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).

Symbiogenesis, gradualism, and mitochondrial energy in eukaryote origin

“…Overexpress inert proteins without enzymatic activity? That would appear to be a possible option, at least one that is not immediately deadly, and it is the option that lineage leading to eukaryotes apparently took (116 ). It is a surprisingly common latent natural property of soluble proteins that they tend to aggregate into linear filaments with only minimal mutational perturbation (117).…”

“…The mitochondrial localization of ATP synthesis permits modern eukaryotes, and permitted the first eukaryotes, to explore the opportunity of protein overexpression that mitochondria afforded, because the intracellular concentration of ATP synthesis in mitochondria provided a cytosol with an increased space and a sufficient energy supply for protein tinkering. My proposition is thus that the mitochondrion arose in a prokaryotic host (41), that the mitochondrial energy configuration permitted that cell to become complex (a eukaryote) (54,116), and that a small population size was conducive to the traversal of that evolutionary transition (118).…”

“…Second, the paper suggests that the stem eukaryotic lineage acquired from prokaryotes the genes for the traits that make eukaryotes eukaryotic (a fully fledged endomembrane system, vesicle flux, nucleus, a true cytoskeleton, cell cycle, mitosis, meiosis, syngamy, karyogamy, sex, alternation of generations, etc. ), but prokaryotes do not have those traits, only eukaryotes do (23,116,143). How can eukaryotes acquire genes from donors that lack the traits to be acquired?…”

“…The symbiogenic version of eukaryote gene transfer is that eukaryotes acquired genes at the origins of mitochondria and chloroplasts and with the help of that genetic starting material plus its ensuing mutations (and mitochondrial energy), selection and differential loss set in to allow eukaryotes to evolve in a very normal Darwinian manner, at least one they had evolved meiosis (116), without the inheritance of acquired traits.…”

“…2f), namely that the host for the origin of mitochondria was a prokaryote, an archaeon, and that eukaryote specific traits arose as a consequence of that symbiosis (22, 23, 41, 54, 118). There are several versions of the idea that the host was an archaeon (reviewed in (45, 51)), though only one of those suggestions accounted for eukaryotic anaerobes (41), having been developed into a fuller theory that makes an earnest attempt to account for the origin of the nucleus (7), the eukaryotic endomembrane system (22), meiosis mitosis and sex (116).…”