Uniting sex and eukaryote origin in an emerging oxygenic world
Theories about eukaryote origin (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 hypothesisWe 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 acquisitionof 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 hypothesisSeveral 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 support the hypothesis that sex and the nucleus evolved to support DNA repair.Implications of the hypothesisOxygen 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.ReviewersThis manuscript was reviewed by Eugene V.
Koonin, Anthony M. Poole, and Gaspar Jekely.
Author: Jeferson GrossDebashish Bhattacharya
Credits/Source: Biology Direct 2010, 5:53
Published on: 2010-08-23
Copyright by the authors listed above - made available via BioMedCentral (Open Access). Please
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