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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Articles
https://doi.org/10.1038/s41564-022-01144-6
1Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, France. 2Center of Life Science, Skolkovo Institute of Science and
Technology, Moscow, Russia. 3Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia,
Queensland, Australia. 4National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA.
5Research Center for Bioscience and Nanoscience, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan. 6Present address:
Institut Pasteur, Université Paris Cité, CNRS UMR6047, Evolutionary Biology of the Microbial Cell Unit, Paris, France. ✉e-mail: takuron@jamstec.go.jp;
c.rinke@uq.edu.au; mart.krupovic@pasteur.fr
Asgard archaea are an expansive group of metabolically ver-
satile archaea that thrive primarily in anoxic sediments
around the globe1–9. Based on phylogenomic analyses,
Asgard archaea were originally classified into multiple phylum-level
lineages, including Lokiarchaeota, Thorarchaeota, Odinarchaeota,
Heimdallarchaeota, Helarchaeota, Sifarchaeota, Wukongarchaeota
and several others, most of which were named after Norse gods1,5,7,9–12.
Recently, taxonomic rank normalization using relative evolu-
tionary divergence has suggested that Asgard archaea represent a
phylum, tentatively named Asgardarchaeota, including the classes
Lokiarchaeia, Thorarchaeia, Odinarchaeia, Heimdallarchaeia,
Sifarchaeia, Hermodarchaeia, Sifarchaeia, Baldrarchaeia,
Wukongarchaeia and Jordarchaeia, with the other lineages clas-
sified as lower-rank taxa within the classes8,13. The vast majority
of Asgard archaea have been discovered through metagenomics,
whereas only one species has been isolated and successfully grown
in the laboratory14. Asgard archaea gained prominence due to
their inferred key role in the origin of eukaryotes15. Indeed,
Heimdallarchaeia form a sister group to eukaryotes in most phy-
logenetic analyses1,5 although alternative phylogenies have also
been presented16,17. Compared with other archaea, Asgard archaea
encode a substantially expanded set of eukaryotic signature pro-
teins, including many proteins implicated in membrane traffick-
ing, vesicle formation and transport, cytoskeleton formation, the
ubiquitin network and other processes characteristic of eukary-
otes1,5. A tantalizing question is whether eukaryotes also inherited
viruses and other types of mobile genetic elements (MGEs) from
the Asgard archaea.
Viruses infecting archaea are remarkably diverse, in terms of both
their genome sequences and virion structures18–20. Some archaeal
viruses, in particular those with icosahedral virions, are evolution-
arily related to bacterial and eukaryotic viruses but the majority of
archaeal virus groups are specific to archaea, with no identifiable
relatives in the two other domains. Archaea-specific viruses often
have odd-shaped virions that resemble lemons, champagne bottles
or droplets19. Most archaeal viruses have, thus far, been isolated
from hyperthermophilic or halophilic hosts, with only a handful of
virus species described for methanogenic and ammonia-oxidizing
mesophilic archaea18. No viruses infecting Asgard archaea have
been isolated, primarily due to the inherent difficulty in propaga-
tion of Asgard archaeal hosts. Nevertheless, analysis of CRISPR–Cas
loci in the genomes of Asgard archaea revealed a remarkable diver-
sity of defence systems in these organisms21, implying a rich Asgard
archaeal virome. CRISPR arrays are archives of past encounters with
viruses and other MGEs, which can be harnessed to uncover the
associations between viruses and their hosts. Indeed, matching the
CRISPR spacers from a known organism to viruses with unknown
hosts is widely used in host assignment for viruses discovered by
metagenomics and, arguably, is the most straightforward and effi-
cient approach to identification of the hosts of viruses infecting
prokaryotes22.
Here we harness CRISPR spacer sequences from the sequenced
Asgard archaeal genomes to search for viruses infecting these
organisms, and describe three distinct family-level groups of
Asgard-associated viruses, all of which display typical features of
viruses infecting bacteria or archaea.
Three families of Asgard archaeal viruses
identified in metagenome-assembled genomes
Sofia Medvedeva1,2,6, Jiarui Sun3, Natalya Yutin 4, Eugene V. Koonin 4, Takuro Nunoura 5 ✉ ,
Christian Rinke 3 ✉ and Mart Krupovic 1 ✉
Asgardarchaeota harbour many eukaryotic signature proteins and are widely considered to represent the closest archaeal rela-
tives 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 icosahe-
dral capsids of the realm Varidnaviria; and the third group, wyrdviruses, is related to spindle-shaped viruses previously identi-
fied 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 prokary-
otes, 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.
NATURE MICROBIOLOGY | VOL 7 | JULY 2022 | 962–973 | www.nature.com/naturemicrobiology
962
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