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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. [ABSTRACT FROM AUTHOR]

Viruses are considered to be the most abundant biological entities on earth. They also display striking genetic diversity as emphatically demonstrated by the recent advances of metagenomics and metatranscriptomics. But what are the limits of this diversity, that is, how many virus species in the earth virome? By combining the available estimates of the number of prokaryote species with those of the virome size, we obtain back‐of‐the‐envelope estimates of the total number of distinct virus species, which come out astronomically large, from about 107 to about 109. The route of virus origins apparently involved non‐viral replicators capturing and exapting various cellular proteins to become virus capsid subunits. How many times in the history of life has this happened? In other words, how many realms of viruses, the highest rank taxa that are supposed to be monophyletic, comprise the global virome? We argue that viruses emerged on a number (even if far from astronomical) independent occasions, so the number of realms will considerably increase from the current 6, by splitting some of the current realms, giving the realm status to some of the currently unclassified groups of viruses and discovery of new distinct groups. [ABSTRACT FROM AUTHOR]

Summary: Deep‐sea hydrothermal vents are inhabited by complex communities of microbes and their viruses. Despite the importance of viruses in controlling the diversity, adaptation and evolution of their microbial hosts, to date, only eight bacterial and two archaeal viruses isolated from abyssal ecosystems have been described. Thus, our efforts focused on gaining new insights into viruses associated with deep‐sea autotrophic archaea. Here, we provide the first evidence of an infection of hyperthermophilic methanogenic archaea by a head‐tailed virus, Methanocaldococcus fervens tailed virus 1 (MFTV1). MFTV1 has an isometric head of 50 nm in diameter and a 150 nm‐long non‐contractile tail. Virions are released continuously without causing a sudden drop in host growth. MFTV1 infects Methanocaldococcus species and is the first hyperthermophilic head‐tailed virus described thus far. The viral genome is a double‐stranded linear DNA of 31 kb. Interestingly, our results suggest potential strategies adopted by the plasmid pMEFER01, carried by M. fervens, to spread horizontally in hyperthermophilic methanogens. The data presented here open a new window of understanding on how the abyssal mobilome interacts with hyperthermophilic marine archaea. [ABSTRACT FROM AUTHOR]