The chromosomal organization of horizontal gene transfer in bacteria

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

doi:10.1038/s41467-017-00808-w

Jean Cury, Eduardo P. C. Rocha + Show 2 more

Open Access

https://doi.org/10.1038/s41467-017-00808-w

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Abstract

Bacterial adaptation is accelerated by the acquisition of novel traits through horizontal gene transfer, but the integration of these genes affects genome organization. We found that transferred genes are concentrated in only ~1% of the chromosomal regions (hotspots) in 80 bacterial species. This concentration increases with genome size and with the rate of transfer. Hotspots diversify by rapid gene turnover; their chromosomal distribution depends on local contexts (neighboring core genes), and content in mobile genetic elements. Hotspots concentrate most changes in gene repertoires, reduce the trade-off between genome diversification and organization, and should be treasure troves of strain-specific adaptive genes. Most mobile genetic elements and antibiotic resistance genes are in hotspots, but many hotspots lack recognizable mobile genetic elements and exhibit frequent homologous recombination at flanking core genes. Overrepresentation of hotspots with fewer mobile genetic elements in naturally transformable bacteria suggests that homologous recombination and horizontal gene transfer are tightly linked in genome evolution.

Highlights

Chromosomes are organized to favor the interactions of DNA with the cellular machinery[8]
As these results show that prophages and Integrative conjugative elements (ICEs) have different distribution patterns, we quantified the frequency of co-occurrence of different Mobile genetic elements (MGEs) and mobility-associated proteins (MAPs) in the same hotspots
Our study showed high concentration of HTgenes in a small number of locations in the chromosomes of many bacterial species

Summary

Introduction

Chromosomes are organized to favor the interactions of DNA with the cellular machinery[8]. At a more global level, early-replicating regions are enriched in highly expressed genes in fast-growing bacteria to enjoy replication-associated gene dosage, creating a negative gradient of expression along the axis from the origin (ori) to the terminus (ter) of replication (ori->ter)[10, 11] These organizational traits can be disrupted by the integration of novel genetic information. The frequency of integration of prophages in the genome of Escherichia coli increases along the ori->ter axis[13] The results of these studies suggest that the fitness effects of HGT in terms of chromosome organization depend on the specific site of integration. Some strains of E. coli have up to 18 prophages[17], and Mesorhizobium loti encodes one ~500 kb ICE18 The integration of these large MGEs changes the chromosome size and may split adaptive genetic structures such as operons.

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