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The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation

Abstract

Production of molecular oxygen was a turning point in the Earth’s history. The geological record indicates the Great Oxidation Event, which marked a permanent transition to an oxidizing atmosphere around 2.4 Ga. However, the degree to which oxygen was available to life before oxygenation of the atmosphere remains unknown. Here, phylogenetic analysis of all known oxygen-utilizing and -producing enzymes (O2-enzymes) indicates that oxygen became widely available to living organisms well before the Great Oxidation Event. About 60% of the O2-enzyme families whose birth can be dated appear to have emerged at the separation of terrestrial and marine bacteria (22 families, compared to two families assigned to the last universal common ancestor). This node, dubbed the last universal oxygen ancestor, coincides with a burst of emergence of both oxygenases and other oxidoreductases, thus suggesting a wider availability of oxygen around 3.1 Ga.

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Fig. 1: Dating the emergence of O2-enzymes.
Fig. 2: An example of the LUOA filtering process for family PF08007, Cupin_4.

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Data availability

Sequence alignments and phylogenetic trees analysed in this study can be found at https://figshare.com/projects/The_evolution_of_oxygen-utilizing_enzymes_suggests_early_biosphere_oxygenation/93818. All other data generated or analysed during this study are included in the published article (and its Supplementary File).

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Acknowledgements

We thank the Israel Science Foundation for funding (grant nos. 980/14 and 2575/20). This research was partially supported by the Israeli Council for Higher Education via the Weizmann Data Science Research Center and by a research grant from Madame Olga Klein – Astrachan. D.S.T. is the Leon and Nella Benoziyo Professor of Biochemistry. We thank S. Malik, D. Matelska and B. Ross for valuable comments on this manuscript and, especially, I. Halevy and P. Crockford, who inspired us to pursue this study and whose knowledge of palaeogeochemistry guided us throughout.

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J.J. and D.S.T. conceived and designed the study, performed the analysis and wrote the paper.

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Correspondence to Dan S. Tawfik.

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Jabłońska, J., Tawfik, D.S. The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation. Nat Ecol Evol 5, 442–448 (2021). https://doi.org/10.1038/s41559-020-01386-9

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