Metabolic adaptations underlying genome flexibility in prokaryotes

Abstract

Even across genomes of the same species, prokaryotes exhibit remarkable flexibility in gene content. We do not know whether this flexible or "accessory" content is mostly neutral or adaptive, largely due to the lack of explicit analyses of accessory gene function. Here, across 96 diverse prokaryotic species, I show that a considerable fraction (~40%) of accessory genomes harbours beneficial metabolic functions. These functions take two forms: (1) they significantly expand the biosynthetic potential of individual strains, and (2) they help reduce strain-specific metabolic auxotrophies via intra-species metabolic exchanges. I find that the potential of both these functions increases with increasing genome flexibility. Together, these results are consistent with a significant adaptive role for prokaryotic pangenomes.

Fig 1. The accessory genomes of prokaryotes harbour extensive biosynthetic potential.

Scatter plot of genome fluidity φ versus accessory metabolic capacity α for the 96 prokaryotic species in this study. Each point represents the average number of precursors that could be synthesized by the accessory genome content alone in each strain of a species. The Venn diagrams on the right provide a schematic representation of open pangenomes (high φ, small core) versus closed pangenomes (low φ, large core). The solid black line represents a linear regression and the gray envelope around it, the 95% prediction interval. rho corresponds to Spearman’s nonparametric correlation coefficient and the P value to a one-way asymptotic permutation test for positive correlation.

Fig 2. Conspecific metabolic dependencies scale with accessory genome content.

a, Scatter plot of genome fluidity φ versus conspecific metabolic dependency potential (MDP) for the 96 prokaryotic species in this study. Each point represents the average number of dependencies detected per strain per condition across all conspecific pairs for one species. Colours represent each species’ phylum-level taxonomic identity. The solid black line represents a linear regression and the gray envelope around it, the 95% prediction interval. rho corresponds to Spearman’s nonparametric correlation coefficient and the P value to a one-way asymptotic permutation test for positive correlation. b, Pie chart of the types of interactions detected in each conspecific pair. c, Pie chart of the types of auxotrophies that the detected dependencies relieve due to pairwise growth. Each of the 137 precursors belongs to a unique chosen category (S4 Table).