Nature׳s favorite building block: Deciphering folding and capsid assembly of proteins with the HK97-fold

Suhanovsky, Margaret M.; Teschke, Carolyn M.

doi:10.1016/j.virol.2015.02.055

Cited by 98 publications

(112 citation statements)

References 116 publications

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“…There are three major architectural classes of viruses with icosahedral capsids and dsDNA genomes, two of which are featured by viruses infecting hosts in all three cellular domains, testifying to their antiquity (41). The first of these architectural classes includes viruses that build their capsids using the major capsid proteins (MCPs) with the so-called HK97-like fold (45).…”

Section: Discussionmentioning

confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

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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...

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Section: Discussionmentioning

confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

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“…The pBS32 capsid protein ZpbH shows structural similarity (HHpred, E value ϭ e Ϫ47 ), but not sequence similarity, to the capsid from the lambdoid bacteriophage HK97 (40,41). The HK97 capsid protein is translated as a 42-kDa protein, and with the portal protein and protease (corresponding to ZpbJ and ZpbI, respectively), self-assembles into a structural stage called prohead I (42,43).…”

Section: Discussionmentioning

confidence: 99%

ZpdN, a Plasmid-Encoded Sigma Factor Homolog, Induces pBS32-Dependent Cell Death in Bacillus subtilis

et al. 2016

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The ancestral Bacillus subtilis strain 3610 contains an 84-kb plasmid called pBS32 that was lost during domestication of commonly used laboratory derivatives. Here we demonstrate that pBS32, normally present at 1 or 2 copies per cell, increases in copy number nearly 100-fold when cells are treated with the DNA-damaging agent mitomycin C. Mitomycin C treatment also caused cell lysis dependent on pBS32-borne prophage genes. ZpdN, a sigma factor homolog encoded by pBS32, was required for the plasmid response to DNA damage, and artificial expression of ZpdN was sufficient to induce pBS32 hyperreplication and cell death. Plasmid DNA released by cell death was protected by the capsid protein ZpbH, suggesting that the plasmid was packaged into a phagelike particle. The putative particles were further indicated by CsCl sedimentation but were not observed by electron microscopy and were incapable of killing B. subtilis cells extracellularly. We hypothesize that pBS32-mediated cell death releases a phagelike particle that is defective and unstable. IMPORTANCEProphages are phage genomes stably integrated into the host bacterium's chromosome and less frequently are maintained as extrachromosomal plasmids. Here we report that the extrachromosomal plasmid pBS32 of Bacillus subtilis encodes a prophage that, when activated, kills the host. pBS32 also encodes both the sigma factor homolog ZpdN that is necessary and sufficient for prophage induction and the protein ComI, which is a potent inhibitor of DNA uptake by natural transformation. We provide evidence that the entire pBS32 sequence may be part of the prophage and thus that competence inhibition may be linked to lysogeny.

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“…One is the PRD1-adenovirus lineage of double-stranded DNA (dsDNA) viruses, whose icosahedral capsids are constructed from major capsid proteins characterized by a vertical double beta-barrel fold (12, 23–27). The other includes capsid proteins from the HK97 lineage (28–30), where the icosahedral dsDNA-containing capsid is constructed from the major coat protein with a long spine helix. We also included myosin, globulin, and sialic acid synthase (NANS) as controls and virus coat proteins from single-stranded RNA (ssRNA) comoviruses that also have the double beta-barrel fold, but in a horizontal orientation in the capsid, unlike PRD1-adenovirus lineage viruses with an upright beta-barrel fold (31).…”

Section: Introductionmentioning

confidence: 99%

Nucleic and Amino Acid Sequences Support Structure-Based Viral Classification

Sinclair

Ravantti

Bamford

2017

J Virol

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Viral capsids ensure viral genome integrity by protecting the enclosed nucleic acids. Interactions between the genome and capsid and between individual capsid proteins (i.e., capsid architecture) are intimate and are expected to be characterized by strong evolutionary conservation. For this reason, a capsid structure-based viral classification has been proposed as a way to bring order to the viral universe. The seeming lack of sufficient sequence similarity to reproduce this classification has made it difficult to reject structural convergence as the basis for the classification. We reinvestigate whether the structure-based classification for viral coat proteins making icosahedral virus capsids is in fact supported by previously undetected sequence similarity. Since codon choices can influence nascent protein folding cotranslationally, we searched for both amino acid and nucleotide sequence similarity. To demonstrate the sensitivity of the approach, we identify a candidate gene for the pandoravirus capsid protein. We show that the structure-based classification is strongly supported by amino acid and also nucleotide sequence similarities, suggesting that the similarities are due to common descent. The correspondence between structure-based and sequence-based analyses of the same proteins shown here allow them to be used in future analyses of the relationship between linear sequence information and macromolecular function, as well as between linear sequence and protein folds.IMPORTANCE Viral capsids protect nucleic acid genomes, which in turn encode capsid proteins. This tight coupling of protein shell and nucleic acids, together with strong functional constraints on capsid protein folding and architecture, leads to the hypothesis that capsid protein-coding nucleotide sequences may retain signatures of ancient viral evolution. We have been able to show that this is indeed the case, using the major capsid proteins of viruses forming icosahedral capsids. Importantly, we detected similarity at the nucleotide level between capsid protein-coding regions from viruses infecting cells belonging to all three domains of life, reproducing a previously established structure-based classification of icosahedral viral capsids.

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Nature׳s favorite building block: Deciphering folding and capsid assembly of proteins with the HK97-fold

Cited by 98 publications

References 116 publications

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

ZpdN, a Plasmid-Encoded Sigma Factor Homolog, Induces pBS32-Dependent Cell Death in Bacillus subtilis

Nucleic and Amino Acid Sequences Support Structure-Based Viral Classification

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