IV secretion system (T4SS), with larger genomes encoding more conjugative systems. Surprisingly, almost half of the chromosomal T4SS lack co-localized relaxases and, consequently, might be devoted to protein transport instead of conjugation. This class of elements is preponderant among small genomes, is less commonly associated with integrases, and is rarer in plasmids. ICEs and conjugative plasmids in proteobacteria have different preferences for each type of T4SS, but all types exist in both chromosomes and plasmids. Mobilizable elements outnumber self-conjugative elements in both ICEs and plasmids, which suggests an extensive use of T4SS in trans. Our evolutionary analysis indicates that switch of plasmids to and from ICEs were frequent and that extant elements began to differentiate only relatively recently. According to the present results, ICEs are the most abundant conjugative elements in practically all prokaryotic clades and might be far more frequently domesticated into non-conjugative protein transport systems than previously thought. While conjugative plasmids and ICEs have different means of genomic stabilization, their mechanisms of mobility by conjugation show strikingly conserved patterns, arguing for a unitary view of conjugation in shaping the genomes of prokaryotes by horizontal gene transfer.

Author Summary
Some mobile genetic elements spread genetic information horizontally between prokaryotes by conjugation, a mechanism by which DNA is transferred directly from one cell to the other. Among the processes allowing genetic transfer between cells, conjugation is the one allowing the simultaneous transfer of larger amounts of DNA and between the least related cells. As such, conjugative systems are key players in horizontal transfer, including the transfer of antibiotic resistance to and between many human pathogens. Conjugative systems are encoded both in plasmids and in chromosomes. The latter are called Integrative Conjugative Elements (ICE); and their number, identity, and mechanism of conjugation were poorly known. We have developed an approach to identify and characterize these elements and found more ICEs than conjugative plasmids in genomes. While both ICEs and plasmids use similar conjugative systems, there are remarkable preferences for some systems in some elements. Our evolutionary analysis shows that plasmid conjugative systems have often given rise to ICEs and vice versa. Therefore, ICEs and conjugative plasmids should be regarded as one and the same, the differences in their means of existence in cells probably the result of different requirements for stabilization and/or transmissibility of the genetic information they contain.

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