Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes

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Abstract
Gene duplication followed by neo- or sub-functionalization deeply impacts the evolution of protein families and is regarded as the main source of adaptive functional novelty in eukaryotes. While there is ample evidence of adaptive gene duplication in prokaryotes, it is not clear whether duplication outweighs the contribution of horizontal gene transfer in the expansion of protein families. We analyzed closely related prokaryote strains or species with small genomes (Helicobacter, Neisseria, Streptococcus, Sulfolobus), average-sized genomes (Bacillus, Enterobacteriaceae), and large genomes (Pseudomonas, Bradyrhizobiaceae) to untangle the effects of duplication and horizontal transfer. After removing the effects of transposable elements and phages, we show that the vast majority of expansions of protein families are due to transfer, even among large genomes. Transferred genes—xenologs—persist longer in prokaryotic lineages possibly due to a higher/longer adaptive role. On the other hand, duplicated genes—paralogs—are expressed more, and, when persistent, they evolve slower. This suggests that gene transfer and gene duplication have very different roles in shaping the evolution of biological systems: transfer allows the acquisition of new functions and duplication leads to higher gene dosage. Accordingly, we show that paralogs share most protein–protein interactions and genetic regulators, whereas xenologs share very few of them. Prokaryotes invented most of life's biochemical diversity. Therefore, the study of the evolution of biology systems should explicitly account for the predominant role of horizontal gene transfer in the diversification of protein families. Prokaryotes can be found in the most diverse and severe ecological niches of the planet. Their rapid adaptation is, in part, the result of the ability to acquire genetic information horizontally. This means that prokaryotes utilize two major paths to expand their repertoire of protein families: they can duplicate a pre-existing gene or acquire it by horizontal transfer. In this study, we track family expansions among closely related strains of prokaryotic species. We find that the majority of gene expansions arrive via transfer not via duplication. Additionally, we find that duplicate genes tend be more transient and evolve slower than transferred ones, highlighting different roles with respect to adaptation and evolution. These results suggest that prevailing theories aimed at understanding the evolution of biological systems grounded on gene duplication might be poorly fit to explain the evolution of prokaryotic systems, which include the vast majority of life's biochemical diversity.