Exploring Asgard archaea and their relationships with Eukaryotes

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The discovery of the Lokiarchaeota in 2015 by Thijs Ettema’s lab (then, in Uppsala University and now in Wageningen University) [1] and the subsequent exploration and mining of the diverse Asgard archaea in natural environments have dramatically changed our understanding of the origin of eukaryotes. The discovery of Asgard archaea has led biologists to wonder whether they are our mother or sister. It has become a major research interest to many laboratories worldwide, including my lab in Shenzhen University, China, and Eugene V. Koonin’s group at the National Institutes of Health, USA. Our collaboration started after the Gordon Research Conference on Archaea in Les Diablerets, Switzerland, in 2019, when I gave a short talk about transcriptionally active Asgard archaea in mangrove sediments, and Eugene was the Discussion Leader of that session. My group and colleagues have collected seawater and sediment samples from various places in China and the open sea. We have identified plenty of Asgard archaea metagenome-assembled genomes (MAGs), revealing several putative novel lineages, and we were incessantly fascinated by the possibility that the newly discovered Asgard archaea could shake the tree of life and shed new light on the relationship between Archaea and Eukaryotes. So Eugene, Kira and I had a wonderful conversation during the GRC conference, and afterwards, we immediately launched a broad scope collaboration on the comprehensive phylogeny and comparative genomics [2], physiological and biochemical function [3], and CRISPR-Cas systems [4] of Asgard archaea. 

The photo of Meng Li, Kira Makarova, and Eugene Koonin at the Gordon Research Conference on Archaea, Switzerland 2019.

Asgard is the fourth superphylum of the Archaea domain, which initially included five phyla, including Loki-, Thor-, Odin-, Heimdall- and Helarchaeota [5,6]. My group identified the sixth Asgard archaea phylum named Gerdarchaeota in mangrove sediments in early of 2020 [7]. In collaboration with Eugene’s group, we present 75 novel Asgard MAGs, which substantially expand the phylogenetic diversity of Asgard, and propose six additional phyla. Five phyla are named after the Norse deities, i.e., Hermod- [8], Baldr-, Borr-, Kari-, Hod- and a deep branch Wukongarchaeota is named after the Chinese mythological character “The Monkey King – Sun Wukong”, who created a tremendous uproar in the heavenly palace [9].

Cartoon showing the expanded Asgard archaea. The characters standing on the somersault cloud are representing Borrarchaeota, Baldrarchaeota, Hodarchaeota, Wukongarchaeota, Kariarchaeota, Gerdarchaeota and Hermodarchaeota (from left to right).

In this study, we constructed a tree of life with high species coverage and systematically analyzed the evolutionary relationships between Asgard archaea and eukaryotes. We made a strong effort to assess the robustness of the phylogeny with respect to the selection of species and conserved marker genes. The phylogenetic results are best compatible with the origin of eukaryotes from within Asgard, from a common ancestor with the Heimdal-Wukong branch, but do not rule out a deeper branch for the eukaryote ancestor within archaea. We also identified a major expansion of eukaryotic signature proteins (ESPs) among the twelve phyla of Asgard archaea. The patchy distribution and variable domain architectures of Asgard ESPs suggest a dynamic evolutionary history of Asgard archaea.

The metabolic reconstruction suggests that Wukongarchaeota is an obligate hydrogenotrophic acetogen, which is dramatically different from other known Asgard archaea. This is the reason why we decided to name it after a Chinese mythological character, the departure from the Norse Pantheon for Asgard archaea. We hope Wukong gets along with the Norse deities in Asgard… even with Loki.

The results of our phylogenomic analysis substantially broaden our understanding of the complex evolutionary history of Asgard archaea and the Asgard-Eukaryote relationship. However, further efforts, including hunting for unknown archaeal lineages, verification by strain enrichment/cultivation, and physiological/biochemical experiments, are certainly essential. The collaborative team in Shenzhen and Bethesda is forging ahead towards our goal to unveil the mysterious archaea.

Amidst the devastating pandemic, this story is a poignant reminder to all of us that, the tremendous power of online communication notwithstanding, serendipitous exchange of ideas at actual meetings is indispensable for the progress of science. We hope and trust it resumes soon!

To get more information, please read our paper at https://www.nature.com/articles/s41586-021-03494-3

References

[1] Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173-179 (2015)

[2] Liu, Y. et al. Expanded diversity of Asgard archaea and their relationships with eukaryotes. Nature, (2021) https://doi.org/10.1038/s41586-021-03494-3

[3] Lu, Z. et al. Coevolution of eukaryote-like Vps4 and ESCRT-III subunits in the Asgard archaea. mBio 11, e00417-20 (2020)

[4] Makarova, K. S. et al. Unprecedented diversity of unique CRISPR-Cas-related systems and Cas1 homologs in Asgard archaea. The CRISPR Journal 3, 156-163 (2020)

[5] Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353-358 (2017)

[6] Seitz, K. W. et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat. Commun. 10:1822 (2019)

[7] Cai, M. et al. Diverse Asgard archaea including the novel phylum Gerdarchaeotaparticipate in organic matter degradation. Sci. China Life Sci. 63, 886-897 (2020)

[8] Zhang, J. W. et al. Newly discovered Asgard archaea Hermodarchaeota potentially degrade alkanes and aromatics via alkyl/benzyl-succinate synthase and benzoyl-CoA pathway. ISME J, (2021) https://doi.org/10.1038/s41396-020-00890-x

[9] Wu, C. Journey to the West (1592) (Monkey: A Folk-Tale of China, an abridged translation published in 1942 by Arthur Waley, Publisher: Allen and Unwin)

Meng Li

Professor, Shenzhen University

Microbial Ecology, Metagenomics, Archaea

Comments

Go to the profile of Xing-Xing Shen
7 months ago

The cartoon is incredibly beautiful! Congrats Dr. Li