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Genomes of six viruses that infect Asgard archaea from deep-sea sediments

Nature Microbiology volume 7, pages 953–961 (2022)Cite this article

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Abstract

Asgard archaea are globally distributed prokaryotic microorganisms related to eukaryotes; however, viruses that infect these organisms have not been described. Here, using metagenome sequences recovered from deep-sea hydrothermal sediments, we characterize six relatively large (up to 117 kb) double-stranded DNA (dsDNA) viral genomes that infected two Asgard archaeal phyla, Lokiarchaeota and Helarchaeota. These viruses encode Caudovirales-like structural proteins, as well as proteins distinct from those described in known archaeal viruses. Their genomes contain around 1–5% of genes associated with eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs) and appear to be capable of semi-autonomous genome replication, repair, epigenetic modifications and transcriptional regulation. Moreover, Helarchaeota viruses may hijack host ubiquitin systems similar to eukaryotic viruses. Genomic analysis of these Asgard viruses reveals that they contain features of both prokaryotic and eukaryotic viruses, and provides insights into their potential infection and host interaction mechanisms.

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Fig. 1: Protein clustering network of virus genomes recovered from Guaymas Basin sediments compared to previously described viruses.
Fig. 2: Virus–host linkages to Asgard archaea.
Fig. 3: Taxonomic placement of Asgard viruses based on phylogeny and protein composition.
Fig. 4: Model of Asgard viral infection mechanisms and protein similarity with other viruses.

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Data availability

The genomic sequences associated with the study have been deposited in NCBI under BioProject PRJNA692327.

Code availability

All custom scripts, alignments and phylogenetic tree files have been made available at https://github.com/bakermicrolab/asgardviruses.

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Acknowledgements

This work was supported by grants from the Moore-Simons Project on the Origin of the Eukaryotic Cell (Simons Foundation grant 73592LPI; https://doi.org/10.46714/735925LPI; B.J.B.) and the Simons Foundation Early Career Award (687165, B.J.B.). We thank D. Tamarit and T. Ettema for discussions about this research; A. P. Teske (Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA) for providing the sediments from Guaymas Basin.

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Author notes

  1. Marguerite V. Langwig

    Present address: Department of Bacteriology and Department of Integrative Biology, University of Wisconsin-Madison, Madison, WI, USA

Authors and Affiliations

  1. Department of Marine Science, The University of Texas at Austin, Port Aransas, TX, USA

    Ian M. Rambo, Marguerite V. Langwig, Pedro Leão, Valerie De Anda & Brett J. Baker

  2. Department of Integrative Biology, The University of Texas at Austin, Austin, TX, USA

    Brett J. Baker

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Contributions

V.D.A. and B.J.B. conceptualized the project. I.M.R., V.D.A. and M.V.L. curated the data. B.J.B. acquired funding. I.M.R., V.D.A. and P.L. conducted the investigations. I.M.R., V.D.A. and B.J.B. developed the methodology. B.J.B. and V.D.A. administered and supervised the project. B.J.B acquired resources. I.M.R., V.D.A. and P.L. created the visualizations. I.M.R., V.D.A., M.V.L. and B.J.B. wrote the original draft. I.M.R., V.D.A., M.V.L., P.L. and B.J.B. reviewed and edited the manuscript.

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Correspondence to Brett J. Baker.

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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 Asgard virus genome structures.

a, Genomic architecture of the complete Helarchaeota virus Nidhogg Meg22_1012. From outside to center: genes described in the main text, genes with homologs not described in the main text, hypothetical proteins, GC content, genome size ruler. Arrows pointing left indicate (−) sense, while those pointing right indicate (+) sense. b, Structures of the linear Fenrir, Sköll, and Ratatoskr genomes. Sequence length is designated by the measure on the x-axis. Genes with hypothetical products do not have labels and are colored in gray. CRISPR spacer match locations are highlighted with vertical bars, colored to represent 0 or 1 mismatches in the alignment.

Extended Data Fig. 2 Range of Asgard virus sizes vs known archaeal viruses.

Median value (Asgard virus = 89,108 / Archaea virus = 35,450); Minimum value (Asgard virus = 39,909 / Archaea virus = 5,278); maximum value (Asgard virus = 117,419 / Archaea virus = 103,257); Archaea virus outlier = 143,855. Data and code for this figure is available at https://github.com/bakermicrolab/asgardviruses.

Extended Data Fig. 3 Average read depths of Asgard virus contigs versus host MAG contigs.

The y-axis denotes average read depth for a contig within its respective sample, with each Asgard host shown on the x-axis. Each point on the x-axis contains two box-and-whisker plots indicating average read depths for linked viral contigs (left) and host contigs (right). Data points represent mean values. Taxonomic assignment is designated by the color of the points and/or box. Average read depth was calculated for each contig using reads from the same sample used in assembly. Helarchaeota Meg19_1012_Bin_504 (virus: n = 3, min=25.52, max=173.4, mid=32.50; MAG: n = 170, min=9.12, mean=56.58, max=81.45, SD = 5.8, 1st quartile=54.9, 3rd quartile=58.9), Lokiarchaeota Meg22_1012_Bin_233 (virus: n = 1, 77.5; MAG: n = 94, min=6.16, mean=37.3, max=202.9, SD = 24.8, 1st quartile=31.5, 3rd quartile=34.3), Lokiarchaeota Meg22_1214_Bin_191 (virus: n = 1, 17.05; MAG: n = 246, min=8.1, mean=44.8, max=1253, SD = 95.6, 1st quartile=29.7, 3rd quartile=39.7), Lokiarchaeota Meg22_1416_Bin_151 (virus: n = 1, 16.32; MAG: n = 217, min=5.9, mean=17, max=48, SD = 3.7, 1st quartile=15.7, 3rd quartile=18.5).

