Unification of the Globally Distributed Spindle-Shaped Viruses of the Archaea

Abstract

Viruses with spindle-shaped virions are abundant in diverse environments. Over the years, such viruses have been isolated from a wide range of archaeal hosts. Evolutionary relationships between them remained enigmatic, however. Here, using structural proteins as markers, we define familial ties among these "dark horses" of the virosphere and segregate all spindle-shaped viruses into two distinct evolutionary lineages, corresponding to Bicaudaviridae and Fuselloviridae. Our results illuminate the utility of structure-based virus classification and bring additional order to the virosphere.

Sulfolobus Spindle-Shaped Virus 1 Contains Glycosylated Capsid Proteins, a Cellular Chromatin Protein, and Host-Derived Lipids

“…Functional studies proved to be highly challenging due to the lack of similarity between the protein sequences and structures of archaeal viruses and those from other viruses and cellular organisms (6)(7)(8)(9)(10). Among the morphotypes that are exclusively associated with archaea, spindle-shaped viruses are particularly widespread (11) and have been isolated from highly different environments, including deep-sea hydrothermal vents (12)(13)(14), hypersaline environments (15)(16)(17)(18), anoxic freshwaters (19), cold Antarctic lakes (20), terrestrial hot springs (21)(22)(23), and acidic mines (24).…”

“…The first group includes members of the Bicaudaviridae family and several currently unclassified viruses. Viruses of this group have large spindle-shaped virions with one or two long tails and contain circular double-stranded DNA (dsDNA) genomes of ϳ70 kb (11,25). In the case of Acidianus two-tailed virus (ATV), the type species of the Bicaudaviridae family, the two tails develop following …”

Archaeal Extrachromosomal Genetic Elements

“…The considerable variation in morphology and genomic properties found in known archaeal viruses has prompted a search for general principles applicable to the classification of some archaeal viruses in particular and all viruses in general. In this regard, structural proteins have been increasingly recognized as candidates for being a valuable marker in determining the relatedness of viruses, primarily because they are encoded by the true viral "self" genes (63,68,69). For example, structural studies have revealed that the structure of the coat protein of STIV is very similar to that of the coat protein of the bacterial virus PRD1 and those of the eukaryal viruses Paramecium bursaria Chlorella virus 1 (PBCV-1) and adenovirus (70).…”

“…Among spindle-shaped or lemon-shaped viruses, some have been placed in the families Fuselloviridae (i.e., SSV1, SSV2, SSV4 to -7, SSV8 [also known as SSV K1], SSV9 [also known as SSV RH], and Acidianus spindle-shaped virus 1 [ASV1]) and Bicaudaviridae (Acidianus two-tailed virus 1 [ATV]). Unclassified spindle-shaped viruses (e.g., Sulfolobus tengchongenesis spindle-shaped virus 1/2 [STSV1/2] and Pyrococcus abyssi virus 1 [PAV1]) are believed to be associated with either of the above-mentioned two families on the basis of structural protein analysis (63). Of the spherical archaeal viruses, two (i.e., Pyrobaculum spherical virus [PSV] and Thermoproteus tenax spherical virus 1 [TTSV1]) have been assigned to the family Globuloviridae, and the rest are still unclassified (e.g., STIV/ STIV2, spherical halovirus 1 [SH1], Pink Lake Haloarcula hispanica virus 1 [PH1], and Haloarcula hispanica icosahedral virus 2 [HHIV-2]).…”

ICTV Virus Taxonomy Profile: Bicaudaviridae

“…These viruses share many genes with Acidianus two-tailed virus (Fig. 2) and may represent a new genus within the family Bicaudaviridae [10]. Bicaudaviruses encode a conserved DnaA-like AAA+ ATPase, which is shared with members of the archaeal virus families Fuselloviridae and Guttaviridae, suggesting that the three groups of viruses might be evolutionarily related [11].…”