Selective Pressures to Maintain Attachment Site Specificity of Integrative and Conjugative Elements

Kayla L Menard,Alan D Grossman,Diarmaid Hughes

doi:10.1371/journal.pgen.1003623

Kayla L Menard, Alan D Grossman + Show 1 more

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https://doi.org/10.1371/journal.pgen.1003623

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Journal: PLoS Genetics	Publication Date: Jul 18, 2013
Citations: 79	License type: CC BY 4.0

Affiliation: Massachusetts Institute of Technology

Abstract

Integrative and conjugative elements (ICEs) are widespread mobile genetic elements that are usually found integrated in bacterial chromosomes. They are important agents of evolution and contribute to the acquisition of new traits, including antibiotic resistances. ICEs can excise from the chromosome and transfer to recipients by conjugation. Many ICEs are site-specific in that they integrate preferentially into a primary attachment site in the bacterial genome. Site-specific ICEs can also integrate into secondary locations, particularly if the primary site is absent. However, little is known about the consequences of integration of ICEs into alternative attachment sites or what drives the apparent maintenance and prevalence of the many ICEs that use a single attachment site. Using ICEBs1, a site-specific ICE from Bacillus subtilis that integrates into a tRNA gene, we found that integration into secondary sites was detrimental to both ICEBs1 and the host cell. Excision of ICEBs1 from secondary sites was impaired either partially or completely, limiting the spread of ICEBs1. Furthermore, induction of ICEBs1 gene expression caused a substantial drop in proliferation and cell viability within three hours. This drop was dependent on rolling circle replication of ICEBs1 that was unable to excise from the chromosome. Together, these detrimental effects provide selective pressure against the survival and dissemination of ICEs that have integrated into alternative sites and may explain the maintenance of site-specific integration for many ICEs.

Highlights

Integrative and conjugative elements (ICEs, known as conjugative transposons) are mobile genetic elements that encode conjugation machinery that mediates their transfer from cell to cell
Little is known about the consequences of a site-specific ICE integrating into an alternative attachment site, or the selective pressures that maintain the specificity of integration for ICEs with a single attachment site
We found that integration of ICEBs1, a site-specific ICE in Bacillus subtilis, into alternative attachment sites was detrimental to both ICEBs1 and the host cell

Summary

Introduction

Integrative and conjugative elements (ICEs, known as conjugative transposons) are mobile genetic elements that encode conjugation machinery that mediates their transfer from cell to cell. Most characterized ICEs were identified because they carry additional genes that confer phenotypes to the host cell. These can be genes involved in pathogenesis, symbiosis, and antibiotic resistances, among others {reviewed in [1]}. ICEs are typically found integrated in the host bacterial chromosome and can excise to form a circular product that is the substrate for conjugation. Their ability to spread to other organisms through conjugation makes ICEs important agents of horizontal gene transfer in bacteria, and they appear to be more prevalent than plasmids [2]. ICEs can facilitate transfer (mobilization) of other genetic elements [1,3,4]

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