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Gain and loss of accessory genes accelerates gene sequence divergence and promotes speciation in prokaryotes

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. Thus, prokaryotic taxa are characterized by large sets of accessory genes -i.e. genes that are present only in some strains and provide adaptation to specific environments- and much smaller sets of core genes -i.e. genes harbored by every genome from the same taxon and typically involved in housekeeping functions. How large-scale changes in the accessory genome interact with mutations in core genes to drive diversification of prokaryotes is a long-standing question where microbial genomics, ecology, and evolution converge.

In their work, Dr. Iranzo and colleagues compared the dynamics of sequence divergence in highly conserved core genes with the dynamics of gene gain and loss for 34 groups of closely related bacterial and archaeal genomes. They found that sequence evolution in core genes is delayed with respect to genome -i.e. gene content- evolution, and that the extent of this delay widely varies across taxa (Figure 1). Then, the authors used a mathematical model to demonstrate that the delay in the evolution of core genes can result from sequence homogenization, which itself is caused by homologous recombination within the population. 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. Only after the evolving genomes become isolated by barriers that impede homologous recombination, do gene and genome evolution processes settle into parallel trajectories and genomes diverge. Notably, the analyses carried out by Dr. Iranzo and colleagues revealed that the higher the gene turnover rate, the faster the barriers to homologous recombination are established. In consequence, gain and loss of accessory genes promote sequence divergence and, eventually, speciation.

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Figure 1: Sequence evolution in the core genome is delayed with respect to gene content evolution in the accessory genome. The evolution of the Bacillus thuringiensis/anthracis/cereus group of bacteria was studied by building phylogenetic trees based on the sequence alignment of highly conserved core genes (a) or on the comparison of accessory gene gains and losses across genomes (b). (c) Comparison of both trees reveals a delayed onset of sequence evolution (y-axis) with respect to gene content evolution (x-axis), with a delay that varies among different groups of bacteria.


Beyond its contribution to our fundamental understanding of speciation, the findings of this work have practical implications for the study of molecular evolution in bacteria and archaea. Specifically, it shows that molecular clocks and phylogenetic trees inferred from sequence alignments are generally inconsistent with those based on gene content comparisons. At the same time, the theory developed by the authors provides a framework to correct such inconsistencies and reconcile gene- and genome-centric approaches.

Original Paper:

Iranzo, J., Wolf, Y.I., Koonin, E.V., Sela, I. 2019. Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence. Nature Communications 10, 5376. DOI: 10.1038/s41467-019-13429-2

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