The chromosomal organization of horizontal gene transfer in bacteria

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.

PPanGGOLiN: depicting microbial diversity via a partitioned pangenome graph

“…To partition this graph, we established a statistical model taking into consideration that persistent genes share conserved genomic organizations along genomes [27] and that horizontally transferred genes (i.e. shell and cloud genes) tend to insert preferentially in a few chromosomal regions (hotspots) [28]. Thereby, PPanGGOLiN assumes that two gene families that are consistent neighbors in the graph are more likely to belong to the same partition.…”

“…the average number of adjacent edges between gene families of the same partition, is 2.80 for the persistent genome while the shell genome has a higher average degree (3.95, P=5.0e-6 with bilateral unpaired 2-sample Student's t test) and the cloud a lower one (1.97, P=3.3e-40 with the same test). The shell genome is the most diversified in terms of network topology with many interconnections between families reflecting a mosaic composition of regions from different HGT events [28]. The major part of the cloud has a shell-like graph topology with a large connected component containing 60% of the nodes.…”

ACI‐1 beta‐lactamase is widespread across human gut microbiomes in Negativicutes due to transposons harboured by tailed prophages

“…Proteobacteria T4‐like phages are also targets of external mobile DNA (Edgell et al ., ), so phages from diverse bacterial hosts may facilitate the integration of other mobile element classes (Foley et al ., ). Furthermore, in general horizontally transferred genes in bacterial genomes, including Firmicutes, are preferentially located in hotspot regions, often with mobile elements (Oliveira et al ., ). Since aci1 appears to reside in an integration hotspot in the genome, it is still at risk of further mobilization.…”

“…4, information on the assembly scaffolds is in Supporting Information Table S4, and alignment statistics for the three strains with prophages are in Supporting Information Table S5. 2000). Furthermore, in general horizontally transferred genes in bacterial genomes, including Firmicutes, are preferentially located in hotspot regions, often with mobile elements (Oliveira et al, 2017). Since aci1 appears to reside in an integration hotspot in the genome, it is still at risk of further mobilization.…”

Comparative genomics groups phages of Negativicutes and classical Firmicutes despite different Gram‐staining properties

“…These bacterial genomes replicate bidirectionally and the regions near the origin generally have highly transcribed genes due to gene dosage effects. As prophages are transcriptionally mostly silent and should not interfere with the expression of bacterial household genes, it was postulated that prophages should preferentially be inserted away from the origin of replication (Canchaya et al ., ; Bobay et al ., ; Oliveira et al ., ). Indeed, dividing up Negativicute genomes into 20 equally sized windows, with each window representing 5% of the chromosome length, we found that Negativicute prophages were not distributed randomly across bacterial genomes ( P < 0.01, χ 2 test), with a trend towards insertion towards the terminus of replication (Fig.…”