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.
This is a preview of subscription content, access via your institution
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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).
Raymond, J. & Segrè, D. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764–1767 (2006).
Holland, H. D. The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. Lond. B https://doi.org/10.1098/rstb.2006.1838 (2006).
Holland, H. D. Volcanic gases, black smokers, and the great oxidation event. Geochim. Cosmochim. Acta 66, 3811–3826 (2002).
Farquhar, J., Bao, H. & Thiemens, M. Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–758 (2000).
Kasting, J. F. & Howard, M. T. Atmospheric composition and climate on the early Earth. Philos. Trans. R. Lond. Soc. B 361, 1733–1741 (2006).
Olson, S. L., Kump, L. R. & Kasting, J. F. Quantifying the areal extent and dissolved oxygen concentrations of Archean oxygen oases. Chem. Geol. 362, 35–43 (2013).
Lalonde, S. V. & Konhauser, K. O. Benthic perspective on Earth’s oldest evidence for oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 112, 995–1000 (2015).
Duan, Y. et al. A whiff of oxygen before the great oxidation event? Science 317, 1903–1906 (2007).
Jabłońska, J. & Tawfik, D. S. The number and type of oxygen-utilizing enzymes indicates aerobic vs. anaerobic phenotype. Free Radic. Biol. Med. 140, 84–92 (2019).
Sousa, F. L., Nelson-Sathi, S. & Martin, W. F. One step beyond a ribosome: the ancient anaerobic core. Biochim. Biophys. Acta Bioenerg. 1857, 1027–1038 (2016).
Das, A., Silaghi-Dumitrescu, R., Ljungdahl, L. G. & Kurtz, D. M. Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica. J. Bacteriol. 187, 2020–2029 (2005).
Ettwig, K. F. et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464, 543–548 (2010).
Slesak, I., Slesak, H. & Kruk, J. Oxygen and hydrogen peroxide in the early evolution of life on earth: in silico comparative analysis of biochemical pathways. Astrobiology 12, 775–784 (2012).
Ouzounis, C. A., Kunin, V., Darzentas, N. & Goldovsky, L. A minimal estimate for the gene content of the last universal common ancestor – exobiology from a terrestrial perspective. Res. Microbiol. 157, 57–68 (2006).
Hofbauer, S., Schaffner, I., Furtmüller, P. G. & Obinger, C. Chlorite dismutases – a heme enzyme family for use in bioremediation and generation of molecular oxygen. Biotechnol. J. 9, 461–473 (2014).
Kanehisa, M. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).
Gribaldo, S., Talla, E. & Brochier-Armanet, C. Evolution of the haem copper oxidases superfamily: a rooting tale. Trends Biochem. Sci. 34, 375–381 (2009).
Fischer, W. W., Hemp, J. & Johnson, J. E. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44, 647–683 (2016).
Battistuzzi, F. U. & Hedges, S. B. A major clade of prokaryotes with ancient adaptations to life on land. Mol. Biol. Evol. 26, 335–343 (2009).
Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).
Giovannelli, D. et al. Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans. eLife 6, e18990 (2017).
Bansal, M. S., Wu, Y.-C., Alm, E. J. & Kellis, M. Improved gene tree error correction in the presence of horizontal gene transfer. Bioinformatics 31, 1211–1218 (2015).
Gribaldo, S. & Brochier, C. Phylogeny of prokaryotes: does it exist and why should we care? Res. Microbiol. 160, 513–521 (2009).
Nelson-Sathi, S. et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517, 77–80 (2015).
Fuchsman, C. A., Collins, R. E., Rocap, G. & Brazelton, W. J. Effect of the environment on horizontal gene transfer between bacteria and archaea. PeerJ. 2017, e3865 (2017).
Garushyants, S. K., Kazanov, M. D. & Gelfand, M. S. Horizontal gene transfer and genome evolution in Methanosarcina. BMC Evol. Biol. 15, 102 (2015).
Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).
Maxwell Burroughs, A., Glasner, M. E., Barry, K. P., Taylor, E. A. & Aravind, L. Oxidative opening of the aromatic ring: tracing the natural history of a large superfamily of dioxygenase domains and their relatives. J. Biol. Chem. 294, 10211–10235 (2019).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
Cardona, T., Sánchez-Baracaldo, P., Rutherford, A. W. & Larkum, A. W. Early Archean origin of Photosystem II. Geobiology 17, 127–150 (2019).
Granold, M., Hajieva, P., Toşa, M. I., Irimie, F. D. & Moosmann, B. Modern diversification of the amino acid repertoire driven by oxygen. Proc. Natl Acad. Sci. USA 115, 41–46 (2018).
Gray, H. B. & Winkler, J. R. Living with oxygen. Acc. Chem. Res. 51, 1850–1857 (2018).
