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

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.

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.

References

  1. Liu, Y. et al. Expanded diversity of Asgard archaea and their relationships with eukaryotes. Nature 593, 553–557 (2021).

    CAS  PubMed  Google Scholar 

  2. Dombrowski, N., Teske, A. P. & Baker, B. J. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat. Commun. 9, 4999 (2018).

    PubMed  PubMed Central  Google Scholar 

  3. Wong, H. L. et al. Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes. ISME J. 12, 2619–2639 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Liu, Y. et al. Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota. ISME J. 12, 1021–1031 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  6. Seitz, K. W., Lazar, C. S., Hinrichs, K. U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. 10, 1696–1705 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Sun, J. et al. Recoding of stop codons expands the metabolic potential of two novel Asgardarchaeota lineages. ISME Commun. 1, 30 (2021).

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  10. Farag, I. F., Zhao, R. & Biddle, J. F. “Sifarchaeota,” a novel Asgard phylum from Costa Rican sediment capable of polysaccharide degradation and anaerobic methylotrophy. Appl. Environ. Microbiol. 87, e02584–20 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 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. 15, 1826–1843 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Cai, M. et al. Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation. Sci. China Life Sci. 63, 886–897 (2020).

    CAS  PubMed  Google Scholar 

  13. Rinke, C. et al. A standardized archaeal taxonomy for the Genome Taxonomy Database. Nat. Microbiol. 6, 946–959 (2021).

    CAS  PubMed  Google Scholar 

  14. Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Lopez-Garcia, P. & Moreira, D. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nat. Microbiol. 5, 655–667 (2020).

    CAS  PubMed  Google Scholar 

  16. Da Cunha, V., Gaia, M., Nasir, A. & Forterre, P. Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genet. 14, e1007215 (2018).

    PubMed  PubMed Central  Google Scholar 

  17. Da Cunha, V., Gaia, M., Gadelle, D., Nasir, A. & Forterre, P. Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet. 13, e1006810 (2017).

    PubMed  PubMed Central  Google Scholar 

  18. Baquero, D. P. et al. Structure and assembly of archaeal viruses. Adv. Virus Res. 108, 127–164 (2020).

    CAS  PubMed  Google Scholar 

  19. Prangishvili, D. et al. The enigmatic archaeal virosphere. Nat. Rev. Microbiol. 15, 724–739 (2017).

    CAS  PubMed  Google Scholar 

  20. Dellas, N., Snyder, J. C., Bolduc, B. & Young, M. J. Archaeal viruses: diversity, replication, and structure. Annu. Rev. Virol. 1, 399–426 (2014).

    PubMed  Google Scholar 

  21. Makarova, K. S. et al. Unprecedented diversity of unique CRISPR-Cas-related systems and Cas1 homologs in Asgard archaea. CRISPR J. 3, 156–163 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Coclet, C. & Roux, S. Global overview and major challenges of host prediction methods for uncultivated phages. Curr. Opin. Virol. 49, 117–126 (2021).

    CAS  PubMed  Google Scholar 

  23. Nunoura, T. et al. Variance and potential niche separation of microbial communities in subseafloor sediments off Shimokita Peninsula, Japan. Environ. Microbiol. 18, 1889–1906 (2016).

    CAS  PubMed  Google Scholar 

  24. Glass, J. B. et al. Microbial metabolism and adaptations in Atribacteria-dominated methane hydrate sediments. Environ. Microbiol. 23, 4646–4660 (2021).

    CAS  PubMed  Google Scholar 

  25. Dion, M. B., Oechslin, F. & Moineau, S. Phage diversity, genomics and phylogeny. Nat. Rev. Microbiol. 18, 125–138 (2020).

    CAS  PubMed  Google Scholar 

  26. Iranzo, J., Krupovic, M. & Koonin, E. V. The double-stranded DNA virosphere as a modular hierarchical network of gene sharing. mBio 7, e00978–16 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Koonin, E. V. et al. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84, e00061–19 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Baek, M. et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373, 871–876 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Wang, Z. et al. Structure of the marine siphovirus TW1: evolution of capsid-stabilizing proteins and tail spikes. Structure 26, 238–248 (2018).

    CAS  PubMed  Google Scholar 

  30. Hendrix, R. W. Tail length determination in double-stranded DNA bacteriophages. Curr. Top. Microbiol. Immunol. 136, 21–29 (1988).

    CAS  PubMed  Google Scholar 

  31. Mahony, J. et al. Functional and structural dissection of the tape measure protein of lactococcal phage TP901-1. Sci. Rep. 6, 36667 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Pope, W. H. et al. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. eLife 4, e06416 (2015).

    PubMed  PubMed Central  Google Scholar 

  33. Krupovic, M., Forterre, P. & Bamford, D. H. Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J. Mol. Biol. 397, 144–160 (2010).

    CAS  PubMed  Google Scholar 

  34. Krupovic, M., Cvirkaite-Krupovic, V., Iranzo, J., Prangishvili, D. & Koonin, E. V. Viruses of archaea: structural, functional, environmental and evolutionary genomics. Virus Res. 244, 181–193 (2018).

