scholarly journals ATP serves as a nucleotide switch coupling the genome maturation and packaging motor complexes of a virus assembly machine

2020 ◽  
Vol 48 (9) ◽  
pp. 5006-5015
Author(s):  
Qin Yang ◽  
Carlos E Catalano
Keyword(s):  
Atp Hydrolysis ◽  
Virus Assembly ◽  
Genome Packaging ◽  
Dna Viruses ◽  
Motor Complex ◽  
Double Stranded Dna ◽  
Tightly Coupled ◽  
Switch Mechanism ◽  
Genome Maturation ◽  
Dsdna Viruses

Abstract The assembly of double-stranded DNA viruses, from phages to herpesviruses, is strongly conserved. Terminase enzymes processively excise and package monomeric genomes from a concatemeric DNA substrate. The enzymes cycle between a stable maturation complex that introduces site-specific nicks into the duplex and a dynamic motor complex that rapidly translocates DNA into a procapsid shell, fueled by ATP hydrolysis. These tightly coupled reactions are catalyzed by terminase assembled into two functionally distinct nucleoprotein complexes; the maturation complex and the packaging motor complex, respectively. We describe the effects of nucleotides on the assembly of a catalytically competent maturation complex on viral DNA, their effect on maturation complex stability and their requirement for the transition to active packaging motor complex. ATP plays a major role in regulating all of these activities and may serve as a ‘nucleotide switch’ that mediates transitions between the two complexes during processive genome packaging. These biological processes are recapitulated in all of the dsDNA viruses that package monomeric genomes from concatemeric DNA substrates and the nucleotide switch mechanism may have broad biological implications with respect to virus assembly mechanisms.

scholarly journals Adintoviruses: A Proposed Animal-Tropic Family of Midsize Eukaryotic Linear dsDNA (MELD) Viruses

2020 ◽  
Author(s):  
Gabriel J Starrett ◽  
Michael J Tisza ◽  
Nicole L Welch ◽  
Anna K Belford ◽  
Alberto Peretti ◽  
...  
Keyword(s):  
Genome Packaging ◽  
Metagenomic Sequence ◽  
Dna Viruses ◽  
Diverse Range ◽  
Integrase Gene ◽  
Data Mining Approach ◽  
Double Stranded Dna ◽  
Wide Range ◽  
Linear Dsdna ◽  
Dsdna Viruses

Abstract Polintons (also known as Mavericks) were initially identified as a widespread class of eukaryotic transposons named for their hallmark type B DNA polymerase and retrovirus-like integrase genes. It has since been recognized that many polintons encode possible capsid proteins and viral genome-packaging ATPases similar to those of a diverse range of double-stranded DNA (dsDNA) viruses. This supports the inference that at least some polintons are actually viruses capable of cell-to-cell spread. At present, there are no polinton-associated capsid protein genes annotated in public sequence databases. To rectify this deficiency, we used a data-mining approach to investigate the distribution and gene content of polinton-like elements and related DNA viruses in animal genomic and metagenomic sequence datasets. The results define a discrete family-like clade of viruses with two genus-level divisions. We propose the family name Adintoviridae, connoting similarities to adenovirus virion proteins and the presence of a retrovirus-like integrase gene. Although adintovirus-class PolB sequences were detected in datasets for fungi and various unicellular eukaryotes, sequences resembling adintovirus virion proteins and accessory genes appear to be restricted to animals. Degraded adintovirus sequences are endogenized into the germlines of a wide range of animals, including humans.

scholarly journals Adintoviruses: An Animal-Tropic Family of Midsize Eukaryotic Linear dsDNA (MELD) Viruses

2019 ◽  
Author(s):  
Gabriel J. Starrett ◽  
Michael J. Tisza ◽  
Nicole L. Welch ◽  
Anna K. Belford ◽  
Alberto Peretti ◽  
...  
Keyword(s):  
Genome Packaging ◽  
Metagenomic Sequence ◽  
Dna Viruses ◽  
Diverse Range ◽  
Data Mining Approach ◽  
Double Stranded Dna ◽  
Wide Range ◽  
The Family ◽  
Linear Dsdna ◽  
Dsdna Viruses

AbstractPolintons (also known as Mavericks) were initially identified as a widespread class of eukaryotic transposons named for their hallmark type B DNA polymerase and retrovirus-like integrase genes. It has since been recognized that many polintons encode possible capsid proteins and viral genome-packaging ATPases similar to those of a diverse range of double-stranded DNA (dsDNA) viruses. This supports the inference that at least some polintons are viruses that remain capable of cell-to-cell spread. At present, there are no polinton-associated capsid protein genes annotated in public sequence databases. To rectify this deficiency, we used a data-mining approach to investigate the distribution and gene content of polinton-like elements and related DNA viruses in animal genomic and metagenomic sequence datasets. The results define a discrete family-like clade of animal-specific viruses with two genus-level divisions. We suggest the family name Adintoviridae, connoting similarities to adenovirus virion proteins and the presence of a retrovirus-like integrase gene. Although adintovirus-class PolB sequences were detected in datasets for fungi and various unicellular eukaryotes, sequences resembling adintovirus virion proteins and accessory genes appear to be restricted to animals. Degraded adintovirus sequences are endogenized into the germlines of a wide range of animals, including humans.

