How oxygen gave rise to eukaryotic sex

Abstract

How did full meiotic eukaryotic sex evolve and what was the immediate advantage allowing it to develop? We propose that the crucial determinant can be found in internal reactive oxygen species (ROS) formation at the start of eukaryotic evolution approximately 2 × 109 years ago. The large amount of ROS coming from a bacterial endosymbiont gave rise to DNA damage and vast increases in host genome mutation rates. Eukaryogenesis and chromosome evolution represent adaptations to oxidative stress. The host, an archaeon, most probably already had repair mechanisms based on DNA pairing and recombination, and possibly some kind of primitive cell fusion mechanism. The detrimental effects of internal ROS formation on host genome integrity set the stage allowing evolution of meiotic sex from these humble beginnings. Basic meiotic mechanisms thus probably evolved in response to endogenous ROS production by the ‘pre-mitochondrion’. This alternative to mitosis is crucial under novel, ROS-producing stress situations, like extensive motility or phagotrophy in heterotrophs and endosymbiontic photosynthesis in autotrophs. In multicellular eukaryotes with a germline–soma differentiation, meiotic sex with diploid–haploid cycles improved efficient purging of deleterious mutations. Constant pressure of endogenous ROS explains the ubiquitous maintenance of meiotic sex in practically all eukaryotic kingdoms. Here, we discuss the relevant observations underpinning this model.

HDAC6 inhibition induces the failure of mouse early embryonic development

“…The detrimental effects of ROS formation could give rise to DNA lesion in cells (Horandl & Speijer, ). Next, we examined the DNA damage status in the control and TubA‐treated embryos by staining the phosphorylated H2AX (γH2AX), a surrogate marker for DNA damage (Yukawa, Oda, Mitani, Nagata, & Aoki, ).…”

Metabolism‐induced oxidative stress and DNA damage selectively trigger genome instability in polyploid fungal cells

“…The emergence of sex would have enhanced DNA repair yet came with significant costs including the twofold cost of sex (de Visser & Elena, ; Bernstein et al , ; Goddard, ; McDonald et al , ). Intriguingly, sex may have been especially advantageous in dealing with oxidative stress from the endosymbiont that formed the pre‐mitochondrion, as this aerobic bacterium would have generated high levels of ROS (Blackstone, ; Bernstein et al , ; Horandl & Speijer, ). Sex would have been particularly effective in repairing subsequent ROS‐induced DNA damage via homologous recombination.…”

All Eukaryotes Are Sexual, unless Proven Otherwise

“…During meiosis, homologous chromosomes are aligned allowing for recombination and silencing of newly translocated selfish elements . As meiosis promotes a large‐scale repair of the nuclear genome, it was suggested that meiosis evolved and was maintained as a way to repair the genome from continuous DNA damage caused by increased amounts of reactive oxygen species generated by mitochondrial metabolism …”

“…[11] As meiosis promotes a large-scale repair of the nuclear genome, it was suggested that meiosis evolved and was maintained as a way to repair the genome from continuous DNA damage caused by increased amounts of reactive oxygen species generated by mitochondrial metabolism. [12,13] 2. Meiosis Toolkit Can Reveal the Nature of Asexual Scandals Meiotic processes are performed by the meiosis-specific machinery (the "meiosis toolkit"), and this set of proteins may be used for indirect detection of meiosis based on genomic information.…”