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Structure of a filamentous virus uncovers familial ties within the archaeal virosphere.

ABSTRACT: Viruses infecting hyperthermophilic archaea represent one of the most enigmatic parts of the global virome, with viruses from different families showing no genomic relatedness to each other or to viruses of bacteria and eukaryotes. Tristromaviruses, which build enveloped filamentous virions and infect hyperthermophilic neutrophiles of the order Thermoproteales, represent one such enigmatic virus families. They do not share genes with viruses from other families and have been believed to represent an evolutionarily independent virus lineage. A cryo-electron microscopic reconstruction of the tristromavirus Pyrobaculum filamentous virus 2 at 3.4?Å resolution shows that the virion is constructed from two paralogous major capsid proteins (MCP) which transform the linear dsDNA genome of the virus into A-form by tightly wrapping around it. Unexpectedly, the two MCP are homologous to the capsid proteins of other filamentous archaeal viruses, uncovering a deep evolutionary relationship within the archaeal virosphere.

SUBMITTER: Wang F

PROVIDER: S-EPMC7189273 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Structure of a filamentous virus uncovers familial ties within the archaeal virosphere.

Wang Fengbin F Baquero Diana P DP Su Zhangli Z Osinski Tomasz T Prangishvili David D Egelman Edward H EH Krupovic Mart M

Virus evolution 20200101 1

Viruses infecting hyperthermophilic archaea represent one of the most enigmatic parts of the global virome, with viruses from different families showing no genomic relatedness to each other or to viruses of bacteria and eukaryotes. Tristromaviruses, which build enveloped filamentous virions and infect hyperthermophilic neutrophiles of the order Thermoproteales, represent one such enigmatic virus families. They do not share genes with viruses from other families and have been believed to represen ...[more]

PMID: 32368353

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Project description:Four novel filamentous viruses with double-stranded DNA genomes, namely, Acidianus filamentous virus 3 (AFV3), AFV6, AFV7, and AFV8, have been characterized from the hyperthermophilic archaeal genus Acidianus, and they are assigned to the Betalipothrixvirus genus of the family Lipothrixviridae. The structures of the approximately 2-mum-long virions are similar, and one of them, AFV3, was studied in detail. It consists of a cylindrical envelope containing globular subunits arranged in a helical formation that is unique for any known double-stranded DNA virus. The envelope is 3.1 nm thick and encases an inner core with two parallel rows of protein subunits arranged like a zipper. Each end of the virion is tapered and carries three short filaments. Two major structural proteins were identified as being common to all betalipothrixviruses. The viral genomes were sequenced and analyzed, and they reveal a high level of conservation in both gene content and gene order over large regions, with this similarity extending partly to the earlier described betalipothrixvirus Sulfolobus islandicus filamentous virus. A few predicted gene products of each virus, in addition to the structural proteins, could be assigned specific functions, including a putative helicase involved in Holliday junction branch migration, a nuclease, a protein phosphatase, transcriptional regulators, and glycosyltransferases. The AFV7 genome appears to have undergone intergenomic recombination with a large section of an AFV2-like viral genome, apparently resulting in phenotypic changes, as revealed by the presence of AFV2-like termini in the AFV7 virions. Shared features of the genomes include (i) large inverted terminal repeats exhibiting conserved, regularly spaced direct repeats; (ii) a highly conserved operon encoding the two major structural proteins; (iii) multiple overlapping open reading frames, which may be indicative of gene recoding; (iv) putative 12-bp genetic elements; and (v) partial gene sequences corresponding closely to spacer sequences of chromosomal repeat clusters.

Project description:Archaea and particularly hyperthermophilic crenarchaea are hosts to many unusual viruses with diverse virion shapes and distinct gene compositions. As is typical of viruses in general, there are no universal genes in the archaeal virosphere. Therefore, to obtain a comprehensive picture of the evolutionary relationships between viruses, network analysis methods are more productive than traditional phylogenetic approaches. Here we present a comprehensive comparative analysis of genomes and proteomes from all currently known taxonomically classified and unclassified, cultivated and uncultivated archaeal viruses. We constructed a bipartite network of archaeal viruses that includes two classes of nodes, the genomes and gene families that connect them. Dissection of this network using formal community detection methods reveals strong modularity, with 10 distinct modules and 3 putative supermodules. However, compared to similar previously analyzed networks of eukaryotic and bacterial viruses, the archaeal virus network is sparsely connected. With the exception of the tailed viruses related to bacteriophages of the order Caudovirales and the families Turriviridae and Sphaerolipoviridae that are linked to a distinct supermodule of eukaryotic and bacterial viruses, there are few connector genes shared by different archaeal virus modules. In contrast, most of these modules include, in addition to viruses, capsidless mobile elements, emphasizing tight evolutionary connections between the two types of entities in archaea. The relative contributions of distinct evolutionary origins, in particular from nonviral elements, and insufficient sampling to the sparsity of the archaeal virus network remain to be determined by further exploration of the archaeal virosphere.ImportanceViruses infecting archaea are among the most mysterious denizens of the virosphere. Many of these viruses display no genetic or even morphological relationship to viruses of bacteria and eukaryotes, raising questions regarding their origins and position in the global virosphere. Analysis of 5,740 protein sequences from 116 genomes allowed dissection of the archaeal virus network and showed that most groups of archaeal viruses are evolutionarily connected to capsidless mobile genetic elements, including various plasmids and transposons. This finding could reflect actual independent origins of the distinct groups of archaeal viruses from different nonviral elements, providing important insights into the emergence and evolution of the archaeal virome.

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Dataset Information

Structure of a filamentous virus uncovers familial ties within the archaeal virosphere.

Publications

Structure of a filamentous virus uncovers familial ties within the archaeal virosphere.

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