Expanded diversity of Asgard archaea and their relationships with eukaryotes

Yang Liu, Kira S. Makarova, Wen-Cong Huang, Yuri I. Wolf, Anastasia N. Nikolskaya, Xinxu Zhang, Mingwei Cai, Cui-Jing Zhang, Wei Xu, Zhuhua Luo, Lei Cheng, Eugene V. Koonin () and Meng Li ()
Additional contact information
Yang Liu: Shenzhen University
Kira S. Makarova: National Institutes of Health
Wen-Cong Huang: Shenzhen University
Yuri I. Wolf: National Institutes of Health
Anastasia N. Nikolskaya: National Institutes of Health
Xinxu Zhang: Shenzhen University
Mingwei Cai: Shenzhen University
Cui-Jing Zhang: Shenzhen University
Wei Xu: Third Institute of Oceanography, Ministry of Natural Resources
Zhuhua Luo: Third Institute of Oceanography, Ministry of Natural Resources
Lei Cheng: Biogas Institute of Ministry of Agriculture
Eugene V. Koonin: National Institutes of Health
Meng Li: Shenzhen University

Nature, 2021, vol. 593, issue 7860, 553-557

Abstract: Abstract Asgard is a recently discovered superphylum of archaea that appears to include the closest archaeal relatives of eukaryotes1–5. Debate continues as to whether the archaeal ancestor of eukaryotes belongs within the Asgard superphylum or whether this ancestor is a sister group to all other archaea (that is, a two-domain versus a three-domain tree of life)6–8. Here we present a comparative analysis of 162 complete or nearly complete genomes of Asgard archaea, including 75 metagenome-assembled genomes that—to our knowledge—have not previously been reported. Our results substantially expand the phylogenetic diversity of Asgard and lead us to propose six additional phyla that include a deep branch that we have provisionally named Wukongarchaeota. Our phylogenomic analysis does not resolve unequivocally the evolutionary relationship between eukaryotes and Asgard archaea, but instead—depending on the choice of species and conserved genes used to build the phylogeny—supports either the origin of eukaryotes from within Asgard (as a sister group to the expanded Heimdallarchaeota–Wukongarchaeota branch) or a deeper branch for the eukaryote ancestor within archaea. Our comprehensive protein domain analysis using the 162 Asgard genomes results in a major expansion of the set of eukaryotic signature proteins. The Asgard eukaryotic signature proteins show variable phyletic distributions and domain architectures, which is suggestive of dynamic evolution through horizontal gene transfer, gene loss, gene duplication and domain shuffling. The phylogenomics of the Asgard archaea points to the accumulation of the components of the mobile archaeal ‘eukaryome’ in the archaeal ancestor of eukaryotes (within or outside Asgard) through extensive horizontal gene transfer.

Date: 2021
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DOI: 10.1038/s41586-021-03494-3

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