Prokaryotic nucleotide composition is shaped by both phylogeny and the environment

Abstract

The causes of the great variation in nucleotide composition of prokaryotic genomes have long been disputed. Here, we use extensive metagenomic and whole-genome data to demonstrate that both phylogeny and the environment shape prokaryotic nucleotide content. We show that across environments, various phyla are characterized by different mean guanine and cytosine (GC) values as well as by the extent of variation on that mean value. At the same time, we show that GC-content varies greatly as a function of environment, in a manner that cannot be entirely explained by disparities in phylogenetic composition. We find environmentally driven differences in nucleotide content not only between highly diverged environments (e.g., soil, vs. aquatic vs. human gut) but also within a single type of environment. More specifically, we demonstrate that some human guts are associated with a microbiome that is consistently more GC-rich across phyla, whereas others are associated with a more AT-rich microbiome. These differences appear to be driven both by variations in phylogenetic composition and by environmental differences-which are independent of these phylogenetic composition differences. Combined, our results demonstrate that both phylogeny and the environment significantly affect nucleotide composition and that the environmental differences affecting nucleotide composition are far subtler than previously appreciated.

Keywords: GC-content; evolutionary forces; genomic variation; metagenomics; mutation; natural selection.

Fig. 1.—

Relative abundance of each phylum within the various sampled environments.

Fig. 2.—

Average GC-composition by environment. The GC-composition was averaged across the ten phyla found to be most abundant across all sampled biomes in an environmental category.

Fig. 3.—

Relative abundance of the ten most abundant phyla in the human gut samples.