Differential virus host-ranges of the Fuselloviridae of hyperthermophilic Archaea: implications for evolution in extreme environments

Ceballos, Ruben Michael; Marceau, Caleb; Marceau, Joshua Ovila; Morris, Steven; Clore, Adam; Stedman, Kenneth M.

doi:10.3389/fmicb.2012.00295

Cited by 29 publications

(48 citation statements)

References 37 publications

(99 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…There are reasons to believe that the known variety of archaeal viruses represents no more than the tip of an iceberg and that comprehensive information on them may shed light on the problems of origin and evolution of viruses and virus-host interactions (16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28).…”

mentioning

confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

View full text Add to dashboard Cite

Encapsidation of genetic material into polyhedral particles is one of the most common structural solutions employed by viruses infecting hosts in all three domains of life. Here, we describe a new virus of hyperthermophilic archaea, Sulfolobus polyhedral virus 1 (SPV1), which condenses its circular double-stranded DNA genome in a manner not previously observed for other known viruses. The genome complexed with virion proteins is wound up sinusoidally into a spherical coil which is surrounded by an envelope and further encased by an outer polyhedral capsid apparently composed of the 20-kDa virion protein. Lipids selectively acquired from the pool of host lipids are integral constituents of the virion. None of the major virion proteins of SPV1 show similarity to structural proteins of known viruses. However, minor structural proteins, which are predicted to mediate host recognition, are shared with other hyperthermophilic archaeal viruses infecting members of the order Sulfolobales. The SPV1 genome consists of 20,222 bp and contains 45 open reading frames, only one-fifth of which could be functionally annotated.IMPORTANCE Viruses infecting hyperthermophilic archaea display a remarkable morphological diversity, often presenting architectural solutions not employed by known viruses of bacteria and eukaryotes. Here we present the isolation and characterization of Sulfolobus polyhedral virus 1, which condenses its genome into a unique spherical coil. Due to the original genomic and architectural features of SPV1, the virus should be considered a representative of a new viral family, "Portogloboviridae."KEYWORDS archaea, hyperthermophile, viral genome, virion structure O ne of the most unexpected results of recent studies on viral diversity is the unveiling of astounding morphological variety of DNA viruses in geothermal environments with temperatures exceeding 80°C (1). Hardly over two dozen viruses isolated from such environments, all parasitizing hyperthermophilic members of the domain Archaea, display diverse virion shapes, many of which have not been observed among viruses from the two other domains of life, Bacteria and Eukarya. Due to distinct genome compositions and peculiar morphological properties of these viruses, 11 new virus families were established by the International Committee on Taxonomy of Viruses (ICTV) for the classification of these viruses (1-4).The remarkable morphological diversity of hyperthermophilic archaeal viruses radically contrasts the limited structural diversity of double-stranded DNA (dsDNA) viruses of Bacteria, nearly all of which, with the exception of several pleomorphic species, have icosahedral particles, with or without helical tails (5). The existing picture seems to accurately reflect the actual differences between bacterial and archaeal viruses. The morphological landscape of bacterial viruses is formed by more than six thousand species, whereas that of hyperthermophilic archaeal viruses is formed by only a couple of dozen known species. Moreover, while no new morpho...

show abstract

mentioning

confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

View full text Add to dashboard Cite

show abstract

“…To better understand the function of SSV1 genetic elements, both specific and random mutagenesis of SSV1 were performed. All 35 ORFs in the SSV1 genome were mutated via insertion and/or deletion (Table 3), and all 78 of these mutants were tested for their ability to infect S. solfataricus S441, a host permissive and susceptible to infection by all SSVs tested to date (38). Insertion mutants in intergenic regions were also isolated and characterized.…”

Section: Resultsmentioning

confidence: 99%

Extreme Mutation Tolerance: Nearly Half of the Archaeal Fusellovirus Sulfolobus Spindle-Shaped Virus 1 Genes Are Not Required for Virus Function, Including the Minor Capsid Protein Gene vp3

