Evolutionary consequences of polyploidy in prokaryotes and the origin of mitosis and meiosis.

Alexander V Markov,Ilya S Kaznacheev

doi:10.1186/s13062-016-0131-8

Abstract

BackgroundThe origin of eukaryote-specific traits such as mitosis and sexual reproduction remains disputable. There is growing evidence that both mitosis and eukaryotic sex (i.e., the alternation of syngamy and meiosis) may have already existed in the basal eukaryotes. The mating system of the halophilic archaeon Haloferax volcanii probably represents an intermediate stage between typical prokaryotic and eukaryotic sex. H. volcanii is highly polyploid, as well as many other Archaea. Here, we use computer simulation to explore genetic and evolutionary outcomes of polyploidy in amitotic prokaryotes and its possible role in the origin of mitosis, meiosis and eukaryotic sex.ResultsModeling suggests that polyploidy can confer strong short-term evolutionary advantage to amitotic prokaryotes. However, it also promotes the accumulation of recessive deleterious mutations and the risk of extinction in the long term, especially in highly mutagenic environment. There are several possible strategies that amitotic polyploids can use in order to reduce the genetic costs of polyploidy while retaining its benefits. Interestingly, most of these strategies resemble different components or aspects of eukaryotic sex. They include asexual ploidy cycles, equalization of genome copies by gene conversion, high-frequency lateral gene transfer between relatives, chromosome exchange coupled with homologous recombination, and the evolution of more accurate chromosome distribution during cell division (mitosis). Acquisition of mitosis by an amitotic polyploid results in chromosome diversification and specialization. Ultimately, it transforms a polyploid cell into a functionally monoploid one with multiple unique, highly redundant chromosomes. Specialization of chromosomes makes the previously evolved modes of promiscuous chromosome shuffling deleterious. This can result in selective pressure to develop accurate mechanisms of homolog pairing, and, ultimately, meiosis.ConclusionEmergence of mitosis and the first evolutionary steps towards eukaryotic sex could have taken place in the ancestral polyploid, amitotic proto-eukaryotes, as they were struggling to survive in the highly mutagenic environment of the Early Proterozoic shallow water microbial communities, through the succession of the following stages: (1) acquisition of high-frequency between-individual genetic exchange coupled with homologous recombination; (2) acquisition of mitosis, followed by rapid chromosome diversification and specialization; (3) evolution of homolog synapsis and meiosis. Additional evidence compatible with this scenario includes mass acquisition of new families of paralogous genes by the basal eukaryotes, and recently discovered correlation between polyploidy and the presence of histones in Archaea.ReviewerThis article was reviewed by Eugene Koonin, Uri Gophna and Armen Mulkidjanian. For the full reviews, please go to the Reviewers' comments section.

Highlights

Introduction "This obstacle can be partially overcome by ongoing strong selection against homozygotes [12, 31]" should be "In the lab, this obstacle can be partially overcome by ongoing strong selection against homozygotes [12, 31]", since no such natural selection has been observed
Polyploidy in prokaryotes increases the risk of genetic degradation and extinction Unless the mutation rate (M) is low enough to ensure stable existence of the population regardless of ploidy, monoploids are more viable than polyploids in the long term
Between-individual chromosome exchange coupled with homologous recombination retains its positive effect in mitotic polyploid protoeukaryotes, at least initially

Summary

Introduction

Introduction "This obstacle can be partially overcome by ongoing strong selection against homozygotes [12, 31]" should be "In the lab, this obstacle can be partially overcome by ongoing strong selection against homozygotes [12, 31]", since no such natural selection has been observed. There is growing evidence that both mitosis and eukaryotic sex (i.e., the alternation of syngamy and meiosis) may have already existed in the basal eukaryotes. The mating system of the halophilic archaeon Haloferax volcanii probably represents an intermediate stage between typical prokaryotic and eukaryotic sex. It is possible that some early forms of amphimixis already existed in the basal eukaryotes and probably even in their prokaryotic ancestors [4,5,6,7,8]. From this standpoint, it is interesting to look for possible intermediate forms of sex in extant Archaea. Cell fusion can occur under laboratory conditions when cytoplasmic bridges become destabilized (this can be achieved by lowering the Mg2+ concentration to remove the cell envelopes [9]), and probably in nature [10]

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