    CAS  PubMed  Google Scholar 

  35. Liu, Y. et al. Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes. PLoS Biol. 19, e3001442 (2021).

    PubMed  PubMed Central  Google Scholar 

  36. Gardner, A. F., Bell, S. D., White, M. F., Prangishvili, D. & Krupovic, M. Protein-protein interactions leading to recruitment of the host DNA sliding clamp by the hyperthermophilic Sulfolobus islandicus rod-shaped virus 2. J. Virol. 88, 7105–7108 (2014).

    PubMed  PubMed Central  Google Scholar 

  37. Gussow, A. B. et al. Machine-learning approach expands the repertoire of anti-CRISPR protein families. Nat. Commun. 11, 3784 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Li, Y. & Bondy-Denomy, J. Anti-CRISPRs go viral: the infection biology of CRISPR-Cas inhibitors. Cell Host Microbe 29, 704–714 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Krupovic, M. & Bamford, D. H. Virus evolution: how far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol. 6, 941–948 (2008).

    CAS  PubMed  Google Scholar 

  40. Hong, C. et al. A structural model of the genome packaging process in a membrane-containing double stranded DNA virus. PLoS Biol. 12, e1002024 (2014).

    PubMed  PubMed Central  Google Scholar 

  41. Frickey, T. & Lupas, A. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20, 3702–3704 (2004).

    CAS  PubMed  Google Scholar 

  42. Yutin, N., Bäckström, D., Ettema, T. J. G., Krupovic, M. & Koonin, E. V. Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol. J. 15, 67 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. Abrescia, N. G. et al. Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol. Cell 31, 749–761 (2008).

    CAS  PubMed  Google Scholar 

  44. Oksanen, H. M., ICTV Report Consortium. ICTV Virus Taxonomy Profile: Corticoviridae. J. Gen. Virol. 98, 888–889 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Krupovic, M. & Bamford, D. H. Putative prophages related to lytic tailless marine dsDNA phage PM2 are widespread in the genomes of aquatic bacteria. BMC Genomics 8, 236 (2007).

    PubMed  PubMed Central  Google Scholar 

  46. Kazlauskas, D., Varsani, A., Koonin, E. V. & Krupovic, M. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10, 3425 (2019).

    PubMed  PubMed Central  Google Scholar 

  47. Takahashi, T. S. et al. Expanding the type IIB DNA topoisomerase family: identification of new topoisomerase and topoisomerase-like proteins in mobile genetic elements. NAR Genom. Bioinform. 2, lqz021 (2020).

    PubMed  Google Scholar 

  48. Krupovic, M., Quemin, E. R., Bamford, D. H., Forterre, P. & Prangishvili, D. Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 88, 2354–2358 (2014).

    PubMed  PubMed Central  Google Scholar 

  49. Bath, C., Cukalac, T., Porter, K. & Dyall-Smith, M. L. His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 350, 228–239 (2006).

    CAS  PubMed  Google Scholar 

  50. Wang, F. et al. Spindle-shaped archaeal viruses evolved from rod-shaped ancestors to package a larger genome. Cell 185, 1297–1307.e11 (2022).

    CAS  PubMed  Google Scholar 

  51. Hong, C. et al. Lemon-shaped halo archaeal virus His1 with uniform tail but variable capsid structure. Proc. Natl Acad. Sci. USA 112, 2449–2454 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Quemin, E. R. et al. Sulfolobus spindle-shaped virus 1 contains glycosylated capsid proteins, a cellular chromatin protein, and host-derived lipids. J. Virol. 89, 11681–11691 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Roux, S. et al. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. Nat. Microbiol. 4, 1895–1906 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Straus, S. K. & Bo, H. E. Filamentous bacteriophage proteins and assembly. Subcell. Biochem. 88, 261–279 (2018).

    CAS  PubMed  Google Scholar 

  55. Kim, J. G. et al. Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea. Proc. Natl Acad. Sci. USA 116, 15645–15650 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Quemin, E. R. et al. Eukaryotic-like virus budding in Archaea. mBio 7, e01439–16 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Rahlff, J. et al. Lytic archaeal viruses infect abundant primary producers in Earth’s crust. Nat. Commun. 12, 4642 (2020).

    Google Scholar 

  58. Bamford, D. H. et al. ICTV Virus Taxonomy Profile: Pleolipoviridae. J. Gen. Virol. 98, 2916–2917 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Wu, F. et al. Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes. Nat. Microbiol. 7, 200–212 (2022).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Summer, E. J., Gill, J. J., Upton, C., Gonzalez, C. F. & Young, R. Role of phages in the pathogenesis of Burkholderia, or ‘Where are the toxin genes in Burkholderia phages?’. Curr. Opin. Microbiol. 10, 410–417 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Krupovic, M., Dolja, V. V. & Koonin, E. V. The LUCA and its complex virome. Nat. Rev. Microbiol. 18, 661–670 (2020).

