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Eukaryotes were shaped by Oxygen

Nature Ecology & Evolution volume 6, page 1242 (2022)Cite this article

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To the editor — Though I thoroughly enjoyed reading ‘Eukaryogenesis and oxygen in Earth history’ by Daniel B. Mills and co-workers1, as a review, it left something to be desired. I will deal with two issues here. First of all, while the article, to my mind correctly, focuses on symbiogenic theories, it seems overly biased towards favouring the hydrogen hypothesis of Muller and Martin2. As such, this is understandable, because with its publication of the first well-constructed theory explaining eukaryogenesis only starting with interactions between prokaryotes (an archaeon and a bacterium to be precise), the concept of symbiogenesis entered mainstream scientific discourse. However, recent insights have weakened some of the arguments used with its proposal. First, the hydrogen hypothesis was partly based on the analysis of rare eukaryotic organisms that had hydrogenosomes instead of mitochondria, with their presence in unrelated eukaryotic groups interpreted as evidence of ancient, common ancestry, implying that the original ancestor of mitochondria had hydrogen-generating potential2. This common ancestry is also claimed by Mills et al1. However, there are strong indications that all these examples are derived states of secondary anaerobic lifestyles enabled by horizontal gene transfer3,4. Another weakness of the hypothesis is the absence of any trace of this metabolic pathway when we reconstruct the last eukaryotic common ancestor (LECA) from our ever-expanding gene trees. In this respect, hydrogen generation resembles phagocytosis, which was also posited to be present in LECA (to explain bacterial uptake), but now seems to have evolved later in several independent instances5. Alternative syntrophic theories abound, and quite a few are expertly discussed in the review. Here I would only mention that Margulis’ earlier (alas, serial) endosymbiotic theory6 already pegged the progenitor of mitochondria as an oxidative bacterium and that new syntrophic theories try to deduce the original interactions from current metabolic exchanges between mitochondrion and cytoplasm7.

Not only is the focus on hydrogen-based syntrophy for the initial symbiosis rather arbitrary, it also has the unfortunate corollary of neglecting or downplaying the crucial role that molecular oxygen played during eukaryogenesis. One recent example is the downward recalculation of ATP generated using molecular oxygen as the final acceptor in the light of the cellular investments needed to prevent and repair damage from its reactive oxygen species (ROS) side products3,8. However, this is just another way of describing one of the main driving forces behind the enormous increase in complexity occurring during eukaryogenesis, which can be conceived of as ‘adapting to life with oxygen’.

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  1. Amsterdam UMC, Department of Medical Biochemistry, University of Amsterdam, Amsterdam, The Netherlands

    Dave Speijer

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Correspondence to Dave Speijer.

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Speijer, D. Eukaryotes were shaped by Oxygen. Nat Ecol Evol 6, 1242 (2022). https://doi.org/10.1038/s41559-022-01819-7

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