Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence

Jaime Iranzo,Eugene V Koonin,Itamar Sela,Yuri I Wolf

doi:10.1038/s41467-019-13429-2

Abstract

Bacterial and archaeal evolution involve extensive gene gain and loss. Thus, phylogenetic trees of prokaryotes can be constructed both by traditional sequence-based methods (gene trees) and by comparison of gene compositions (genome trees). Comparing the branch lengths in gene and genome trees with identical topologies for 34 clusters of closely related bacterial and archaeal genomes, we show here that terminal branches of gene trees are systematically compressed compared to those of genome trees. Thus, sequence evolution is delayed compared to genome evolution by gene gain and loss. The extent of this delay differs widely among bacteria and archaea. Mathematical modeling shows that the divergence delay can result from sequence homogenization by homologous recombination. The model explains how homologous recombination maintains the cohesiveness of the core genome of a species while allowing extensive gene gain and loss within the accessory genome. Once evolving genomes become isolated by barriers impeding homologous recombination, gene and genome evolution processes settle into parallel trajectories, and genomes diverge, resulting in speciation.

Highlights

Bacterial and archaeal evolution involve extensive gene gain and loss
Mathematical modeling of the molecular processes involved in homologous recombination has shown that barriers to recombination can build up spontaneously and lead to speciation if (i) recombination efficiency decays sufficiently fast with sequence divergence and (ii) the balance of mutation and recombination favors the accumulation of sequence variability in the population[20,21,22,23,24]
By studying sequence and gene content divergence in groups of closely related prokaryotes, we found that the onset of sequence evolution is often delayed with respect to genome evolution, the magnitude of the delay broadly varies across bacterial and archaeal lineages

Summary

Introduction

Bacterial and archaeal evolution involve extensive gene gain and loss. phylogenetic trees of prokaryotes can be constructed both by traditional sequence-based methods (gene trees) and by comparison of gene compositions (genome trees). Evolution of bacterial and archaeal genomes is a highly dynamic process that involves extensive gain and loss of genes, with turnover rates comparable to if not exceeding the rate of nucleotide substitution[1,2,3]. Mathematical modeling of the molecular processes involved in homologous recombination has shown that barriers to recombination can build up spontaneously and lead to speciation if (i) recombination efficiency decays sufficiently fast with sequence divergence and (ii) the balance of mutation and recombination favors the accumulation of sequence variability in the population[20,21,22,23,24]. We combine comparative genomics and phylogenetic analysis to investigate how the fraction of genes shared by closely related bacterial and archaeal genomes decays with the phylogenetic distance and show that the sequence-based molecular clock and the gene turnover clock are incongruent at short evolutionary times. We investigate the tempo and the factors that contribute to the establishment of barriers to recombination and, eventually, speciation in the populations of diverse bacteria and archaea

Methods

Results

Conclusion