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Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes

['Ying Liu', 'Institut Pasteur', 'Université De Paris', 'Archaeal Virology Unit', 'Paris', 'Tatiana A. Demina', 'Molecular', 'Integrative Biosciences Research Programme', 'Faculty Of Biological', 'Environmental Sciences']

Date: 2021-11

The archaeal tailed viruses (arTV), evolutionarily related to tailed double-stranded DNA (dsDNA) bacteriophages of the class Caudoviricetes, represent the most common isolates infecting halophilic archaea. Only a handful of these viruses have been genomically characterized, limiting our appreciation of their ecological impacts and evolution. Here, we present 37 new genomes of haloarchaeal tailed virus isolates, more than doubling the current number of sequenced arTVs. Analysis of all 63 available complete genomes of arTVs, which we propose to classify into 14 new families and 3 orders, suggests ancient divergence of archaeal and bacterial tailed viruses and points to an extensive sharing of genes involved in DNA metabolism and counter defense mechanisms, illuminating common strategies of virus–host interactions with tailed bacteriophages. Coupling of the comparative genomics with the host range analysis on a broad panel of haloarchaeal species uncovered 4 distinct groups of viral tail fiber adhesins controlling the host range expansion. The survey of metagenomes using viral hallmark genes suggests that the global architecture of the arTV community is shaped through recurrent transfers between different biomes, including hypersaline, marine, and anoxic environments.

Funding: This work was supported by l’Agence Nationale de la Recherche grant ANR-20-CE20-0009-02 (to M.K.) and the European Union’s Horizon 2020 research and innovation program under grant agreement 685778, project VIRUS X (to D.P.). Y.L. is a recipient of the Pasteur-Roux-Cantarini Fellowship from Institut Pasteur. The Ella and Georg Ehrnrooth Foundation and the Finnish Cultural Foundation are sincerely acknowledged (grants to T.D.). The work conducted by the U.S. Department of Energy Joint Genome Institute (S.R.) is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231. The development and application of GRAViTy analysis was supported by a grant to PS from the Wellcome Trust (WT108418AIA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Virus discovery in the “age of metagenomics” is increasingly performed by culture-independent methods, whereby viral genomes are sequenced directly from the environment. This is a powerful approach that has already yielded thousands of viral genomes, providing unprecedented insights into virus diversity, environmental distribution, and evolution [ 39 – 46 ]. The limitation of viral metagenomics, however, is that the exact host species for the sequenced viruses typically remain unknown, and many molecular aspects of virus–host interactions cannot be accurately predicted. Here, to further explore the biology and diversity of arTVs, we sequenced the genomes of 37 viruses that infect different species of halophilic archaea and were isolated from hypersaline environments using classical approaches [ 16 , 17 ]. Collectively, our results provide the first global overview of arTV diversity and evolution and establish a taxonomic framework for their classification.

Genomic and structural analyses have shown that archaeal and bacterial tailed viruses have similar genomic organizations, with genes clustered into functional modules, and share homologous virion morphogenesis modules, including the major capsid protein (MCP) with the characteristic HK97 fold and the genome packaging terminase complex, suggesting common principles of virion assembly [ 11 , 13 , 22 , 30 , 37 , 38 ]. Nevertheless, at the sequence level, arTVs are strikingly diverse showing little similarity to each other and virtually no recognizable similarity to their bacterial relatives, indicative of scarce sampling of the archaeal virosphere [ 38 ]. Indeed, for several thousands of complete genome sequences of tailed bacteriophages [ 2 ], only 25 arTV isolates have been sequenced thus far. The low number of isolates severely limits our appreciation of the ecological impacts of arTVs and obscures the evolutionary history of this important and ancient group of viruses.

The arTVs have been thus far isolated on halophilic (class Halobacteria) and methanogenic (family Methanobacteriaceae ) archaea, both belonging to the phylum Euryarchaeota [ 16 – 25 ]. Related proviruses have also been sighted in other lineages of the Euryarchaeota as well as in ammonia-oxidizing Thaumarchaeota and Aigarchaeota [ 26 – 30 ], whereas recent metagenomics studies revealed novel groups of arTVs putatively infecting marine group II Euryarchaeota, Thaumarchaeota, and Thermoplasmata [ 31 – 35 ]. Ecologically, it has been shown that virus-mediated lysis of archaea in the deep ocean is more rapid than that of bacteria, suggesting an important ecological role of archaeal viruses in marine ecosystems [ 36 ]. Evolutionarily, the broad distribution of tailed (pro)viruses in both bacteria and archaea suggests that viruses of this type were part of the virome associated with the last universal cellular ancestor, LUCA [ 3 ].

