Spindle-shaped archaeal viruses evolved from rod-shaped ancestors to package a larger genome

Wang, Fengbin; Cvirkaitė-Krupovič, Virginija; Vos, Matthijn; Beltrán, Leticia C.; Kreutzberger, Mark A.; Winter, Jean-Marie; Su, Zhangli; Li, Jun; Schouten, Stefan; Krupovìč, Mart

doi:10.1016/j.cell.2022.02.019

Cited by 32 publications

(44 citation statements)

References 76 publications

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“…In particular, the closest homolog was found in haloarchaeal virus His1 (family Halspiviridae; Extended Data 5) 49 . His1-like MCPs are ~80 aa-long and contain two hydrophobic segments predicted to be membrane spanning domains 48 and in all spindle-shaped viruses playing key roles in virion structure and assembly 50 . BLASTP searches using the WyrdV1 MCP as a query against the JGI and GenBank databases identified eight additional contigs (Fig.…”

Section: Wyrdviruses Are Related To Spindle-shaped Archaeal Virusesmentioning

confidence: 99%

“…The homology between the tubulaviral and wyrdviral ATPases suggests that virion assembly of wyrdviruses is mechanistically similar to the extrusion of filamentous bacteriophages. Indeed, spindle-shaped viruses infecting other archaea are released from the host without causing the cell lysis through a budding-like mechanism 50,55,56 . Notably, some spindle-shaped viruses encode a single MCP (e.g., halspiviruses), whereas others encode two paralogous MCP (e.g., fuselloviruses).…”

Section: Wyrdviruses Are Related To Spindle-shaped Archaeal Virusesmentioning

confidence: 99%

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Three families of Asgard archaeal viruses identified in metagenome-assembled genomes

et al. 2022

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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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Section: Wyrdviruses Are Related To Spindle-shaped Archaeal Virusesmentioning

confidence: 99%

Section: Wyrdviruses Are Related To Spindle-shaped Archaeal Virusesmentioning

confidence: 99%

Three families of Asgard archaeal viruses identified in metagenome-assembled genomes

et al. 2022

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“…4c). In particular, head-tailed viruses of the class Caudoviricetes (realm Duplodnaviria ) encode characteristic HK97-fold major capsid proteins (MCP) as well as the large subunit of the terminase and portal proteins 52,53 ; tailless icosahedral viruses of the realm Varidnaviria are characterized by double jelly-roll MCPs 52,54,55 ; viruses of the realm Adnaviria encode unique α-helical MCPs which form claw-like dimers that wrap around the viral DNA forming a helical, rod-shaped capsid 56–58 ; and all spindle-shaped viruses encode unique, highly hydrophobic α-helical MCPs 59,60 (Supplementary Table 9-10). In total, 16 new candidate viral families were discovered in this study, including five families with representative complete genomes (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Based on the conservation of signature genes encoding viral structural proteins, we concluded that ANME-1 MGEs encompass double-stranded DNA viruses belonging to at least 4 widely different virus assemblages characterized by different evolutionary histories and distinct virion morphologies. In particular, head-tailed viruses of the class Caudoviricetes (realm Duplodnaviria) encode characteristic HK97-fold major capsid proteins (MCP) as well as the large subunit of the terminase and portal proteins 73,74 ; tailless icosahedral viruses of the realm Varidnaviria are characterized by double jelly-roll MCPs 73,75 ; viruses of the realm Adnaviria encode unique α-helical MCPs which form claw-like dimers that wrap around the viral DNA forming a helical, rod-shaped capsid [76][77][78] ; and all spindle-shaped viruses (realm yet unassigned) encode unique, highly hydrophobic α-helical MCPs 79,80 (Supplementary Table 9-10). With the exception of adnaviruses, all other viral types associated with ANME-1 appear to be highly diverse, each comprising several new families.…”

Section: Crispr-based Discovery Of An Expansive Anme-1 Mobilomementioning

confidence: 99%

Evolutionary Diversification of MethanotrophicCa. Methanophagales (ANME-1) and Their Expansive Virome

Laso-Pérez

Crémière

et al. 2022

Preprint

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Candidatus Methanophagales (ANME-1) is a major order-level clade of archaea responsible for methane removal in deep-sea sediments through anaerobic oxidation of methane. Yet the extent of their diversity and factors which drive their dynamics and evolution remain poorly understood. Here, by sampling hydrothermal rocks and sediments, we expand their phylogenetic diversity and characterize a new deep-branching, thermophilic ANME-1 family, Candidatus Methanoxibalbaceae (ANME-1c). They are phylogenetically closest to the short-chain-alkane oxidizers Candidatus Syntrophoarchaeales and Candidatus Alkanophagales, and encode ancestral features including a methyl coenzyme M reductase chaperone McrD and a hydrogenase complex. Global phylogeny and near-complete genomes clarified that the debated hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Our expanded genomic and metagenomic sampling allowed the discovery of viruses constituting 3 new orders and 16 new families that so far are exclusive to ANME-1 hosts. These viruses represent 4 major archaeal virus assemblages, characterized by tailless icosahedral, head-tailed, rod-shaped, and spindle-shaped virions, but display unique structural and replicative signatures. Exemplified by the analyses of thymidylate synthases that unveiled a virus-mediated ancestral process of host gene displacement, this expansive ANME-1 virome carries a large gene repertoire that can influence their hosts across different timescales. Our study thus puts forth an emerging evolutionary continuum between anaerobic methane and short-chain-alkane oxidizers and opens doors for exploring the impacts of viruses on the dynamics and evolution of the anaerobic methane-driven ecosystems.

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“…The 13 formerly defined core genes [ 14 , 29 , 30 ] were kept in our analysis as part of the soft-core, and we incorporated four additional genes (A92, VP3, C102, and A100). Core genes VP1, VP3, VP4, and C166 play a structural role [ 28 , 36 , 37 , 38 ], the integrase D355 serves virus integration into the genome [ 22 ], and proteins B251 an ATPase with similarity to the bacterial DnaA [ 39 ] and A154 have been implicated in replication and packaging of the genome. Indeed, B251 and A154 are also encoded by the satellite virus pSSVx, which replicates during infection of an SSV2 helper [ 40 ].…”

Section: Genomic Analysismentioning

confidence: 99%

Genomics, Transcriptomics, and Proteomics of SSV1 and Related Fusellovirus: A Minireview

Aulitto

Martínez-Álvarez

Fusco

et al. 2022

Viruses

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Saccharolobus spindle-shaped virus 1 (SSV1) was one of the first viruses identified in the archaeal kingdom. Originally isolated from a Japanese species of Saccharolobus back in 1984, it has been extensively used as a model system for genomic, transcriptomic, and proteomic studies, as well as to unveil the molecular mechanisms governing the host–virus interaction. The purpose of this mini review is to supply a compendium of four decades of research on the SSV1 virus.

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Spindle-shaped archaeal viruses evolved from rod-shaped ancestors to package a larger genome

Cited by 32 publications

References 76 publications

Three families of Asgard archaeal viruses identified in metagenome-assembled genomes

Three families of Asgard archaeal viruses identified in metagenome-assembled genomes

Evolutionary Diversification of MethanotrophicCa. Methanophagales (ANME-1) and Their Expansive Virome

Genomics, Transcriptomics, and Proteomics of SSV1 and Related Fusellovirus: A Minireview

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