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Review
, 285 (1872)

How Oxygen Gave Rise to Eukaryotic Sex

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Review

How Oxygen Gave Rise to Eukaryotic Sex

Elvira Hörandl et al. Proc Biol Sci.

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.

Keywords: Muller's ratchet; eukaryotes; meiosis; oxidative stress; paradox of sex.

Conflict of interest statement

The authors have no competing interests.

Figures

Figure 1.
Figure 1.
Possible steps describing eukaryotic origins and evolution of meiotic sex. The specific timing is arbitrary (e.g. meiotic sex probably evolved before phagocytosis). (1) Cell fusion of Archaeon and alpha-proteobacterium; (2) establishment of endosymbiosis with aerobic respiration, efficient energy generation and internal ROS production; (3) remodelling of membranes, origin of peroxisomes, transition to linear host chromosomes, chromatin, transfer of genes from mitochondrial genome to host genome and RNA splicing; (4) endogenous evolution of nuclear envelope for protection from short-lived ROS, spindle formation for moving bulky linear chromosomes, establishment of mitosis, mitochondrial ATP production allowing increase of body size (and phagocytosis?); (5A) novel stress situations with ROS (H2O2) production and increase in nuclear DNA damage: e.g. high motility, phagotrophy, endosymbiosis with cyanobacteria (the first plastid acquisition is difficult to date, but probably earlier than previously thought, [33,34]); (5B) mitosis and clonal growth as an alternative mode of reproduction under favourable conditions; (6) DNA damage triggers cell and nuclear fusions in various combinations, leading to early eukaryotic, mostly mixotrophic, panmictic (?) populations; (7) meiosis I established as HR DNA repair tool, homologous pairing established by controlled DSB formation, lineage-specific spo11 evolution; and (8) meiosis II and establishment of diploid–haploid cycles. (Online version in colour.)

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