Abstract
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.
Highlights
Prokaryotes, both bacteria and archaea, have remarkably plastic genomes because they can acquire genetic information at high rates by horizontal transfer from other prokaryotes
If we are correct in assuming homology between conjugative systems in integrative conjugative elements (ICE) and plasmids, we should be able to detect a large fraction of ICEs in prokaryotic genomes using information on proteins involved in plasmid conjugation
ICEs are more numerous than conjugative plasmids While few ICEs have been experimentally studied in terms of conjugation, we found large numbers of them in the genomes of prokaryotes
Summary
Prokaryotes, both bacteria and archaea, have remarkably plastic genomes because they can acquire genetic information at high rates by horizontal transfer from other prokaryotes. This allows them to adapt rapidly to specific niches and results in large differences in gene repertoires among closely related strains [1,2,3]. Natural transformation is controlled by the receptor cell and mostly implicated in DNA transfer within species leading to allelic recombination [4] Both transduction and conjugation are more invasive, since the recipient has little control over both processes which change gene repertoires dramatically and allow transfer between distant lineages. Conjugative elements are known for encoding other adaptive traits such as toxins, transporters and many secreted proteins including enzymes of industrial interest [11,12]
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