Bacteriophages with helical tails and icosahedral capsids (tailed bacteriophages), classified into the class Caudoviricetes [ 1 ], represent the most widespread, abundant, and diverse group of viruses on our planet [ 2 ] and are likely to infect hosts from most, if not all, known bacterial lineages [ 3 ]. Extensive experimental studies conducted over several decades, coupled with comparative analysis of several thousands of complete tailed phage genomes currently available in the public sequence databases, have resulted in detailed understanding of the mechanisms that govern the biology, ecology, and evolution of this group of viruses [ 2 , 4 – 6 ]. Due to their ubiquity, tailed bacteriophages have a profound impact on the functioning of the biosphere through regulating the structure, composition, and dynamics of bacterial populations in diverse environments, from marine ecosystems to the human gut, and modulate major biogeochemical cycles [ 7 – 9 ]. Archaeal tailed viruses (arTVs) are morphologically indistinguishable from tailed bacteriophages [ 1 , 4 , 10 – 12 ]. Similar to their bacterial relatives, the helical tails of arTVs can be short (podovirus morphology), long noncontractile (siphovirus morphology), or contractile (myovirus morphology) [ 13 – 15 ].

Results and discussion

Overview of new haloarchaeal tailed viruses We sequenced a collection of 37 arTVs (5 siphoviruses and 32 myoviruses) infecting haloarchaeal species belonging to the genera Halorubrum and Haloarcula [16,17], more than doubling the number of complete genomes of arTVs (S1 Table). The sequenced viruses originate from geographically remote locations, including Thailand, Israel, Italy, and Slovenia, and in combination with the previously described isolates, provide a substantially improved genomic insight into the global distribution of arTVs. The viruses possess double-stranded DNA (dsDNA) genomes ranging from 35.3 to 104.7 kb in length. Genomes of several isolates were nearly identical (<17 nucleotide polymorphisms; S1 Table) and analysis of these genomes, in combination with host range experiments, was particularly illuminating toward the host range evolution among halophilic arTVs (see below).

Gene content of archaeal tailed viruses All virus genes were functionally annotated using sensitive profile–profile hidden Markov model (HMM) comparisons using HHpred [51] (S3 Table). The virus-encoded proteins were further classified into functional categories based on their affiliation to the archaeal clusters of orthologous genes (arCOG) [52] (S3 Table). Apart from the “Virus-related” proteins, the most frequent functional category assigned to archaeal virus proteins was the “Information storage and processing,” with the “Genome replication, recombination, and repair” subcategory being most strongly enriched (Fig 4A). Proteins of the “Defense mechanisms” subcategory from the “Cellular processes and signaling” category, primarily including diverse nucleases and DNA MTases, were also abundant. Finally, a substantial fraction of proteins was assigned to the “Metabolism” category, with proteins involved in nucleotide transport and metabolism being most common (Fig 4A). Below we highlight some of the observations with the more detailed description provided in S1 Text. PPT PowerPoint slide

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TIFF original image Download: Fig 4. Classification of genes encoded by arTVs. (A) Classification of arTV genes into arCOG functional categories. The homologous gene shared by viruses in the same species is counted as one. The letters represent the following: J, translation, ribosomal structure and biogenesis; K, transcription; L, replication, recombination and repair; D, cell cycle control, cell division, chromosome partitioning; V, defense mechanisms; T, signal transduction mechanisms; M, cell wall/membrane/envelope biogenesis; N, cell motility; O, posttranslational modification, protein turnover, chaperons; G, carbohydrate transport and metabolism; E, amino acid transport and metabolism; F, nucleotide transport and metabolism; H, coenzyme transport and metabolism; I, lipid transport and metabolism; P, inorganic ion transport and metabolism; Q, secondary metabolites biosynthesis, transport and catabolism; R, general function prediction only; S, function unknown; X, virus related. (B) Schematic showing nucleotide-related (partial) metabolic pathways, with a particular enzyme indicated for each reaction. Enzymes that are found encoded by arTVs are in red, otherwise in gray. The number of virus families that harbor the enzyme was labeled beside the name the enzyme, with the number of virus species shown in the brackets. NrdA: RnR, MazG: NTP pyrophosphatase, 5′-NCT: 5′-deoxyribonucleotidase, CarA: CP synthase small subunit, Dcd: dCTP deaminase, Tmk: thymidylate kinase, THY1: thymidylate synthase thyX, NDT: nucleoside deoxyribosyltransferase, FolE: GTP cyclohydrolase I, QueC: queuosine biosynthesis protein, QueD: 6-pyruvoyl tetrahydropterin synthase, QueE: 7-carboxy-7-deazaguanine synthase, DpdA: paralog of queuine tRNA-ribosyltransferase, QueFC: NADPH-dependent 7-cyano-7deazaguanine reductase. See S3 and S5 Tables for individual genes classification. arCOG, archaeal clusters of orthologous gene; arTV, archaeal tailed virus; CP, carbamoylphosphate; RnR, ribonucleotide diphosphate reductase. https://doi.org/10.1371/journal.pbio.3001442.g004

