4.5 Review

Eukaryogenesis and oxygen in Earth history

期刊

NATURE ECOLOGY & EVOLUTION
卷 6, 期 5, 页码 520-532

出版社

NATURE PORTFOLIO
DOI: 10.1038/s41559-022-01733-y

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资金

  1. Agouron Institute Geobiology Postdoctoral Fellowship programme [AI-F-GB53.19.2]
  2. Natural Environment Research Council [NE/P013651/1, NE/P013678/1]
  3. Biotechnology and Biological Sciences Research Council [BB/T012773/1]
  4. John Templeton Foundation [62220]
  5. Leverhulme Trust [RF-2022-167]
  6. Gordon and Betty Moore Foundation [GBMF9741]
  7. European Union [764840]
  8. NERC [NE/P013651/1] Funding Source: UKRI

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The origin of mitochondria and the oxygenation of Earth have been found to be decoupled by recent research. The authors review the literature and conclude that eukaryogenesis and the rise of oxygen were separate events, and that obligate aerobiosis in eukaryotes only became widespread in the past 1 billion years.
The endosymbiotic origin of mitochondria during eukaryogenesis has long been viewed as an adaptive response to the oxygenation of Earth's surface environment, presuming a fundamentally aerobic lifestyle for the free-living bacterial ancestors of mitochondria. This oxygen-centric view has been robustly challenged by recent advances in the Earth and life sciences. While the permanent oxygenation of the atmosphere above trace concentrations is now thought to have occurred 2.2 billion years ago, large parts of the deep ocean remained anoxic until less than 0.5 billion years ago. Neither fossils nor molecular clocks correlate the origin of mitochondria, or eukaryogenesis more broadly, to either of these planetary redox transitions. Instead, mitochondria-bearing eukaryotes are consistently dated to between these two oxygenation events, during an interval of pervasive deep-sea anoxia and variable surface-water oxygenation. The discovery and cultivation of the Asgard archaea has reinforced metabolic evidence that eukaryogenesis was initially mediated by syntrophic H-2 exchange between an archaeal host and an alpha-proteobacterial symbiont living under anoxia. Together, these results temporally, spatially and metabolically decouple the earliest stages of eukaryogenesis from the oxygen content of the surface ocean and atmosphere. Rather than reflecting the ancestral metabolic state, obligate aerobiosis in eukaryotes is most probably derived, having only become globally widespread over the past 1 billion years as atmospheric oxygen approached modern levels. For decades, the origin of mitochondria during eukaryogenesis has been viewed as a response to Earth's oxygenation, but this has been challenged by more recent research. Here, the authors review recent literature, concluding that eukaryogenesis and the rise of oxygen were decoupled, and obligate aerosis in eukaryotes has only become widespread in the past 1 billion years

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