Compensatory Relationship between Low Complexity Regions and Gene Paralogy in the Evolution of Prokaryotes

Abstract Evolution of genomes in all life forms involves two distinct, dynamic types of genomic changes: gene duplication (and loss) that shape families of paralogous genes and extension (and contraction) of low complexity regions (LCR), which occurs through dynamics of short repeats in protein-coding genes. Although the roles of each of these types of events in genome evolution have been studied, their co-evolutionary dynamics is not thoroughly understood. Here, by analyzing a wide range of genomes from diverse bacteria and archaea, we show that LCR and paralogy represent two distinct routes of evolution that are inversely correlated. Emergence of LCR is a prominent evolutionary mechanism in fast evolving, young protein families, whereas paralogy dominates the comparatively slow evolution of old protein families. Analysis of multiple prokaryotic genomes shows that the formation of LCR is likely a widespread, transient evolutionary mechanism that temporally and locally affects also ancestral functions, but apparently, fades away with time, under mutational and selective pressures, yielding to gene paralogy. We propose that compensatory relationships between short-term and longer-term evolutionary mechanisms are universal in the evolution of life. Significance Evolution of genomes in all organisms involves a variety of changes occurring on different spatial and temporal scales, from point mutations to whole genome duplication. Here we demonstrate that during the evolution of bacterial and archaeal genomes, there is a universal inverse relationship between the formation of low complexity regions in protein sequences through proliferation of short repeats and gene duplication. The former process apparently is a route of short-term adaptation whereas the latter one dominates evolution on longer temporal scales. We propose that compensatory relationships between evolutionary mechanisms acting at different spatial and temporal scales are a general feature of the process of evolution.