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Expanded diversity of Asgard archaea and their relationships with eukaryotes

Author

Listed:
  • 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)

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.

Suggested Citation

  • 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 & Meng Li, 2021. "Expanded diversity of Asgard archaea and their relationships with eukaryotes," Nature, Nature, vol. 593(7860), pages 553-557, May.
  • Handle: RePEc:nat:nature:v:593:y:2021:i:7860:d:10.1038_s41586-021-03494-3
    DOI: 10.1038/s41586-021-03494-3
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    Citations

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    Cited by:

    1. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Zhongyi Lu & Runyue Xia & Siyu Zhang & Jie Pan & Yang Liu & Yuri I. Wolf & Eugene V. Koonin & Meng Li, 2024. "Evolution of optimal growth temperature in Asgard archaea inferred from the temperature dependence of GDP binding to EF-1A," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    3. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Yan-Ling Qi & Ya-Ting Chen & Yuan-Guo Xie & Yu-Xian Li & Yang-Zhi Rao & Meng-Meng Li & Qi-Jun Xie & Xing-Ru Cao & Lei Chen & Yan-Ni Qu & Zhen-Xuan Yuan & Zhi-Chao Xiao & Lu Lu & Jian-Yu Jiao & Wen-She, 2024. "Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. David Moi & Shunsuke Nishio & Xiaohui Li & Clari Valansi & Mauricio Langleib & Nicolas G. Brukman & Kateryna Flyak & Christophe Dessimoz & Daniele de Sanctis & Kathryn Tunyasuvunakool & John Jumper & , 2022. "Discovery of archaeal fusexins homologous to eukaryotic HAP2/GCS1 gamete fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Clément Madru & Markel Martínez-Carranza & Sébastien Laurent & Alessandra C. Alberti & Maelenn Chevreuil & Bertrand Raynal & Ahmed Haouz & Rémy A. Meur & Marc Delarue & Ghislaine Henneke & Didier Flam, 2023. "DNA-binding mechanism and evolution of replication protein A," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Zhiguang Qiu & Li Yuan & Chun-Ang Lian & Bin Lin & Jie Chen & Rong Mu & Xuejiao Qiao & Liyu Zhang & Zheng Xu & Lu Fan & Yunzeng Zhang & Shanquan Wang & Junyi Li & Huiluo Cao & Bing Li & Baowei Chen & , 2024. "BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Susheel Bhanu Busi & Massimo Bourquin & Stilianos Fodelianakis & Grégoire Michoud & Tyler J. Kohler & Hannes Peter & Paraskevi Pramateftaki & Michail Styllas & Matteo Tolosano & Vincent Staercke & Mar, 2022. "Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Jonathan Filée & Hubert F. Becker & Lucille Mellottee & Rima Zein Eddine & Zhihui Li & Wenlu Yin & Jean-Christophe Lambry & Ursula Liebl & Hannu Myllykallio, 2023. "Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Carolien Bastiaanssen & Pilar Bobadilla Ugarte & Kijun Kim & Giada Finocchio & Yanlei Feng & Todd A. Anzelon & Stephan Köstlbacher & Daniel Tamarit & Thijs J. G. Ettema & Martin Jinek & Ian J. MacRae , 2024. "RNA-guided RNA silencing by an Asgard archaeal Argonaute," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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