G+C3 Structuring Along the Genome: A Common Feature in Prokaryotes

Abstract

The heterogeneity of gene nucleotide content in prokaryotic genomes is commonly interpreted as the result of three main phenomena: (1) genes undergo different selection pressures both during and after translation (affecting codon and amino acid choice); (2) genes undergo different mutational pressure whether they are on the leading or lagging strand; and (3) genes may have different phylogenetic origins as a result of lateral transfers. However, this view neglects the necessity of organizing genetic information on a chromosome that needs to be replicated and folded, which may add constraints to single gene evolution. As a consequence, genes are potentially subjected to different mutation and selection pressures, depending on their position in the genome. In this paper, we analyze the structuring of different codon usage measures along completely sequenced bacterial genomes. We show that most of them are highly structured, suggesting that genes have different base content, depending on their location on the chromosome. A peculiar pattern of genome structure, with a tendency toward an A+T-enrichment near the replication terminus, is found in most bacterial phyla and may reflect common chromosome constraints. Several species may have lost this pattern, probably because of genome rearrangements or integration of foreign DNA. We show that in several species, this enrichment is associated with an increase of evolutionary rate and we discuss the evolutionary implications of these results. We argue that structural constraints acting on the circular chromosome are not negligible and that this natural structuring of bacterial genomes may be a cause of overestimation in lateral gene transfer predictions using codon composition indices.

Comparative genomics of the genus Bifidobacterium

“…In fact, the rightmost and leftmost parts of the plots that correspond to the ori do not display synteny, suggesting that such regions are subject to a higher rate of reshuffling or an increased acquisition of alien DNA by horizontal gene transfer (HGT) compared with the alignment within the B. longum phylogenetic group. Such findings contrast with what has previously been described for bacterial genome evolution, where it was suggested that the regions around the replication terminus display an increased frequency of HGT compared with the remainder of the chromosome (Daubin & Perriere, 2003).…”

Diversity of the genus Lactobacillus revealed by comparative genomics of five species

“…The leftmost and rightmost parts of the plots that correspond to the ori region have no clear regions of synteny, which may indicate that these regions are subject to a greater rate of change by a higher rate of reshuffling or by an increased acquisition of foreign DNA by horizontal gene transfer. This contrasts with previous analyses of other bacteria (Daubin & Perriere, 2003), which suggested that the region opposite to the replication origin (terminus) had a higher frequency of phage insertion and 'orphan' gene acquisition. Other important regions with a null synteny correspond to the megaplasmid pMP118 and a large region next to the origin of replication at the end of the L. plantarum circular chromosome as depicted in Fig.…”

Comparative genomics and the evolution of prokaryotes

“…This is also correlated with several evolutionary features ( Figure 1): in many genomes, genes near the terminus of replication tend to have lower content in G + C nucleotides and to exhibit higher rates of evolution [12]. Also, as a result of the replication process, genes located close to the Ori can be significantly amplified in dividing cells, in comparison with those closer to the terminus.…”