Genomic GC content drifts downward in most bacterial genomes

Abstract

In every kingdom of life, GC->AT transitions occur more frequently than any other type of mutation due to the spontaneous deamination of cytidine. In eukaryotic genomes, this slow loss of GC base pairs is counteracted by biased gene conversion which increases genomic GC content as part of the recombination process. However, this type of biased gene conversion has not been observed in bacterial genomes, so we hypothesized that GC->AT transitions cause a reduction of genomic GC content in prokaryotic genomes on an evolutionary time scale. To test this hypothesis, we used a phylogenetic approach to analyze triplets of closely related genomes representing a wide range of the bacterial kingdom. The resulting data indicate that genomic GC content is drifting downward in bacterial genomes where GC base pairs comprise 40% or more of the total genome. In contrast, genomes containing less than 40% GC base pairs have fewer opportunities for GC->AT transitions to occur so genomic GC content is relatively stable or actually increasing. It should be noted that this observed change in genomic GC content is the net change in shared parts of the genome and does not apply to parts of the genome that have been lost or acquired since the genomes being compared shared common ancestor. However, a more detailed analysis of two Caulobacter genomes revealed that the acquisition of mobile elements by the two genomes actually reduced the total genomic GC content as well.

Fundamental metabolic strategies of heterotrophic bacteria

“…On long evolutionary timescales (at or above the level of orders), slow adaptation of genomic GC content may optimize whole taxonomic clades to the nutrient availabilities in that clade's typical ecological niche. Thus, metabolic strategies that are well-adapted to the nutrient requirements of the proteome may be one of many potential factors shaping GC content evolution, including biases in mutations and their repair (27)(28)(29), DNA stability (30), and GC-biased gene conversion (gBGC) (31).…”

A simple stochastic model describing the evolution of genomic GC content in asexually reproducing organisms

“…While there are many examples of microbial genomes becoming more AT rich 32 there are so few examples of genomes becoming more GC rich that it was recently suggested that it may not happen at all 16 . Some examples have however been observed in the microbial world although the increase is minuscule 14 , 15 , 41 .…”

“…Environmental influence on genomic GC content in prokaryotes appears to be mediated, at least to some extent, as selective pressures 14 , 15 . In this respect, it is of interest to note that large drops in genomic GC content is wide-spread in prokaryotes 7 while examples of substantial increase is practically non-existent as of now 16 , although smaller increases are documented 13 , 15 , 17 , 18 . Examination of AT- and GC mutation rates in prokaryotes points to an AT bias also in recombining microbes while AT GC substitutions are more likely to be retained 9 , 19 .…”

Biosynthetic Gene Clusters in Sequenced Genomes of Four Contrasting Rhizobacteria in Phytopathogen Inhibition and Interaction with Capsicum annuum Roots

“…Prokaryotes in high-temperature environments have higher GC content than those in low temperatures, suggesting that higher GC contents may be related to thermal adaptation ( 16 ). Mutation events in the DNA, ecological niche conditions, and above all, horizontal gene transfer affect the GC content in bacterial genomes ( 17 ). For the bacteria in this study, the distant signatures between species and the percentages of GC content in their genomes also seem to be a genetic characteristic of these species.…”