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Three families of Asgard archaeal viruses identified in metagenome-assembled genomes

Nature Microbiology volume 7, pages 962–973 (2022)Cite this article

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Abstract

Asgardarchaeota harbour many eukaryotic signature proteins and are widely considered to represent the closest archaeal relatives of eukaryotes. Whether similarities between Asgard archaea and eukaryotes extend to their viromes remains unknown. Here we present 20 metagenome-assembled genomes of Asgardarchaeota from deep-sea sediments of the basin off the Shimokita Peninsula, Japan. By combining a CRISPR spacer search of metagenomic sequences with phylogenomic analysis, we identify three family-level groups of viruses associated with Asgard archaea. The first group, verdandiviruses, includes tailed viruses of the class Caudoviricetes (realm Duplodnaviria); the second, skuldviruses, consists of viruses with predicted icosahedral capsids of the realm Varidnaviria; and the third group, wyrdviruses, is related to spindle-shaped viruses previously identified in other archaea. More than 90% of the proteins encoded by these viruses of Asgard archaea show no sequence similarity to proteins encoded by other known viruses. Nevertheless, all three proposed families consist of viruses typical of prokaryotes, providing no indication of specific evolutionary relationships between viruses infecting Asgard archaea and eukaryotes. Verdandiviruses and skuldviruses are likely to be lytic, whereas wyrdviruses potentially establish chronic infection and are released without host cell lysis. All three groups of viruses are predicted to play important roles in controlling Asgard archaea populations in deep-sea ecosystems.

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Fig. 1: Phylogenomic tree of Asgardarchaeota.
Fig. 2: Description of the Asgardarchaeota CRISPR spacer dataset.
Fig. 3: Diversity of verdandiviruses.
Fig. 4: Diversity of skuldviruses.
Fig. 5: Diversity of wyrdviruses.
Fig. 6: Asgard archaeal viruses and MGEs.

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Data availability

The raw reads, as well as assembled virus and MGE genome sequences from the metagenomes described in this study, are available at NCBI under BioProject no. PRJDB12054, BioSample accession nos SAMD00394285–SAMD00394296. Accession numbers of the 20 MAGs assembled in the course of this study are listed in Supplementary Table 1. Accession numbers of the virus and MGE genome sequences are listed in Supplementary Table 3. Source data are provided with this paper.

Code availability

No custom code was used.

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Acknowledgements

We thank the crews, technical staff and shipboard scientists of the DV Chikyu for the operation and sampling during cruise CK06-06 in 2006. We thank M. Hirai and Y. Takaki for library construction, sequencing and data deposition of subseafloor samples off Shimokita. The work in the M.K. laboratory is supported by grants from l’Agence Nationale de la Recherche (nos. ANR-20-CE20-0009-02 and ANR-21-CE11-0001-01) and Ville de Paris (Emergence(s) project MEMREMA). S.M. was supported by the Metchnikov fellowship from Campus France and Russian Science Foundation (grant no. 19-74-20130). N.Y. and E.V.K. are supported by the Intramural Research Program of the National Institutes of Health of the USA (National Library of Medicine). The work of C.R. and J.S. is funded by the Australian Research Council Future Fellow Award (no. FT170100213, to CR). T.N. was partly supported by MEXT KAKENHI (grant nos. JP19H05684 within JP19H05679 (Post-Koch Ecology) and 16H06429, 16K21723 and 16H06437 (NeoVirology)).

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  1. Sofia Medvedeva

    Present address: Institut Pasteur, Université Paris Cité, CNRS UMR6047, Evolutionary Biology of the Microbial Cell Unit, Paris, France

Authors and Affiliations

  1. Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, France

    Sofia Medvedeva & Mart Krupovic

  2. Center of Life Science, Skolkovo Institute of Science and Technology, Moscow, Russia

    Sofia Medvedeva

  3. Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland, Australia

    Jiarui Sun & Christian Rinke

  4. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA

    Natalya Yutin & Eugene V. Koonin

  5. Research Center for Bioscience and Nanoscience, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan

    Takuro Nunoura

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Contributions

M.K. initiated the project and designed research. T.N. collected samples and extracted and sequenced DNA. J.S. and C.R. assembled, curated and analysed Asgard archaeal MAGs. S.M. assembled the Asgard archaeal CRISPR and viral datasets. S.M., N.Y., E.V.K. and M.K. analysed viral sequences. S.M. and M.K. wrote the manuscript with input from all authors.

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Correspondence to Takuro Nunoura, Christian Rinke or Mart Krupovic.

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Nature Microbiology thanks Susanne Erdmann, Hiroyuki Ogata and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Matches between asgardarchaeal CRISPR spacers and viruses.

The figure is divided into three blocks (green, red and blue) corresponding to the three groups of asgardarchaeal viruses, namely, verdandiviruses, skuldviruses and wyrdviruses. CRISPR repeats and spacers are indicated as diamonds and boxes, respectively. Spacers matching asgardarchaeal viruses are shown in yellow and are connected to the names of targeted viruses with arrows. Thick vertical lines connect related repeats and the exact pairwise sequence identities are indicated.

Extended Data Fig. 2 Partial provirus integrated within a genomic contig of Lokiarchaeia.

The verdandivirus-derived region is boxed. Homologous genes are shown using the same colors and the key is provided on the left of the figure. Housekeeping cellular genes are shown in black and include those encoding transcription factor S (TFS) and ribosomal proteins S7e, S12e, S27e, L30e and L44e. Grey shading connects genes displaying sequence similarity at the protein level, with the percent of sequence identity depicted with different shades of grey.

Extended Data Fig. 3 Maximum likelihood phylogenetic tree of Topo mini-A proteins.

Proteins of skuldviruses and wyrdviruses are shown in cyan and dark blue, respectively, whereas those encoded by other asgardarchaeal MGE are shown in red. Other Topo mini-A homologs encoded by archaea and bacteria (or their corresponding viruses) are shown in green and orange, respectively. Topo VI proteins were used as an outgroup and are colored grey. The tree was constructed using the automatic optimal model selection (LG+R5). The scale bar represents the number of substitutions per site. Circles at the nodes denote aLRT SH-like branch support values larger than 90%.

Source data

Extended Data Fig. 4 Sequence alignment of the major capsid proteins of selected wyrdviruses, fusellovirus SSV1 and halspivirus His1.

When available, proteins are identified with their accession numbers followed by a virus name. TMD, transmembrane domain.

Supplementary information

Supplementary Information

Supplementary text, references and Figs. 1–4.

Reporting Summary

Peer Review File

Supplementary Table

The file contains eight supplementary tables in a single workbook.

Supplementary Data 1

The file contains an output of the CRISPRdetect program.

Source data

Source Data Fig. 1

Sequence alignment and the tree file in Newick format.

Source Data Fig. 2

List of spacers used to prepare Fig. 2.

Source Data Fig. 3

Sequence alignment and the tree file in Newick format.

Source Data Extended Data Fig. 3

Sequence alignment and the tree file in Newick format.

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Medvedeva, S., Sun, J., Yutin, N. et al. Three families of Asgard archaeal viruses identified in metagenome-assembled genomes. Nat Microbiol 7, 962–973 (2022). https://doi.org/10.1038/s41564-022-01144-6

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