Department of Ecology, Evolution and Natural Resources, Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, New Brunswick, 08901, USA.
Biol Direct. 2010 Aug 23;5:53. doi: 10.1186/1745-6150-5-53.
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.
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.
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.
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.
This manuscript was reviewed by Eugene V. Koonin, Anthony M. Poole, and Gáspár Jékely.
真核生物起源（真核发生）理论需要为定义这一谱系的各种复杂特征的出现提供统一的解释。提出原核生物到真核生物过渡模型的理论陷入了“吞噬作用优先”和“线粒体作为种子”两种对立范式之间的僵局，这两种范式都不能完全解释真核细胞复杂性的起源。性（减数分裂和有性生殖）是一个尚未在真核发生理论中得到满意解决的复杂特征的例子。减数分裂的祖先性质及其对真核细胞生物学的依赖表明，性和真核发生的出现是同时发生的，协同作用的，并且可能是由共同的选择压力来解释的。
我们提出，由于古代古菌微环境中的蓝细菌光合作用，氧气水平的局部升高对周围生物群具有高度毒性。这种选择压力促使一个古菌（古细菌）谱系转化为第一个真核生物。关键是，氧气可能与紫外线（UV）辐射和/或干燥等环境压力协同作用，导致活性氧（ROS）的积累。内共生体系统和获得线粒体等真核生物特征的出现被认为是应对细胞质膜代谢危机和 ROS 积累的策略。高效修复 ROS/UV 损伤 DNA 的选择压力推动了性的进化，这需要细胞融合、细胞骨架介导的染色体运动以及核膜的出现。我们的模型意味着性和真核发生的进化是不可分割的过程。
可以使用几种类型的数据来检验我们的假说。这些包括古生物学预测、模拟古代含氧微环境以及暴露于 ROS 和 UV 应激的古菌的细胞生物学实验。对古菌接合、原核生物 DNA 重组以及核介导减数分裂活动的普遍性的研究可能证实性和核的进化是为了支持 DNA 修复的假说。
氧气耐受性成为研究真核发生的重要原则。真核生物复杂性的进化可能最好理解为关键进化创新之间的协同过程，其中减数分裂（性）起着核心作用。
这份手稿由 Eugene V. Koonin、Anthony M. Poole 和 Gáspár Jékely 进行了审查。
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