The nucleotide composition of microbial genomes indicates differential patterns of selection on core and accessory genomes

Abstract

BackgroundThe core genome consists of genes shared by the vast majority of a species and is therefore assumed to have been subjected to substantially stronger purifying selection than the more mobile elements of the genome, also known as the accessory genome. Here we examine intragenic base composition differences in core genomes and corresponding accessory genomes in 36 species, represented by the genomes of 731 bacterial strains, to assess the impact of selective forces on base composition in microbes. We also explore, in turn, how these results compare with findings for whole genome intragenic regions.ResultsWe found that GC content in coding regions is significantly higher in core genomes than accessory genomes and whole genomes. Likewise, GC content variation within coding regions was significantly lower in core genomes than in accessory genomes and whole genomes. Relative entropy in coding regions, measured as the difference between observed and expected trinucleotide frequencies estimated from mononucleotide frequencies, was significantly higher in the core genomes than in accessory and whole genomes. Relative entropy was positively associated with coding region GC content within the accessory genomes, but not within the corresponding coding regions of core or whole genomes.ConclusionThe higher intragenic GC content and relative entropy, as well as the lower GC content variation, observed in the core genomes is most likely associated with selective constraints. It is unclear whether the positive association between GC content and relative entropy in the more mobile accessory genomes constitutes signatures of selection or selective neutral processes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3543-7) contains supplementary material, which is available to authorized users.

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

“…Several methods were considered to identify and filter contigs or reads that were likely contaminants in our data. Initially we considered to filter contigs or reads based on their GC content, since this differs between oomycete genomes [78] and most other microbes [79]. However, not all bacteria have a distinctive nucleotide usage, for example E. coli has a GC content of 51.7% [79], which is close to that of most oomycetes.…”

“…Initially we considered to filter contigs or reads based on their GC content, since this differs between oomycete genomes [78] and most other microbes [79]. However, not all bacteria have a distinctive nucleotide usage, for example E. coli has a GC content of 51.7% [79], which is close to that of most oomycetes. In addition, the GC bases are not evenly distributed over the genome, so filtering based on GC content could therefore potentially remove valuable parts of the genome.…”

Disentangling the impact of environmental and phylogenetic constraints on prokaryotic strain diversity

“…4). The conservation of the core genome in a given clade is likely due to the fact that it consists of essential genes that are under strong negative selection pressure [68][69][70], which leads to vertical "heritability" of its content and size from ancestral species to descendants during speciation events.…”

Codon-usage optimization in the prokaryotic tree of life: How synonymous codons are differentially selected in sequence domains with different expression levels and degrees of conservation

“…That process is counterbalanced by selection-based constraints that, in turn, increase the GC content and fine-tune codon usage— i. e. , the so-called mutation-selection-drift model (14–16). Intragenomic codon-usage heterogeneities, however, are always present among different gene sets— i. e. , between core genes that are shared throughout a given lineage, and singletons (unique accessory genes) that are taxa- and/or strain-specific (17, 18). Furthermore, in a multipartite genome, the linkage between the physical patterns of heterogeneity in codon usage and the replicon location of the different core genes has also been recently demonstrated (19).…”

“…The analysis of an extensive number of genes with different functions, ubiquitousness, and degrees of phylogenetic conservation has demonstrated that codon usage is related to gene-expression level (33, 42, 43), the degree of conservation (18, 32, 44, 45), the genomic location— i. e. , chromosome, chromid, plasmidome (19, 46, 47)—and different features such as codon ramps, and mRNA secondary structure, among others (48–50). Current evidence indicates that accessory genes involve atypical codon usages (21, 47, 51, 52) compared to the more conserved (ancestral) core genes in a given lineage.…”