Iverson

Goodman

Gorchels

et al. 2017

J Virol

Self Cite

View full text Add to dashboard Cite

Viruses infecting the Archaea harbor a tremendous amount of genetic diversity. This is especially true for the spindle-shaped viruses of the family Fuselloviridae, where Ͼ90% of the viral genes do not have detectable homologs in public databases. This significantly limits our ability to elucidate the role of viral proteins in the infection cycle. To address this, we have developed genetic techniques to study the well-characterized fusellovirus Sulfolobus spindle-shaped virus 1 (SSV1), which infects Sulfolobus solfataricus in volcanic hot springs at 80°C and pH 3. Here, we present a new comparative genome analysis and a thorough genetic analysis of SSV1 using both specific and random mutagenesis and thereby generate mutations in all open reading frames. We demonstrate that almost half of the SSV1 genes are not essential for infectivity, and the requirement for a particular gene correlates well with its degree of conservation within the Fuselloviridae. The major capsid gene vp1 is essential for SSV1 infectivity. However, the universally conserved minor capsid gene vp3 could be deleted without a loss in infectivity and results in virions with abnormal morphology. IMPORTANCE Most of the putative genes in the spindle-shaped archaeal hyperthermophile fuselloviruses have no sequences that are clearly similar to characterized genes. In order to determine which of these SSV genes are important for function, we disrupted all of the putative genes in the prototypical fusellovirus, SSV1. Surprisingly, about half of the genes could be disrupted without destroying virus function. Even deletions of one of the known structural protein genes that is present in all known fuselloviruses, vp3, allows the production of infectious viruses. However, viruses lacking vp3 have abnormal shapes, indicating that the vp3 gene is important for virus structure. Identification of essential genes will allow focused research on minimal SSV genomes and further understanding of the structure of these unique, ubiquitous, and extremely stable archaeal viruses.

show abstract

“…All plasmids derived from pAJC97 were grown in NovaBlue cells (Millipore). Sulfolobus strain S441 was isolated from Lassen Volcanic National Park [8] and was used for Sulfolobus transformations and as an indicator lawn for halo assays. Sulfolobus cells were grown in YS media [20] and E.coli were grown in Lysogeny Broth (LB) with appropriate antibiotics [21,22].…”

Section: Methodsmentioning

confidence: 99%

“…SSV1 has a 15,465 basepair double stranded circular DNA genome, packaged as positively supercoiled DNA in a spindle or lemon-shaped virion with a short tail at one end [3,5,6]. SSV1 infects a number of Sulfolobus species and the virus genome is integrated into the host genome on infection [7][8][9]. How the virus genome is released or how SSV1 binds to Sulfolobus is not clear.…”

Section: Introductionmentioning

confidence: 99%

Genetic Analysis of the Major Capsid Protein of the Archaeal Fusellovirus SSV1: Mutational Flexibility and Conformational Change<strong> </strong>

Iverson

Goodman

Gorchels

et al. 2017

Preprint

Self Cite

View full text Add to dashboard Cite

Abstract:Viruses with spindle or lemon-shaped virions are rare in the world of viruses, but are common in viruses of archaeal extremophiles, possibly due to the extreme conditions in which they thrive. However, the structural and genetic basis for the unique spindle shape is unknown. The best-studied spindle-shaped virus, SSV1, is composed mostly of the major capsid protein VP1. Similar to many other viruses, proteolytic cleavage of VP1 is thought to be critical for virion formation.Unlike half of the genes in SSV1, including the minor capsid protein gene vp3, the vp1 gene does not tolerate deletion or transposon insertion. In order determine the role of the vp1 gene and its proteolysis for virus function, we developed techniques for site-directed mutagenesis of the SSV1 genome and complemented deletion mutants with vp1 genes from other SSVs. By analyzing these mutants we demonstrate that the N-terminus of the VP1 protein is required, but the N-terminus, or entire SSV1 VP1 protein, can be exchanged with VP1s from other SSVs. However, the conserved glutamate at the cleavage site is not essential for infectivity. Interestingly, viruses containing point mutations at this position generate mostly abnormal virions.

show abstract

Differential virus host-ranges of the Fuselloviridae of hyperthermophilic Archaea: implications for evolution in extreme environments

Cited by 29 publications

References 37 publications

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Extreme Mutation Tolerance: Nearly Half of the Archaeal Fusellovirus Sulfolobus Spindle-Shaped Virus 1 Genes Are Not Required for Virus Function, Including the Minor Capsid Protein Gene vp3

Genetic Analysis of the Major Capsid Protein of the Archaeal Fusellovirus SSV1: Mutational Flexibility and Conformational Change<strong> </strong>

Contact Info

Product

Resources

About