Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging

Ptchelkine, Denis; Gillum, Ashley; Mochizuki, Tomohiro; Lucas-Staat, Soizick; Liu, Ying; Krupovìč, Mart; Phillips, Simon E. V.; Prangishvili, David; Huiskonen, Juha T.

doi:10.1038/s41467-017-01668-0

Cited by 35 publications

(33 citation statements)

References 27 publications

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“…Thus, they adopt similar structures not because this is the optimal way to build a virus in such aggressive environments but simply because of common ancestry. This is supported by the fact that the virion organization of the evolutionarily unrelated helical virus APBV1 35 is completely different. The latter virus forms a hollow shell into which the circular dsDNA genome is stuffed.…”

Section: Discussionmentioning

confidence: 91%

Structural conservation in a membrane-enveloped filamentous virus infecting a hyperthermophilic acidophile

et al. 2018

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Different forms of viruses that infect archaea inhabiting extreme environments continue to be discovered at a surprising rate, suggesting that the current sampling of these viruses is sparse. We describe here Sulfolobus filamentous virus 1 (SFV1), a membrane-enveloped virus infecting Sulfolobus shibatae. The virus encodes two major coat proteins which display no apparent sequence similarity with each other or with any other proteins in databases. We have used cryo-electron microscopy at 3.7 Å resolution to show that these two proteins form a nearly symmetrical heterodimer, which wraps around A-form DNA, similar to what has been shown for SIRV2 and AFV1, two other archaeal filamentous viruses. The thin (∼ 20 Å) membrane of SFV1 is mainly archaeol, a lipid species that accounts for only 1% of the host lipids. Our results show how relatively conserved structural features can be maintained across evolution by both proteins and lipids that have diverged considerably.

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Section: Discussionmentioning

confidence: 91%

Structural conservation in a membrane-enveloped filamentous virus infecting a hyperthermophilic acidophile

et al. 2018

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“…SSV10 also tolerates deletion mutations of the minor capsid gene VP3 leading to aberrant, elongated morphology of the virions produced, similar to SSV1. Recently proposed structural models of hyperthermophilic archaeal viruses Aeropyrum pernix bacilliform virus 1 (APBV1) ( Ptchelkine et al. 2017 ) and Acidianus tailed spindle virus ( Hochstein et al.…”

Section: Discussionmentioning

confidence: 99%

Comparative genetic and genomic analysis of the novel fusellovirus Sulfolobus spindle-shaped virus 10

Goodman

Stedman

2018

Virus Evolution

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Viruses that infect thermophilic Archaea are unique in both their structure and genetic makeup. The lemon-shaped fuselloviruses—which infect members of the order Sulfolobales, growing optimally at 80 °C and pH 3—are some of the most ubiquitous and best studied viruses of the thermoacidophilic Archaea. Nonetheless, much remains to be learned about these viruses. In order to investigate fusellovirus evolution, we have isolated and characterized a novel fusellovirus, Sulfolobus spindle-shaped virus 10 (formerly SSV-L1). Comparative genomic analyses highlight significant similarity with both SSV8 and SSV9, as well as conservation of promoter elements within the Fuselloviridae. SSV10 encodes five ORFs with no homology within or outside of the Fuselloviridae, as well as a putatively functional Cas4-like ORF, which may play a role in evading CRISPR-mediated host defenses. Moreover, we demonstrate the ability of SSV10 to withstand mutation in a fashion consistent with mutagenesis in SSV1.

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“…The vast majority of the remaining 10-50% are bacterial and archaeal viruses with icosahedral capsids and helical tails (order Caudovirales). Apart from icosahedra, numerous viruses, especially, those infecting plants and archaea, have elongated, rod-shaped or filamentous capsids [64][65][66][67][68] whereas others, such as numerous negative-strand RNA viruses of animals, have helical nucleocapsids [69][70][71] . Finally, there is a long 'tail' of odd-shaped virions such as those found in numerous viruses of hyperthermophilic archaea 72 .…”

Section: [H1] Diversity Of Virus Capsidsmentioning

confidence: 99%

Origin of viruses: primordial replicators recruiting capsids from hosts

2019

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Viruses are ubiquitous parasites of cellular life and the most abundant biological entities on earth. It is widely accepted that viruses are polyphyletic but a consensus scenario for their ultimate origin(s) is still lacking. Traditionally, three different scenarios have been considered for the origin of viruses: descent from primordial, pre-cellular genetic elements, reductive evolution from cellular ancestors, and escape of genes from cellular hosts achieving partial replicative autonomy and becoming parasitic genetic elements. These three classical scenarios give different timelines for the origin of viruses and do not explain the provenance of the two key functional modules that are responsible, respectively, for virus genome replication and virion morphogenesis. Here we outline a 'chimeric' scenario under which different types of primordial, selfish replicons gave rise to viruses by recruiting host proteins for virion formation. We also propose that new groups of viruses have repeatedly emerged at all stages of the evolution of life, often, through the displacement of ancestral structural and genome replication genes. [H1] Introduction Viruses are the most abundant biological entities on our planet and have major roles in global ecology and evolution of the biosphere 1-4. All cellular organisms, with the possible exception of some intracellular parasitic bacteria, harbour distinctive repertoires of viruses, that is, obligate intracellular genetic parasites that package their genomes into virus particles (virions) 5. The ubiquity of viruses, combined with the theoretical argument that genetic parasites will inevitably emerge in replicator systems 6,7 , implies that the entire course of the evolution of life is actually a story of virus-host coevolution 4,8-10. Accordingly, evolution of life cannot be understood without elucidating the origin(s) of viruses, yet, these origins currently remain mysterious. Historically, three distinct scenarios of virus origin have been considered 11-17 (Figure 1). According to the 'primordial virus world' or 'virus early' hypothesis, viruses are direct descendants of the first replicons that existed during the pre-cellular stage of the evolution of life. By contrast, in the 'reductive virus origin' or 'regression' scenario, viruses are the ultimate products of degeneration of ancestral cells that have lost their autonomy and transitioned to obligate intracellular parasitism. Finally, in the 'escaped genes' scenario, viruses evolved on multiple, independent occasions in different cellular organisms from host genes that acquired the capacity for (quasi)autonomous, selfish replication and infectivity. Accordingly, escaped bacterial, archaeal and eukaryotic genes are thought to have given rise to bacterial, 2 archaeal and eukaryotic viruses, respectively. The three scenarios seem to be mutually exclusive with respect to the origin of any particular group of viruses but different groups of viruses potentially could have evolved via different routes. Over the years, all three scenari...

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Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging

Cited by 35 publications

References 27 publications

Structural conservation in a membrane-enveloped filamentous virus infecting a hyperthermophilic acidophile

Structural conservation in a membrane-enveloped filamentous virus infecting a hyperthermophilic acidophile

Comparative genetic and genomic analysis of the novel fusellovirus Sulfolobus spindle-shaped virus 10

Origin of viruses: primordial replicators recruiting capsids from hosts

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