Defense and counterdefense factors Similar to tailed bacteriophages, arTVs are under strong pressure to overcome the host defenses, among which CRISPR/Cas, restriction–modification (RM,) and toxin–antitoxin (TA) are the ubiquitous defense systems in both archaea and bacteria. No clear homologs of viral anti-CRISPR proteins were detected in the arTVs genomes, although several members of the Hafunaviridae and Druskaviridae encode a Cas-4–like nuclease that could potentially function in counterdefense against CRISPR/Cas systems (see S1 Text). By contrast, haloarchaeal tailed viruses (n = 48) from 10 families encode diverse MTases with specificities for N6-adenine, N4-cytosine, and C5-cytosine (S4 Table, S3 Fig). The presence of the MTase genes can be linked to the presence of sequence motifs in the genomes of the corresponding viruses. For instance, GATC motif methylated by the phiCh1-like Dam MTase (Gm6ATC) [53] is present at high frequency (6.47 to 11.04/kb) in the genomes of viruses that encode this MTase. By contrast, viruses that do not encode the Dam MTase also lack the corresponding motif in their genomes. Thus, arTVs have likely evolved to escape the host RM systems by either self-methylation via different virus-encoded MTases or purging the recognition motifs from their genomes. In addition to the stand-alone MTases, some arTVs encode accompanying restriction endonucleases (REases), forming apparently functional RM systems, which could be deployed by the viruses for degradation of the host chromosomes or genomes of competing mobile genetic elements (see S1 Text). A similar function could be envisioned for the RNA- or DNA-specific micrococcal nucleases encoded by HRTV-17, phiH1, HCTV-2, and HHTV-2 (S3 Table). The 7-deazaguanine modifications, produced by the virus-encoded preQ0/G+ pathway, were recently detected in the genomes of diverse viruses, including HVTV-1, and shown to confer viral DNA with resistance to various type II REases [54]. The preQ0/G+ pathway is encoded by all viruses of the Druskaviridae (Fig 4B, S3 Table), suggesting that these viruses depend on a similar genome modification for evasion of the host RM systems. Notably, HCTV-1 and HCTV-16 in addition encode a transporter of the queuosine precursor YhhQ. Interestingly, HRTV-29 (family Haloferuviridae) does not carry genes for the preQ0/G+ pathway, but encodes a DpdA homolog, a key enzyme mediating replacement of the unmodified guanine base in the DNA (Fig 4B, S3 Table). DNA modification with solely virus-encoded DpdA was demonstrated for the Salmonella phage 7–11 [54], suggesting that HRTV-29 also hijacks the host preQ0 pathway for DNA modification through its DpdA protein. The TA systems are widely distributed in prokaryotes and have been shown to function in bacterial antiviral defense by initiating the programmed cell death, thereby preventing the virus spread [55]. Similar to certain marine bacteriophages [56], viruses of the families Druskaviridae, Vertoviridae, and Madisaviridae encode homologs of the nucleoside pyrophosphohydrolase MazG (S5 Table), which prevents the programmed cell death by degrading the intracellular ppGpp [57]. In addition, several arTVs encode homologs of the VapB antitoxins (arCOG08550), but not the associated toxins, suggesting a function in blocking the VapBC TA systems. Thus, arTVs appear to encode different factors for counteracting TA systems.

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