Shared properties of gene transfer agent and core genes revealed by comparative genomics of Alphaproteobacteria

Abstract

Gene transfer agents (GTAs) are phage-like particles that transfer pieces of cellular genomic DNA to other cells. Homologues of the Rhodobacter capsulatus GTA (RcGTA) structural genes are widely distributed in the Alphaproteobacteria and particularly well conserved in the order Rhodobacterales. Possible reasons for their widespread conservation are still being discussed. It has been suggested that these alphaproteobacterial elements originate from a prophage that was present in an ancestral bacterium and subsequently evolved into a GTA that is now widely maintained in extant descendant lineages. Here, we analysed genomic properties that might relate to the conservation of these alphaproteobacterial GTAs. This revealed that the chromosomal locations of the GTA gene clusters are biased. They primarily occur on the leading strand of DNA replication, at large distances from long repetitive elements, and thus are in regions of lower plasticity, and in areas of extreme GC skew, which also accumulate core genes. These extreme GC skew regions arise from the preferential use of codons with an excess of G over C, a distinct phenomenon from the elevated GC content that has previously been found to be associated with GTA genes. The observed properties, along with their high level of conservation, show that GTA genes share multiple features with core genes in the examined lineages of the Alphaproteobacteria.

On the Evolution of Chromosomal Regions with High Gene Strand Bias in Bacteria

“…Contrastingly, the higher mutation rate might provide a fitness benefit for genes that need to be quickly adapted, like those coding for virulence or transcription factors [10,38]. Regardless of the detrimental effects, most bacteria thrive well with a rather large fraction up to almost half of their genes oriented head-on to replication [1,17,39]. Gene inversions, identified through a sign-change in GC- skew compared to the surrounding, seem to be common, although the frequency and directionality can vary between phyla [10,39].…”

“…Regardless of the detrimental effects, most bacteria thrive well with a rather large fraction up to almost half of their genes oriented head-on to replication [1,17,39]. Gene inversions, identified through a sign-change in GC- skew compared to the surrounding, seem to be common, although the frequency and directionality can vary between phyla [10,39]. The Bacillota remain so far the only exception with an almost universally conserved strong GSB, even along large chromosomes.…”

“…Accession numbers can be found in Supplementary Table S1. For all Gemmatimonadota and for additional strains selected for visualization, chromosomes were centered around the ori , as determined by ori-finder website [54], using the reorientCircGenomes package in R [39]. Visualizations were realized using ggplot2 and ggbio [55].…”

On the evolution of chromosomal regions with high gene strand bias in bacteria

“…Contrastingly, the higher mutation rate might provide a fitness benefit for genes that need to be quickly adapted, like those coding for virulence or transcription factors ( 10 , 39 ). Regardless of the detrimental effects, most bacteria thrive well with a rather large fraction up to almost half of their genes oriented head-on to replication ( 1 , 17 , 40 ). Gene inversions, identified through a sign change in GC skew compared to the surrounding, seem to be common, although the frequency and directionality can vary between phyla ( 10 , 40 ).…”

“…Regardless of the detrimental effects, most bacteria thrive well with a rather large fraction up to almost half of their genes oriented head-on to replication ( 1 , 17 , 40 ). Gene inversions, identified through a sign change in GC skew compared to the surrounding, seem to be common, although the frequency and directionality can vary between phyla ( 10 , 40 ). The Bacillota remain so far the only exception with an almost universally conserved HSB, even along large chromosomes.…”