The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts.

Pedro H Oliveira,Marie Touchon,Eduardo P.C Rocha

doi:10.1093/nar/gku734

Pedro H Oliveira, Marie Touchon + Show 1 more

Open Access

https://doi.org/10.1093/nar/gku734

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Abstract

The roles of restriction-modification (R-M) systems in providing immunity against horizontal gene transfer (HGT) and in stabilizing mobile genetic elements (MGEs) have been much debated. However, few studies have precisely addressed the distribution of these systems in light of HGT, its mechanisms and its vectors. We analyzed the distribution of R-M systems in 2261 prokaryote genomes and found their frequency to be strongly dependent on the presence of MGEs, CRISPR-Cas systems, integrons and natural transformation. Yet R-M systems are rare in plasmids, in prophages and nearly absent from other phages. Their abundance depends on genome size for small genomes where it relates with HGT but saturates at two occurrences per genome. Chromosomal R-M systems might evolve under cycles of purifying and relaxed selection, where sequence conservation depends on the biochemical activity and complexity of the system and total gene loss is frequent. Surprisingly, analysis of 43 pan-genomes suggests that solitary R-M genes rarely arise from the degradation of R-M systems. Solitary genes are transferred by large MGEs, whereas complete systems are more frequently transferred autonomously or in small MGEs. Our results suggest means of testing the roles for R-M systems and their associations with MGEs.

Highlights

The flow of genetic information between bacterial cells by horizontal gene transfer (HGT) drives bacterial evolution [1,2] and restriction-modification (R-M) systems are key moderators of this process [3,4]
Type I systems are complex heterooligomers either comprising one DNA sequence specificity (S), two restriction endonuclease (REase) and two MTase subunits with restriction and modification activities, or two MTase and one S subunits with modification activity only
HMMbased methods are more sensitive [66], and we cannot exclude the possibility that we have under-estimated the number of Type IV REases

Summary

Introduction

The flow of genetic information between bacterial cells by horizontal gene transfer (HGT) drives bacterial evolution [1,2] and restriction-modification (R-M) systems are key moderators of this process [3,4]. They are thought to be ubiquitous in bacteria and archaea [5], and operate like many poison-antidote systems: they typically encode a methyltransferase (MTase) function that modifies a particular sequence and a restriction endonuclease (REase) function that cleaves a DNA when its recognition sequence is unmethylated [6,7,8]. Type IV ‘restriction systems’, as opposed to R-M systems, are composed of one or two REases that cleave modified recognition sites [12]

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