Fournier, G. P. & Alm, E. J. Ancestral reconstruction of a pre-LUCA aminoacyl-tRNA synthetase ancestor supports the late addition of Trp to the genetic code. J. Mol. Evol. 80, 171–185 (2015).
De Pouplana, L. R., Frugier, M., Quinn, C. L. & Schimmel, P. Evidence that two present-day components needed for the genetic code appeared after nucleated cells separated from eubacteria. Proc. Natl Acad. Sci. USA 93, 166–170 (1996).
Waldbauer, J. R., Newman, D. K. & Summons, R. E. Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc. Natl Acad. Sci. USA 108, 13409–13414 (2011).
Weiss, M. C., Preiner, M., Xavier, J. C., Zimorski, V. & Martin, W. F. The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genet. 14, e1007518 (2018).
Berkemer, S. J. & McGlynn, S. E. A new analysis of archaea–bacteria domain separation: variable phylogenetic distance and the tempo of early evolution. Mol. Biol. Evol. 37, 2332–2340 (2020).
Ślesak, I., Ślesak, H., Zimak-Piekarczyk, P. & Rozpądek, P. Enzymatic antioxidant systems in early anaerobes: theoretical considerations. Astrobiology 16, 348–358 (2016).
Juty, N. S., Moshiri, F., Merrick, M., Anthony, C. & Hill, S. The Klebsiella pneumoniae cytochrome bd’ terminal oxidase complex and its role in microaerobic nitrogen fixation. Microbiology 143, 2673–2683 (1997).
Jay, Z. J. et al. Predominant Acidilobus-like populations from geothermal environments in Yellowstone National Park exhibit similar metabolic potential in different hypoxic microbial communities. Appl. Environ. Microbiol. 80, 294–305 (2014).
Falcón, L. I., Magallón, S. & Castillo, A. Dating the cyanobacterial ancestor of the chloroplast. ISME J. 4, 777–783 (2010).
Shih, P. M., Hemp, J., Ward, L. M., Matzke, N. J. & Fischer, W. W. Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15, 19–29 (2017).
Betts, H. C. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018).
Magnabosco, C., Moore, K. R., Wolfe, J. M. & Fournier, G. P. Dating phototrophic microbial lineages with reticulate gene histories. Geobiology 16, 179–189 (2018).
Gumsley, A. P. et al. Timing and tempo of the great oxidation event. Proc. Natl Acad. Sci. USA 114, 1811–1816 (2017).
Luo, G. et al. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).
Farquhar, J. & Wing, B. A. Multiple sulfur isotopes and the evolution of the atmosphere. Earth Planet. Sci. Lett. 213, 1–13 (2003).
Wang, X. et al. A Mesoarchean shift in uranium isotope systematics. Geochim. Cosmochim. Acta 238, 438–452 (2018).
Planavsky, N. J. et al. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat. Geosci. 7, 283–286 (2014).
Crowe, S. A. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).
Eickmann, B. et al. Isotopic evidence for oxygenated Mesoarchaean shallow oceans. Nat. Geosci. 11, 133–138 (2018).
Albut, G. et al. Modern rather than Mesoarchaean oxidative weathering responsible for the heavy stable Cr isotopic signatures of the 2.95 Ga old Ijzermijn iron formation (South Africa). Geochim. Cosmochim. Acta 228, 157–189 (2018).
Catling, D. C. & Zahnle, K. J. The Archean atmosphere. Sci. Adv. 6, eaax1420 (2020).
Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).
Bairoch, A. The ENZYME database in 2000. Nucleic Acids Res. 28, 304–305 (2000).
Alborzi, S. Z., Devignes, M. D. & Ritchie, D. W. ECDomainMiner: discovering hidden associations between enzyme commission numbers and Pfam domains. BMC Bioinform. 18, 107 (2017).
Raymond, J. & Blankenship, R. E. Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2, 199–203 (2004).
Gygli, G., Lucas, M. F., Guallar, V. & van Berkel, W. J. H. The ins and outs of vanillyl alcohol oxidase: identification of ligand migration paths. PLoS Comput. Biol. 13, e1005787 (2017).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
Tria, F. D. K., Landan, G. & Dagan, T. Phylogenetic rooting using minimal ancestor deviation. Nat. Ecol. Evol. 1, 193 (2017).
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.
The authors declare no competing interests.
Peer review information Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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
This article is cited by
Antioxidant enzymes that target hydrogen peroxide are conserved across the animal kingdom, from sponges to mammals
Scientific Reports (2023)
Antibiotic hyper-resistance in a class I aminoacyl-tRNA synthetase with altered active site signature motif
Nature Communications (2023)
Replicated life-history patterns and subsurface origins of the bacterial sister phyla Nitrospirota and Nitrospinota
The ISME Journal (2023)
Nature Reviews Molecular Cell Biology (2022)
Nature Ecology & Evolution (2022)