Diverse viruses of marine archaea discovered using metagenomics

Abstract

During the past decade, metagenomics became a method of choice for the discovery of novel viruses. However, host assignment for uncultured viruses remains challenging, especially for archaeal viruses, which are grossly undersampled compared to viruses of bacteria and eukaryotes. Here, we assessed the utility of CRISPR spacer targeting, tRNA gene matching and homology searches for viral signature proteins, such as major capsid proteins, for the assignment of archaeal hosts and validated these approaches on metaviromes from Yangshan Harbor (YSH). We report 35 new genomes of viruses which could be confidently assigned to hosts representing diverse lineages of marine archaea. We show that the archaeal YSH virome is highly diverse, with some viruses enriching the previously described virus groups, such as magroviruses of Marine Group II Archaea (Poseidoniales), and others representing novel groups of marine archaeal viruses. Metagenomic recruitment of Tara Oceans datasets on the YSH viral genomes demonstrated the presence of YSH Poseidoniales and Nitrososphaeria viruses in the global oceans, but also revealed the endemic YSH‐specific viral lineages. Furthermore, our results highlight the relationship between the soil and marine thaumarchaeal viruses. We propose three new families within the class Caudoviricetes for the classification of the five complete viral genomes predicted to replicate in marine Poseidoniales and Nitrososphaeria, two ecologically important and widespread archaeal groups. This study illustrates the utility of viral metagenomics in exploring the archaeal virome and provides new insights into the diversity, distribution and evolution of marine archaeal viruses.

Diversity, distribution, and functional potentials of magroviruses from marine and brackish waters

“…The wide occurrence and metabolic potential of magroviruses discovered in this study suggest a potential global impact of magroviruses on the ecological functions of MGII archaea. During the manuscript preparation of this study, Zhou et al (2022) published a paper on the metagenome sequences of archaeal viruses, which included magroviruses from a coastal but not brackish zone. Our finding of the brackish magroviruses and that of Zhou et al (2022) indicate a substantial diversity of magroviruses on coastal environments.…”

“…During the manuscript preparation of this study, Zhou et al (2022) published a paper on the metagenome sequences of archaeal viruses, which included magroviruses from a coastal but not brackish zone. Our finding of the brackish magroviruses and that of Zhou et al (2022) indicate a substantial diversity of magroviruses on coastal environments.…”

“…To date, no isolated or enriched cultures of MGII archaea have been obtained. The genome sequences of candidate viruses of MGII archaea were only recently identified from metagenome sequences of global open oceans and coasts (Nishimura et al, 2017;Philosof et al, 2017;Vik et al, 2017;Zhou et al, 2022). Named as magroviruses by Philosof et al (2017), these viruses of MGII archaea belong to Caudovirales and possess double-stranded DNA genomes of about 90 kb on average.…”

“…Like haloviruses, magroviruses may also have icosahedral capsids and helical tails (Philosof et al, 2017;Krupovic et al, 2018). Abundance analysis revealed that they are widespread in surface ocean water and are possibly the third most abundant marine planktonic viruses after cyanophages and pelagiphages implying their potential roles in marine ecology by interacting with their hosts (Philosof et al, 2017;Zhou et al, 2022).…”

ICTV Virus Taxonomy Profile: Aoguangviridae 2023

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Members of the family Aoguangviridae have been discovered through metagenomics and have yet to be cultured [1][2][3][4] (Table 1). However, based on the conservation of the structural module typical of bacterial and archaeal viruses of the class Caudoviricetes [5] and including the HK97-fold major capsid protein, capsid maturation protease, large subunit of the terminase, portal, major tail protein, baseplate, etc., virions are predicted to consist of an icosahedral capsid and a helical tail.

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