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Oxygen metabolism in descendants of the archaeal-eukaryotic ancestor

Abstract

Asgard archaea were pivotal in the origin of complex cellular life1. Heimdallarchaeia (a class within the phylum Asgardarchaeota) are inferred to be the closest relatives of eukaryotes. Limited sampling of these archaea constrains our understanding of their ecology and evolution2,3, including their role in eukaryogenesis. Here we use massive DNA sequencing of marine sediments to obtain 404 Asgardarchaeota metagenome-assembled genomes, including 136 new Heimdallarchaeia and several novel lineages. Analyses of their global distribution revealed they are widespread in marine environments, and many are enriched in variably oxygenated coastal sediments. Detailed metabolic reconstructions and structural predictions suggest that Heimdallarchaeia form metabolic guilds that are distinct from other Asgardarchaeota. These archaea encode hallmark proteins of an aerobic lifestyle, including electron transport chain complex (IV), haem biosynthesis and reactive oxygen species detoxification. Heimdallarchaeia also encode novel clades of respiratory membrane-bound hydrogenases with additional Complex I-like subunits, which potentially increase proton-motive force generation and ATP synthesis. Thus, we propose an updated Heimdallarchaeia-centric model of eukaryogenesis in which hydrogen production and aerobic respiration may have been present in the Asgard-eukaryotic ancestor. This expanded catalogue of Asgard archaeal genomic diversity suggests that bioenergetic factors influenced eukaryogenesis and constitutes a valuable resource for investigations into the origins and evolution of cellular complexity.

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Fig. 1: Expanded genomic diversity of Asgard archaea.
Fig. 2: Distribution of Asgardarchaeota based on the recovery of MAGs from a wide variety of habitats.
Fig. 3: Asgard archaea produce structurally diverse respiratory complexes.
Fig. 4: Increased complexity of the electron transport chain in Hodarchaeales (Heimdallarchaeia) compared to Lokiarchaeia.
Fig. 5: Eukaryogenesis in light of an expanded catalogue of Asgard genomes.

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Data availability

The genomic sequences associated with the study are deposited by the sequencing project in NCBI under BioProjects PRJNA743900 (BH), PRJNA692327 (GE2) and PRJNA1112871 (GE3). Supplementary Table 1 includes the BioProject identifiers, BioSample identifiers and genome accession numbers. Supplementary Tables 9 and 11 include lists of the visualized Protein Data Bank structures. All raw data underlying phylogenomic (alignments and resulting phylogenetic trees) and structural analyses have been deposited to Figshare https://figshare.com/s/f139faeb05653d1adf6b (ref. 108).

Code availability

Code used to generate our results has been deposited with the corresponding data to Figshare https://figshare.com/s/f139faeb05653d1adf6b (ref. 108).

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Acknowledgements

This study was supported by the Moore-Simons Project on the Origin of the Eukaryotic Cell, Simons Foundation grant 73592LPI (https://doi.org/10.46714/735925LPI) (T.J.G.E. and B.J.B.), Simons Foundation early career award 687165 (B.J.B.), and a Simons Foundation investigator award LI-SIAME-00002001 (B.J.B.). This research was also supported by National Natural Science Foundation of China (grant numbers 91951202 and 42006134) and Shandong University Foundation for Future Scholar Plan (to X.G.). Stengl-Wyer Graduate Fellowship, David Bruton, Jr Endowed Graduate Fellowship (University of Texas at Austin Graduate Continuing Fellowship), and James Howell Stuckey Scholarship Fund (to K.E.A.). National Health and Medical Research Council Emerging Leader Fellowship (APP1178715 to C.G.) and the Australian Research Council Future Fellowship (FT240100502 to C.G.). This work was supported by the European Research Council Consolidator and Advanced Grants 817834 and 101142180, respectively (T.J.G.E.) and by the Dutch Research Council VI.C.192.016 (T.J.G.E.). We thank SURF (https://www.surf.nl) for supporting the use of the National Supercomputer Snellius, facilitated through a grant from the Dutch Research Council (NWO-2021.059). We thank K. Sietz for her work on the assemblies in GE2; B. Contreras-Moreira for technical support in the GET_HOMOLOGUES analysis; the captain, crew and chief scientists of the research vessels Chuangxin Yi and Atlantis/HOV Alvin (GE2 Project 0647633; GE3 Project OCE-1357238) for their assistance with the Bohai Sea and Guaymas Basin sample collections, respectively; GE3 chief scientist A. Teske, and HOV Alvin pilots D. Forsman, J. Grau and A. Trantino who made this project possible. This work was supported by the MASSIVE HPC facility (www.massive.org.au). This is University of Texas Center for Planetary Systems Habitability (CPSH) contribution no. 0091.

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B.J.B., K.E.A. and V.D.A. conceptualized and designed the study. B.J.B., X.G. and T.J.G.E. acquired funding. B.J.B. and X.G. collected and provided environmental samples. K.E.A., V.D.A., X.G. and M.V.L. performed DNA extractions, metagenomic sequence assemblies and binning. K.E.A. collected environmental metadata and ran the functional annotation. K.E.A. and K.P. performed phylogenetic analyses. P.L. and J.P.L. ran AlphaFold2 predictions and performed structural analysis. K.E.A. conducted protein/gene phylogenetic analyses. K.E.A. and V.D.A. performed metabolic analyses. J.P.L. and C.G. designed and interpreted hydrogenase analyses. K.E.A. and B.J.B. led the writing, with J.P.L., K.P., C.G., T.J.G.E. and V.D.A. assisting with specific sections, and input from all authors. All authors edited and approved the manuscript.

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Correspondence to Brett J. Baker.

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This file contains Supplementary Methods, Supplementary Discussion, Supplementary Figs. 1–83, Supplementary Table 15, and Supplementary References. It provides additional details on sampling, database curation, phylogenomic and structural analyses, and metabolic descriptions. See the table of contents for a complete list of topics.

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Appler, K.E., Lingford, J.P., Gong, X. et al. Oxygen metabolism in descendants of the archaeal-eukaryotic ancestor. Nature 652, 405–415 (2026). https://doi.org/10.1038/s41586-026-10128-z

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