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Eukaryogenesis and oxygen in Earth history

Nature Ecology & Evolution volume 6, pages 520–532 (2022)Cite this article

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Abstract

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 H2 exchange between an archaeal host and an α-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.

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Fig. 1: Models of eukaryogenesis.
Fig. 2: The many ancestors of eukaryotes.
Fig. 3: Correlated fossil, molecular and geochemical timeline.

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Acknowledgements

D.B.M. acknowledges the instruction and influence of L. Margulis, conversations with B. Martin, J. Brocks, M. Fakhraee, A. Bauer, S. Crowe, N. Planavsky and L. Tarhan, as well as the Agouron Institute for their 2019 meeting on the Origin of Eukaryotes. We acknowledge funding from the Agouron Institute Geobiology Postdoctoral Fellowship programme (#AI-F-GB53.19.2 to D.B.M.), the Natural Environment Research Council (NE/P013651/1 to R.A.B., S.J.D. and T.M.L.; NE/P013678/1 to D.P. and P.C.J.D.), the Biotechnology and Biological Sciences Research Council (BB/T012773/1 to P.C.J.D.), the John Templeton Foundation (#62220 to R.A.B., S.J.D., D.P., P.C.J.D. and T.M.L., although the opinions expressed in this paper are those of the authors and not those of the John Templeton Foundation), the Leverhulme Trust (#RF-2022-167 to P.C.J.D), the Gordon and Betty Moore Foundation (GBMF9741 to D.P. and P.C.J.D.), and European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement (764840 to D.P.).

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Authors and Affiliations

  1. Department of Geological Sciences, Stanford University, Stanford, CA, USA

    Daniel B. Mills & Erik A. Sperling

  2. Department of Biology, Portland State University, Portland, OR, USA

    Daniel B. Mills

  3. The Penn State Extraterrestrial Intelligence Center, The Pennsylvania State University, University Park, PA, USA

    Daniel B. Mills

  4. Global Systems Institute, University of Exeter, Exeter, UK

    Richard A. Boyle, Stuart J. Daines & Timothy M. Lenton

  5. Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK

    Davide Pisani & Philip C. J. Donoghue

  6. School of Biological Sciences, University of Bristol, Bristol, UK

    Davide Pisani

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D.B.M. conceived the study and wrote the paper with contributions from R.A.B., S.J.D., E.A.S., D.P., P.C.J.D. and T.M.L.

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Mills, D.B., Boyle, R.A., Daines, S.J. et al. Eukaryogenesis and oxygen in Earth history. Nat Ecol Evol 6, 520–532 (2022). https://doi.org/10.1038/s41559-022-01733-y

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