    CAS  PubMed  Google Scholar 

  62. Cahill, J. & Young, R. Phage lysis: multiple genes for multiple barriers. Adv. Virus Res. 103, 33–70 (2019).

    CAS  PubMed  Google Scholar 

  63. Snyder, J. C. & Young, M. J. Lytic viruses infecting organisms from the three domains of life. Biochem. Soc. Trans. 41, 309–313 (2013).

    CAS  PubMed  Google Scholar 

  64. Krupovic, M., Daugelavicius, R. & Bamford, D. H. A novel lysis system in PM2, a lipid-containing marine double-stranded DNA bacteriophage. Mol. Microbiol. 64, 1635–1648 (2007).

    CAS  PubMed  Google Scholar 

  65. Danovaro, R. et al. Virus-mediated archaeal hecatomb in the deep seafloor. Sci. Adv. 2, e1600492 (2016).

    PubMed  PubMed Central  Google Scholar 

  66. Tamarit, D. et al. A closed Candidatus Odinarchaeum chromosome exposes Asgard archaeal viruses. Nat. Microbiol. https://doi.org/10.1038/s41564-022-01122-y (2022).

  67. Rambo, I. M., de Anda, V., Langwig, M. V. & Baker, B. J. Genomes of six viruses that infect Asgard archaea from deep-sea sediments. Nat. Microbiol. https://doi.org/10.1038/s41564-022-01150-8 (2022).

  68. Kaneko, M. et al. Insights into the methanogenic population and potential in subsurface marine sediments based on coenzyme F430 as a function-specific compound analysis. JACS Au 1, 1743–1751 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Hirai, M. et al. Library construction from subnanogram DNA for pelagic sea water and deep-sea sediments. Microbes Environ. 32, 336–343 (2017).

    PubMed  PubMed Central  Google Scholar 

  70. Hiraoka, S. et al. Microbial community and geochemical analyses of trans-trench sediments for understanding the roles of hadal environments. ISME J. 14, 740–756 (2020).

    CAS  PubMed  Google Scholar 

  71. Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Chaumeil, P. A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).

    PubMed Central  Google Scholar 

  75. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    PubMed  PubMed Central  Google Scholar 

  76. Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    CAS  PubMed  Google Scholar 

  77. Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Antipov, D., Raiko, M., Lapidus, A. & Pevzner, P. A. Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 36, 4126–4129 (2020).

    CAS  PubMed  Google Scholar 

  79. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS  PubMed  Google Scholar 

  80. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    CAS  PubMed  Google Scholar 

  81. Steinegger, M. et al. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics 20, 473 (2019).

    PubMed  PubMed Central  Google Scholar 

  82. Roux, S. et al. Minimum Information about an Uncultivated Virus Genome (MIUViG). Nat. Biotechnol. 37, 29–37 (2019).

    CAS  PubMed  Google Scholar 

  83. Sullivan, M. J., Petty, N. K. & Beatson, S. A. Easyfig: a genome comparison visualizer. Bioinformatics 27, 1009–1010 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Bin Jang, H. et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37, 632–639 (2019).

    Google Scholar 

  85. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Bland, C. et al. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8, 209 (2007).

    PubMed  PubMed Central  Google Scholar 

  87. Biswas, A., Staals, R. H., Morales, S. E., Fineran, P. C. & Brown, C. M. CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics 17, 356 (2016).

    PubMed  PubMed Central  Google Scholar 

  88. Tareen, A. & Kinney, J. B. Logomaker: beautiful sequence logos in Python. Bioinformatics 36, 2272–2274 (2020).

    CAS  PubMed  Google Scholar 

  89. Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20, 1160–1166 (2019).

    CAS  PubMed  Google Scholar 

  90. Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Nayfach, S. et al. Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome. Nat. Microbiol. 6, 960–970 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Camarillo-Guerrero, L. F., Almeida, A., Rangel-Pineros, G., Finn, R. D. & Lawley, T. D. Massive expansion of human gut bacteriophage diversity. Cell 184, 1098–1109 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Gregory, A. C. et al. The gut virome database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 28, 724–740 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Shkoporov, A. N. et al. The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 26, 527–541 (2019).

    CAS  PubMed  Google Scholar 

  95. Zhang, R. et al. SpacePHARER: sensitive identification of phages from CRISPR spacers in prokaryotic hosts. Bioinformatics 37, 3364–3366 (2021).

    CAS  PubMed Central  Google Scholar 

  96. Dion, M. B. et al. Streamlining CRISPR spacer-based bacterial host predictions to decipher the viral dark matter. Nucleic Acids Res. 49, 3127–3138 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Galiez, C., Siebert, M., Enault, F., Vincent, J. & Soding, J. WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs. Bioinformatics 33, 3113–3114 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Zielezinski, A., Deorowicz, S. & Gudys, A. PHIST: fast and accurate prediction of prokaryotic hosts from metagenomic viral sequences. Bioinformatics 38, 1447–1449 (2021).

    PubMed Central  Google Scholar 

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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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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.

Corresponding authors

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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  • DOI: https://doi.org/10.1038/s41564-022-01144-6

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