Chromosomal replication dynamics and interaction with the β sliding clamp determine orientation of bacterial transposable elements

Gomez, MJ; Díaz-Maldonado, H; Gonzalez Tortuero, E; López de Saro, FJ

Abstract

Insertion sequences (ISs) are small transposable elements widespread in bacterial genomes, where they play an essential role in chromosome evolution by stimulating recombination and genetic flow. Despite their ubiquity, it is unclear how ISs interact with the host. Here, we report a survey of the orientation patterns of ISs in bacterial chromosomes with the objective of gaining insight into the interplay between ISs and host chromosomal functions. We find that a significant fraction of IS families present a consistent and family-specific orientation bias with respect to chromosomal DNA replication, especially in Firmicutes. Additionally, we find that the transposases of up to nine different IS families with different transposition pathways interact with the β sliding clamp, an essential replication factor, suggesting that this is a widespread mechanism of interaction with the host. Although we find evidence that the interaction with the β sliding clamp is common to all bacterial phyla, it also could explain the observed strong orientation bias found in Firmicutes, because in this group β is asymmetrically distributed during synthesis of the leading or lagging strands. Besides the interaction with the β sliding clamp, other asymmetries also play a role in the biased orientation of some IS families. The utilization of the highly conserved replication sliding clamps suggests a mechanism for host regulation of IS proliferation and also a universal platform for IS dispersal and transmission within bacterial populations and among phylogenetically distant species.

Citation

Gomez, M., Díaz-Maldonado, H., Gonzalez Tortuero, E., & López de Saro, F. (2014). Chromosomal replication dynamics and interaction with the β sliding clamp determine orientation of bacterial transposable elements. Genome Biology and Evolution, 6(3), 727-740. https://doi.org/10.1093/gbe/evu052

• Journal Article Type: Article
• Acceptance Date: Mar 4, 2014
• Publication Date: Mar 9, 2014
• Deposit Date: Feb 22, 2021
• Publicly Available Date: Feb 22, 2021
• Journal: Genome Biology and Evolution
• Publisher: Oxford University Press
• Volume: 6
• Issue: 3
• Pages: 727-740
• DOI: https://doi.org/10.1093/gbe/evu052
• Publisher URL: https://doi.org/10.1093/gbe/evu052
• Related Public URLs: http://gbe.oxfordjournals.org/
• Additional Information: Funders : Ministry of Economy and Competitiveness of the Spanish Government;Project Consolider Ingenio;FPI Predoctoral Fellowship from the Spanish Government;INTA Training Fellowship; Grant Number: CGL2010-17384; Grant Number: CSD2007-00005