Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Abstract

Theories for the origin of sex traditionally start with an asexual mitosing cell and add recombination, thereby deriving meiosis from mitosis. Though sex was clearly present in the eukaryote common ancestor, the order of events linking the origin of sex and the origin of mitosis is unknown. Here, we present an evolutionary inference for the origin of sex starting with a bacterial ancestor of mitochondria in the cytosol of its archaeal host. We posit that symbiotic association led to the origin of mitochondria and gene transfer to host's genome, generating a nucleus and a dedicated translational compartment, the eukaryotic cytosol, in which-by virtue of mitochondria-metabolic energy was not limiting. Spontaneous protein aggregation (monomer polymerization) and Adenosine Tri-phosphate (ATP)-dependent macromolecular movement in the cytosol thereby became selectable, giving rise to continuous microtubule-dependent chromosome separation (reduction division). We propose that eukaryotic chromosome division arose in a filamentous, syncytial, multinucleated ancestor, in which nuclei with insufficient chromosome numbers could complement each other through mRNA in the cytosol and generate new chromosome combinations through karyogamy. A syncytial (or coenocytic, a synonym) eukaryote ancestor, or Coeca, would account for the observation that the process of eukaryotic chromosome separation is more conserved than the process of eukaryotic cell division. The first progeny of such a syncytial ancestor were likely equivalent to meiospores, released into the environment by the host's vesicle secretion machinery. The natural ability of archaea (the host) to fuse and recombine brought forth reciprocal recombination among fusing (syngamy and karyogamy) progeny-sex-in an ancestrally meiotic cell cycle, from which the simpler haploid and diploid mitotic cell cycles arose. The origin of eukaryotes was the origin of vertical lineage inheritance, and sex was required to keep vertically evolving lineages viable by rescuing the incipient eukaryotic lineage from Muller's ratchet. The origin of mitochondria was, in this view, the decisive incident that precipitated symbiosis-specific cell biological problems, the solutions to which were the salient features that distinguish eukaryotes from prokaryotes: A nuclear membrane, energetically affordable ATP-dependent protein-protein interactions in the cytosol, and a cell cycle involving reduction division and reciprocal recombination (sex).

Keywords: alternation of generations; chromosome segregation; coeocytic; endomembrane system; eukaryotes; karyogamy; meiosis; mitosis; origin; reduction division; syngamy.

Fig. 1.

(A) Cell cycles and life cycles in eukaryotes. Meiosis (reduction division) connects haploid and diploid cell cycles. Each cell cycle is divided into distinct phases G (gap), S (synthesis) and the meiotic or mitotic phase, within which P (prophase), M (metaphase), A (anaphase), and T (telophase) phases are distinguished (see text). Carbon and energy are required to drive all cellular processes, including these cycles, upon which population genetic effects can subsequently operate. The asterisk indicates where, roughly, we would place the starting point in the origin of the process, that is, the symbiotic merger of host and symbiont. (B) Cell cycles and life cycles in prokaryotes, schematic. We recognize that there are spore-forming types, stalk-forming types, heterocyst-forming types, and other exceptions among prokaryotes. But in the main, we find it fair to generalize that the prokaryotic life cycle, if compared with the eukaryotic state, is a matter of continuously simultaneous cell and chromosome division.

Fig. 2.

Steps en route from endosymbiont acquisition to an ancestral cell cycle. Blue, red and gray represent bacterial, archaeal and eukaryotic components, respectively (see text).

Fig. 3.

(A) A coenocytic eukaryote common ancestor(Coeca) with multiple independently dividing nuclei. (B) Accidental budding off of spores using the archaeal vesicle secretion mechanisms. Only spores containing (at least) a complete genome enclosed within a nucleus and at least one (compatible) mitochondrion are viable. All other possibilities result in inviable spores, providing strong selection among spores for viable gene, chromosome and mitonuclear combinations.

Fig. 4.

Possible life cycles of a coenocytic eukaryotic common ancestor. Viable meiospores (yellow) that bud off the syncytium have two possibilities. They can either 1) germinate to a new syncytium and continue with a coenocytic life cycle with multiple nuclear divisions or 2) undergo cell division (spore secretion) immediately after nuclear division, a case of heterochrony (spore secretion before filament formation). If this results in viable progeny, they can undergo fusion, recombination and division, which are characteristic of meiotic lifecycles. Mitotic life cycles can be easily derived from bypassing the fusion (syngamy, karyogamy) and recombination phases of a meiotic life cycle (see also fig. 1).