Uniting sex and eukaryote origins in an emerging oxygenic world

Abstract

Background: Theories about eukaryote origins (eukaryogenesis) need to provide unified explanations for the emergence of diverse complex features that define this lineage. Models that propose a prokaryote-to-eukaryote transition are gridlocked between the opposing "phagocytosis first" and "mitochondria as seed" paradigms, neither of which fully explain the origins of eukaryote cell complexity. Sex (outcrossing with meiosis) is an example of an elaborate trait not yet satisfactorily addressed in theories about eukaryogenesis. The ancestral nature of meiosis and its dependence on eukaryote cell biology suggest that the emergence of sex and eukaryogenesis were simultaneous and synergic and may be explained by a common selective pressure.

Presentation of the hypothesis: We propose that a local rise in oxygen levels, due to cyanobacterial photosynthesis in ancient Archean microenvironments, was highly toxic to the surrounding biota. This selective pressure drove the transformation of an archaeal (archaebacterial) lineage into the first eukaryotes. Key is that oxygen might have acted in synergy with environmental stresses such as ultraviolet (UV) radiation and/or desiccation that resulted in the accumulation of reactive oxygen species (ROS). The emergence of eukaryote features such as the endomembrane system and acquisition of the mitochondrion are posited as strategies to cope with a metabolic crisis in the cell plasma membrane and the accumulation of ROS, respectively. Selective pressure for efficient repair of ROS/UV-damaged DNA drove the evolution of sex, which required cell-cell fusions, cytoskeleton-mediated chromosome movement, and emergence of the nuclear envelope. Our model implies that evolution of sex and eukaryogenesis were inseparable processes.

Testing the hypothesis: Several types of data can be used to test our hypothesis. These include paleontological predictions, simulation of ancient oxygenic microenvironments, and cell biological experiments with Archaea exposed to ROS and UV stresses. Studies of archaeal conjugation, prokaryotic DNA recombination, and the universality of nuclear-mediated meiotic activities might corroborate the hypothesis that sex and the nucleus evolved to support DNA repair.

Implications of the hypothesis: Oxygen tolerance emerges as an important principle to investigate eukaryogenesis. The evolution of eukaryotic complexity might be best understood as a synergic process between key evolutionary innovations, of which meiosis (sex) played a central role.

Reviewers: This manuscript was reviewed by Eugene V. Koonin, Anthony M. Poole, and Gáspár Jékely.

Figure 1

Evolution of the endomembrane system, mitochondrion, and eukaryote cell size. A - F. Model for evolution of the endomembrane system in response to imbalances in plasma membrane activities. Archaeal cells, containing co-translationally active ribosomes, are exposed to an environmental stressor (here exemplified by external H₂O₂, orange background, although UV radiation and/or desiccation may provide additional sources of stress). The plasma membrane was particularly affected by this external injury. As a result of the peripheral damage, a vesicle carrying molecular components (e.g., ribosomes) pinched off from the plasma membrane and accumulated in the inner cell, giving rise to the proto-ER. H₂O₂ that infiltrated the cell was cleared by enzymes (e.g., catalases and peroxidases). This generated a protected intracellular zone (white) that allowed proliferation of the proto-ER and associated ribosomes, while H₂O₂-damaged co-translational targeting gradually disappeared from the plasma membrane. Vesicular traffic, scaffolded by the incipient cytoskeleton (microtubule-organizing center and microtubules in red), emerged as an exocytic avenue to target ER-synthesized proteins to the plasma membrane (E and F). G - K. Putative model for early events in mitochondrial evolution. In a biofilm, archaeal and alphaprotobacterial cells are juxtaposed in a syntrophic association (arrows). Fusogenic and membrane remodeling activities necessary for cell-cell fusions during archaeal mating allowed the capture and retention of the alphaproteobacterium precursor of mitochondria. Environmental O₂ (blue background) penetrates the cells and is photo-activated to ROS by UV. Alphaproteobacterial aerobic respiration clears the intracellular O₂ (white zones). Intracellular mitochondria propagate and deliver ATP to the cytoplasm (J and H). Increase in cell size (E, F and J, K) emerges as a crucial eukaryotic strategy to counterbalance the influx of oxygenic species.

Figure 2

A putative model for the evolution of meiosis from archaeal conjugation. A. Ancestral archaeal conjugation (as described in H. volcanii) involving cell fusions, bidirectional flow of plasmids, and recombination between parental chromosomes (dark blue and green, respectively) [51,52]. B and C. Chromosome linearization permitted efficient pairing of homologues and resolution of crossovers [11,67]. Telomeres (orange) evolved to protect chromosome termini and to nucleate the pairing of homologues [11,67]. A centromere (orange region in the centre of chromosomes) served as a connection between sister chromatids and as an attachment site, via kinetochores, for the meiotic spindles [11,13,99]. This consisted of a network of microtubules (red fibers) radiating from a microtubule-organizing center (red circle) that guided chromosome movement [11,13,99]. The proto-ER progressively (B - F) differentiated into the NE [26] by wrapping segments of chromosomes to scaffold chromosome pairing (B - E) and to constrain diffusion of broken chromosome segments (C). D. Spindle-mediated movements approximate parental chromosomes during mating [10,12]. E. Incipient karyogamy mechanics evolved to fuse proto-NE segments associated with chromosomes to create a common membrane platform to assemble, via clustering of telomeres, the meiotic bouquet [11,13,67]. F. Cytokinesis based on an actomyosin contractile ring (red) facilitated splitting of the fusion partners (i.e., reductional meiotic division) [99]. NE enclosed the nuclear compartment when nuclear pores (yellow cylinders) evolved to ensure nucleo-cytoplasmic traffic of proteins and RNA [26].