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Energetics and evolution of anaerobic microbial eukaryotes

Nature Microbiology volume 8, pages 197–203 (2023)Cite this article

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Abstract

Mitochondria and aerobic respiration have been suggested to be required for the evolution of eukaryotic cell complexity. Aerobic respiration is several times more energetically efficient than fermentation. Moreover, aerobic respiration occurs at internalized mitochondrial membranes that are not constrained by a sublinear scaling with cell volume. However, diverse and complex anaerobic eukaryotes (for example, free-living and parasitic unicellular, and even small multicellular, eukaryotes) that exclusively rely on fermentation for energy generation have evolved repeatedly from aerobic ancestors. How do fermenting eukaryotes maintain their cell volumes and complexity while relying on such a low energy-yielding process? Here I propose that reduced rates of ATP generation in fermenting versus respiring eukaryotes are compensated for by longer cell cycles that satisfy lifetime energy demands. A literature survey and growth efficiency calculations show that fermenting eukaryotes divide approximately four to six times slower than aerobically respiring counterparts with similar cell volumes. Although ecological advantages such as competition avoidance offset lower growth rates and yields in the short term, fermenting eukaryotes inevitably have fewer physiological and ecological possibilities, which ultimately constrain their long-term evolutionary trajectories.

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Fig. 1: Environmental and phylogenetic diversity of anaerobic eukaryotes.
Fig. 2: The lifetime energy requirements of both aerobic and anaerobic eukaryotic cells are a function of their metabolic rates and division times.
Fig. 3: Anaerobic eukaryotes divide several times more slowly than their aerobic counterparts.
Fig. 4: Anaerobes dissimilate most of their ingested carbon.

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Acknowledgements

I thank P. Schavemaker and M. Lynch (Arizona State University), and M. Leger (Institute of Evolutionary Biology, Barcelona) for providing comments on this manuscript. I apologize to those whose important contributions to the diversity of anaerobic eukaryotes have not been cited due to space constraints. This project was supported by an EMBO Postdoctoral Fellowship (ALTF 21-2020).

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  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, USA

    Sergio A. Muñoz-Gómez

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Correspondence to Sergio A. Muñoz-Gómez.

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Nature Microbiology thanks Courtney Stairs and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Tables 1 and 2

Table 1 Anaerobes (this study). Table 2 Aerobes (Fenchel, 1983).

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Muñoz-Gómez, S.A. Energetics and evolution of anaerobic microbial eukaryotes. Nat Microbiol 8, 197–203 (2023). https://doi.org/10.1038/s41564-022-01299-2

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