Extended Data Fig. 4 Comparison of NCVOG proportions in viruses.

Viruses are grouped on the x-axis based on their host, with the NCLDVs included in their own category. The y-axis denotes the percentage of genes present with hits to NCVOGs (see Methods). Each dot in the graph represents a viral genome. Bacterial viruses n = 33442, mean=2, SD = ± 1.2; Archaeal viruses n = 84, mean=2.4’ SD = ± 1.4; Asgard virus n = 6, mean=2.2, SD = ± 1.4; Eukaryotic virus n = 362, mean=36, SD = ± 39; NCLDV n = 149, mean=78, SD = 21.

Extended Data Fig. 5 Functional breakdown of NCVOG proportions.

Viruses are grouped on the y-axis based on their host, with percentages on the x-axis indicating the proportion of NCVOG hits assigned to a particular function. NCVOGs found in Asgard viruses are related to DNA replication, recombination and repair or viral structure proteins. The first group of NCVOGs are commonly found in viruses infecting bacteria, and can also be observed in viruses infecting other archaeal groups, and Eukaryotes. The second group of NCVOGs are not so commonly found in other viruses, which can suggest a similar structure of Asgard viruses and NCLDVs.

Extended Data Fig. 6 Deoxynucleotide monophosphate kinase phylogeny.

A phylogenetic tree of 241 deoxynucleotide/side monophosphate kinase sequences from viruses and bacteria. Circles on branches indicate BOOSTER supports ≥70. Lokiarchaeota virus Fenrir Meg22_1012 and Meg22_1214 sequences are highlighted in gold. The phylogeny was inferred using the LG model with fixed base frequencies and 1000 rapid bootstraps.

Extended Data Fig. 7 Ubiquitin-activating enzyme phylogeny.

A phylogenetic tree of 368 ubiquitin-activating enzyme (E1) protein sequences from archaea, bacteria, eukaryotes, and viruses (taxa are labeled with background colors). Three E1-like protein sequences were identified in Nidhogg viruses, and these are labeled with black circles and bold text. Arched lines show the connections between Nidhogg virus sequences and their Helarchaeota host. This phylogeny was inferred using the LG + R8 model with 1000 ultrafast bootstraps and optimization by nearest neighbor interchange (-bb 1000 -bnni). Circles on tree branches indicate ultrafast bootstrap supports ≥95. The tree is comprised of protein sequences belonging to the NEDD8-activating enzyme E1 catalytic subunit family (n = 11, IPR030468), ubiquitin-activating E1 enzyme (n = 218, IPR035985), viral sequences obtained from NCBI (n = 14), and sequences derived from Lokiarchaeota and Helarchaeota (n = 125).

Supplementary information

Supplementary Information

Extended Data Figs. 1–7, Supplementary Text and description of Supplementary Data 1–13.

Reporting Summary

Peer Review File

Supplementary Data 1

CRISPRDetect results, including spacer and repeat lengths and sequences, and CRISPR sense; Asgard CRISPR spacer BLASTN-short output against Guaymas Basin viruses; average read depth of CRISPR-containing contigs of Asgard MAGs; SpacePHARER hits of Asgard CRISPR spacers to Guaymas Basin UViGs; and CRISPRClassify results for Asgard CRISPR repeats.

Supplementary Data 2

Viral genome overview, Asgard MAG GTDBTk taxonomy and MAG statistics.

Supplementary Data 3

Minimum information about an uncultivated virus genome (MiUViG) metadata for viral genomes described in this study.

Supplementary Data 4

Viral annotations with VIBRANT, DIAMOND and InterProScan; PhANNs classification; and HHPred results for major capsid proteins predicted with PhANNs.

Supplementary Data 5–10

Supplementary_Data_5_Fenrir_Meg22_1012_226.pdf. Visualization of Lokiarchaeota virus Fenrir Meg22_1012_scaffold_226 coverage based on read mapping against the Meg22_1012 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters. Supplementary_Data_6_Fenrir_Meg22_1214.pdf. Visualization of Lokiarchaeota virus Fenrir Meg22_1214_scaffold_313 coverage based on read mapping against the Meg22_1214 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters. Supplementary_Data_7_Skoll_Meg22_1214_2849.pdf. Visualization of Lokiarchaeota virus Sköll Meg22_1214_scaffold_2849 coverage based on read mapping against the Meg22_1214 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters. Supplementary_Data_8_Ratatoskr_Meg22_1012_548.pdf. Visualization of Helarchaeota virus Ratatoskr Meg22_1012_scaffold_548 coverage based on read mapping against the Meg22_1012 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters. Supplementary_Data_9_Nidhogg_Meg22_1012_91.pdf. Visualization of Helarchaeota virus Nidhogg Meg22_1012_scaffold_91 coverage based on read mapping against the Meg22_1012 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters. Supplementary_Data_10_Nidhogg_Meg22_1214_152.pdf. Visualization of Helarchaeota virus Nidhogg Meg22_1214_scaffold_152 coverage based on read mapping against the Meg22_1214 sample performed with BWA-MEM v0.7.17 and Samtools v1.11. Visualized with Geneious version 2022.0 by Biomatters.

Supplementary Data 11

Sequences used in the DNA polymerase B phylogeny.

Supplementary Data 12

Viral protein family (VPF) classification membership ratios for Asgard viruses.

Supplementary Data 13

InterProScan annotations of Asgard MAGs first detailed in this study and IMG/M annotations of all MAGs used in this study.

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Rambo, I.M., Langwig, M.V., Leão, P. et al. Genomes of six viruses that infect Asgard archaea from deep-sea sediments. Nat Microbiol 7, 953–961 (2022). https://doi.org/10.1038/s41564-022-01150-8

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