Genomes in turmoil: quantification of genome dynamics in prokaryote supergenomes.

Pere Puigbò,Alexander E Lobkovsky,Eugene V Koonin,David M Kristensen,Yuri I Wolf

doi:10.1186/s12915-014-0066-4

Pere Puigbò, Alexander E Lobkovsky + Show 3 more

Open Access

https://doi.org/10.1186/s12915-014-0066-4

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Abstract

BackgroundGenomes of bacteria and archaea (collectively, prokaryotes) appear to exist in incessant flux, expanding via horizontal gene transfer and gene duplication, and contracting via gene loss. However, the actual rates of genome dynamics and relative contributions of different types of event across the diversity of prokaryotes are largely unknown, as are the sizes of microbial supergenomes, i.e. pools of genes that are accessible to the given microbial species.ResultsWe performed a comprehensive analysis of the genome dynamics in 35 groups (34 bacterial and one archaeal) of closely related microbial genomes using a phylogenetic birth-and-death maximum likelihood model to quantify the rates of gene family gain and loss, as well as expansion and reduction. The results show that loss of gene families dominates the evolution of prokaryotes, occurring at approximately three times the rate of gain. The rates of gene family expansion and reduction are typically seven and twenty times less than the gain and loss rates, respectively. Thus, the prevailing mode of evolution in bacteria and archaea is genome contraction, which is partially compensated by the gain of new gene families via horizontal gene transfer. However, the rates of gene family gain, loss, expansion and reduction vary within wide ranges, with the most stable genomes showing rates about 25 times lower than the most dynamic genomes. For many groups, the supergenome estimated from the fraction of repetitive gene family gains includes about tenfold more gene families than the typical genome in the group although some groups appear to have vast, ‘open’ supergenomes.ConclusionsReconstruction of evolution for groups of closely related bacteria and archaea reveals an extremely rapid and highly variable flux of genes in evolving microbial genomes, demonstrates that extensive gene loss and horizontal gene transfer leading to innovation are the two dominant evolutionary processes, and yields robust estimates of the supergenome size.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0066-4) contains supplementary material, which is available to authorized users.

Highlights

IntroductionGenomes of bacteria and archaea (collectively, prokaryotes) appear to exist in incessant flux, expanding via horizontal gene transfer and gene duplication, and contracting via gene loss
Genomes of bacteria and archaea appear to exist in incessant flux, expanding via horizontal gene transfer and gene duplication, and contracting via gene loss
These patterns were mapped onto the phylogenetic tree of the respective alignable tight genome cluster (ATGC) and employed for the evolutionary reconstruction using Count, an maximum likelihood (ML) method based on a phylogenetic gene birth-and-death model [22]

Summary

Introduction

Genomes of bacteria and archaea (collectively, prokaryotes) appear to exist in incessant flux, expanding via horizontal gene transfer and gene duplication, and contracting via gene loss. Beyond the comparative genomic observations, estimates of the genome dynamics rates in prokaryotes have been obtained via explicit evolutionary reconstruction using maximum parsimony or maximum likelihood (ML) methods. These approaches typically employ the pattern of gene presence/absence in a set of species, which is mapped onto a guide phylogenetic tree [19,20,21,22,23]. Gene loss has been reported to be a more uniform, ‘clock-like’ process than gene gain, which shows a stronger episodic character [19,29] Taken together, these findings have inspired the concept of genome reduction as the ‘default’ evolutionary process counterbalanced by episodes of gene gain, primarily via HGT [34]

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