PreprintCited by 36Protist diversity and phylogenyMicrobial Community Ecology and PhysiologyOrigins and Evolution of Life

Oxygen metabolism in descendants of the archaeal-eukaryotic ancestor

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Appler, Kathryn E., Lingford, James P., Gong, Xianzhe, Panagiotou, Kassiani, Leão, Pedro, Langwig, Marguerite, Greening, Chris, Ettema, Thijs J. G. +2 more·2024·Nature

Preprint — published as 10.1038/s41586-026-10128-z · Paper page

Abstract

Asgard archaea were pivotal in the origin of complex cellular life. Hodarchaeales (Asgardarchaeota class Heimdallarchaeia) were recently shown to be the closest relatives of eukaryotes. However, limited sampling of these archaea constrains our understanding of their ecology and evolution 1–3 , including their anticipated role in eukaryogenesis. Here, we nearly double the number of Asgardarchaeota metagenome-assembled genomes (MAGs) to 869, including 136 new Heimdallarchaeia (49 Hodarchaeales) and several novel lineages. Examining global distribution revealed Hodarcheales are primarily found in coastal marine sediments. Detailed analysis of their metabolic capabilities revealed guilds of Heimdallarchaeia are distinct from other Asgardarchaeota. These archaea encode hallmarks of aerobic eukaryotes, including electron transport chain complexes (III and IV), biosynthesis of heme, and response to reactive oxygen species (ROS). The predicted structural architecture of Heimdallarchaeia membrane-bound hydrogenases includes additional Complex-I-like subunits potentially increasing the proton motive force and ATP synthesis. Heimdallarchaeia genomes encode CoxD, which regulates the electron transport chain (ETC) in eukaryotes. Thus, key hallmarks for aerobic respiration may have been present in the Asgard-eukaryotic ancestor. Moreover, we found that Heimdallarchaeia is present in a variety of oxic marine environments. This expanded diversity reveals these Archaea likely conferred energetic advantages during early stages of eukaryogenesis, fueling cellular complexity.

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Authors
Appler, K. E., Lingford, J. P., Gong, X., Panagiotou, K., Leão, P., Langwig, M., Greening, C., Ettema, T. J. G., De Anda, V., & Baker, B. J.
Affiliations
  • University of Texas at Austin Marine Science Institute (US)
  • Monash University (AU)
  • Shandong University (CN)
  • Wageningen University & Research (NL)
  • Radboud University Nijmegen (NL)
  • University of Wisconsin–Madison (US)
Corresponding author
Baker, Brett J.
Venue
Nature
Publisher
openRxiv
Published
2024-07-04
Volume
652
Issue
8109
Pages
405-415
ISSN
0028-0836 (ISSN-L)
OpenAlex
W7130454864
Cited by
36
References
151
Citations by year
2026: 26 · 2025: 9 · 2024: 1
FWCI
53.74
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • Socio-Environmental Systems Modeling (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Keywords
Asgard archaea, eukaryotic origin, oxygen metabolism, aerobic respiration, hydrogen production, heme biosynthesis, reactive oxygen species scavenging, marine sediment, metagenome-assembled genomes
MeSH terms
Origin of Life, Aerobiosis, Archaea, Heme, Oxygen, Phylogeny, Reactive Oxygen Species, Geologic Sediments, Genome, Archaeal, Metagenome, Eukaryota

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