The slow:fast substitution ratio reveals changing patterns of natural selection in γ-proteobacterial genomes

Abstract

Different microbial species are thought to occupy distinct ecological niches, subjecting each species to unique selective constraints, which may leave a recognizable signal in their genomes. Thus, it may be possible to extract insight into the genetic basis of ecological differences among lineages by identifying unusual patterns of substitutions in orthologous gene or protein sequences. We used the ratio of substitutions in slow-versus fast-evolving sites (nucleotides in DNA, or amino acids in protein sequence) to quantify deviations from the typical pattern of selective constraint observed across bacterial lineages. We propose that elevated S:F in one branch (an excess of slowsite substitutions) can indicate a functionally relevant change, due to either positive selection or relaxed evolutionary constraint. In a genome-wide comparative study of c-proteobacterial proteins, we find that cell-surface proteins involved with motility and secretion functions often have high S:F ratios, whereas information-processing genes do not. Change in evolutionary constraints in some species is evidenced by increased S:F ratios within functionally related sets of genes (for example, energy production in Pseudomonas fluorescens), whereas other species apparently evolve mostly by drift (for example, uniformly elevated S:F across most genes in Buchnera spp.). Overall, S:F reveals several species-specific, protein-level changes with potential functional/ecological importance. As microbial genome projects yield more species-rich gene trees, the S:F ratio will become an increasingly powerful tool for uncovering functional genetic differences among species.

Pseudomonasgenomes: diverse and adaptable

“…The more sequences that are available, the more in‐depth such analyses. Shapiro & Alm (2009) introduced an additional means by which to measure patterns of selection, based on the ratio of ‘slow’ vs. ‘fast’ substitutions ( S : F ); it finds deviations from a sequence's ‘normal’ selection regime. Using these methods, lineage‐specific adaptations that might have escaped detection because of the absence of appropriate experimental data may be revealed, opening new areas of investigation.…”

“…Although S : F alone cannot discern between positive or relaxed negative selection when a lineage such as Pseudomonas AceE and SdhCD show a high S : F compared with other lineages, it does potentially indicate ecological adaptation and thus allow for the generation of testable hypotheses. For example, Shapiro & Alm (2009) proposed a possible link between the changes in P. fluorescens with growth in oxygen‐limiting biofilms, which has led to the selection of phenazine compounds as terminal electron acceptors. Moreover, changes in SdhCD may reflect changes in redox balance associated with oxidative stress experienced by Pseudomonas interacting with eukaryotes such as plants.…”

“…S : F is less useful when several members of a lineage are under similar selective pressures, because it would not be possible to classify particular sites as generally 'slow' changing if indeed there is a high degree of variability at those sites. When applied to Pseudomonas genomes, Shapiro & Alm (2009) detected an elevated S : F ratio in some energy production proteins [pyruvate dehydrogenase E1 component (AceE) and succinate dehydrogenase complex (SdhCD)], which in most species tend to have low S : F ratios. Although S : F alone cannot discern between positive or relaxed negative selection when a lineage such as Pseudomonas AceE and SdhCD show a high S : F compared with other lineages, it does potentially indicate ecological adaptation and thus allow for the generation of testable hypotheses.…”

Horizontal transmission and recombination maintain forever young bacterial symbiont genomes

“…The transmission bottleneck that occurs when symbionts are passed on to host offspring further exacerbates these dynamics by making deleterious mutations more likely to drift to fixation in the next generation [ 5 , 6 ]. Indeed, many endosymbiont taxa exhibit weak purifying selection at the gene level [ 7 – 10 ]. In the early stages of bacterial symbiont-host associations, deleterious mutations arise on each symbiont chromosome and a portion drift or hitchhike with adaptive mutations to fixation.…”

ODoSE: A Webserver for Genome-Wide Calculation of Adaptive Divergence in Prokaryotes

“…The accessory genome clearly is of profound importance to the physiology and ecology of strains and species. However, it has become increasingly clear that bacterial core genes conserved between species play a major role in niche adaptation as well [2]–[7]. The McDonald-Kreitman (MK) test is a powerful test of selection [8]–[10] comparing patterns of non-synonymous and synonymous substitutions within a species to those separating this species from an outgroup species.…”