Structural insights into a spindle-shaped archaeal virus with a sevenfold symmetrical tail

Abstract

Archaeal viruses with a spindle-shaped virion are abundant and widespread in extremely diverse environments. However, efforts to obtain the high-resolution structure of a spindle-shaped virus have been unsuccessful. Here, we present the structure of SSV19, a spindle-shaped virus infecting the hyperthermophilic archaeon Sulfolobus sp. E11-6. Our near-atomic structure reveals an unusual sevenfold symmetrical virus tail consisting of the tailspike, nozzle, and adaptor proteins. The spindle-shaped capsid shell is formed by seven left-handed helical strands, constructed of the hydrophobic major capsid protein, emanating from the highly glycosylated tail assembly. Sliding between adjacent strands is responsible for the variation of a virion in size. Ultrathin sections of the SSV19-infected cells show that SSV19 virions adsorb to the host cell membrane through the tail after penetrating the S-layer. The tailspike harbors a putative endo-mannanase domain, which shares structural similarity to a Bacteroides thetaiotaomicro endo-mannanase. Molecules of glycerol dibiphytanyl glycerol tetraether lipid were observed in hydrophobic clefts between the tail and the capsid shell. The nozzle protein resembles the stem and clip domains of the portals of herpesviruses and bacteriophages, implying an evolutionary relationship among the archaeal, bacterial, and eukaryotic viruses.

Viruses in astrobiology

“…Archaeoviruses can also incorporate ether lipids from their extremophilic host in their virions, which seem to protect against chemical stress ( Boyd et al, 2013 ). Archaeal lipids are also present in the structure of hyperthermophilic spindle-shaped viruses, but its location remains under debate ( Quemin et al, 2015 ; Han and Yuan, 2022 ).…”

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

“…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 ].…”

“…Three of these genomes (SSV NL101B.C01.09, NL101B.C01.18, and NL101B.C01.22) harbor two VP4 homologs that seem to be the result of the full protein split into its N- and C-terminal domains. For the remaining three (SSV6, SSV19, and ASSV1), it was recently reported that the short VP4 homolog serves as an adaptor protein for the tail, while another protein (belonging to OG0000087) has the same genomic location as VP4 and serves as the tail-spike [ 38 ]. A truncated VP4 and the OG0000087 tail-spike are associated with viruses that show a pleomorphic morphology [ 30 ].…”

“…Since genome organization seems conserved in fuselloviruses and given that transcripts T 4/7/8 and T 1/2 appear to encode for structural proteins, we predict B78 to be also a virion protein as it has two transmembrane helices (similarly to VP1, VP3, VP4, and C166, which also contain transmembrane helices). Intriguingly, homologs of this protein are missing from SSV6, SSV19, and ASSV1, which have a different tail structure [ 38 ]. Interestingly, the absolute core gene B115, which is a putative transcriptional regulator, is encoded in T 4/7/8 and may be involved in the regulation of structural gene expression.…”

“…The structures of VP1, VP2, VP3 ( A ), and VP4 ( C ) were modelled using AlphaFold2 [ 53 ]. ( B ) Cryo-electron micrograph of the SSV19 tail (7XID, [ 38 ]). The atomic models of the B210 adaptor and the VP4-like tail-spike are shown to the right.…”