scholarly journals Molecular fossils reveal ancient associations of dsDNA viruses with several phyla of fungi

2020 ◽  
Vol 6 (1) ◽  
Author(s):  
Zhen Gong ◽  
Yu Zhang ◽  
Guan-Zhu Han
Keyword(s):  
Giant Virus ◽  
Virus Infections ◽  
Dsdna Virus ◽  
Dna Viruses ◽  
Molecular Fossils ◽  
Double Stranded Dna ◽  
Fungal Genomes ◽  
Nucleocytoplasmic Large Dna Viruses ◽  
Dsdna Viruses

Abstract Little is known about the infections of double-stranded DNA (dsDNA) viruses in fungi. Here, we use a paleovirological method to systematically identify the footprints of past dsDNA virus infections within the fungal genomes. We uncover two distinct groups of endogenous nucleocytoplasmic large DNA viruses (NCLDVs) in at least seven fungal phyla (accounting for about a third of known fungal phyla), revealing an unprecedented diversity of dsDNA viruses in fungi. Interestingly, one fungal dsDNA virus lineage infecting six fungal phyla is closely related to the giant virus Pithovirus, suggesting giant virus relatives might widely infect fungi. Co-speciation analyses indicate fungal NCLDVs mainly evolved through cross-species transmission. Taken together, our findings provide novel insights into the diversity and evolution of NCLDVs in fungi.

scholarly journals Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Nicholas P. Stone ◽  
Gabriel Demo ◽  
Emily Agnello ◽  
Brian A. Kelch
Keyword(s):  
Major Capsid Protein ◽  
Extreme Environment ◽  
Structural Basis ◽  
Genome Packaging ◽  
Virus Capsid ◽  
Dna Viruses ◽  
Double Stranded Dna ◽  
High Internal Pressure ◽  
Extracellular Environment ◽  
Catch Bonds

Abstract The capsids of double-stranded DNA viruses protect the viral genome from the harsh extracellular environment, while maintaining stability against the high internal pressure of packaged DNA. To elucidate how capsids maintain stability in an extreme environment, we use cryoelectron microscopy to determine the capsid structure of thermostable phage P74-26 to 2.8-Å resolution. We find P74-26 capsids exhibit an overall architecture very similar to those of other tailed bacteriophages, allowing us to directly compare structures to derive the structural basis for enhanced stability. Our structure reveals lasso-like interactions that appear to function like catch bonds. This architecture allows the capsid to expand during genome packaging, yet maintain structural stability. The P74-26 capsid has T = 7 geometry despite being twice as large as mesophilic homologs. Capsid capacity is increased with a larger, flatter major capsid protein. Given these results, we predict decreased icosahedral complexity (i.e. T ≤ 7) leads to a more stable capsid assembly.

scholarly journals Specificity of Baculovirus P6.9 Basic DNA-Binding Proteins and Critical Role of the C Terminus in Virion Formation

2010 ◽  
Vol 84 (17) ◽  
pp. 8821-8828 ◽  
Author(s):  
Manli Wang ◽  
Era Tuladhar ◽  
Shu Shen ◽  
Hualin Wang ◽  
Monique M. van Oers ◽  
...  
Keyword(s):  
Virus Assembly ◽  
Critical Role ◽  
Nucleocapsid Proteins ◽  
Double Stranded Dna ◽  
C Terminus ◽  
Sequence Elements ◽  
Eukaryotic Organisms ◽  
Dsdna Viruses ◽  
Virion Formation

ABSTRACT The majority of double-stranded DNA (dsDNA) viruses infecting eukaryotic organisms use host- or virus-expressed histones or protamine-like proteins to condense their genomes. In contrast, members of the Baculoviridae family use a protamine-like protein named P6.9. The dephosphorylated form of P6.9 binds to DNA in a non-sequence-specific manner. By using a p6.9-null mutant of Autographa californica multiple nucleopolyhedrovirus (AcMNPV), we demonstrate that P6.9 is not required for viral DNA replication but is essential for the production of infectious virus. Virion production was rescued by P6.9 homologs from a number of Alpha baculovirus species and one Gammabaculovirus species but not from the genus Betabaculovirus, comprising the granuloviruses, or by the P6.9 homolog VP15 from the unrelated white spot syndrome virus of shrimp. Mutational analyses demonstrated that AcMNPV P6.9 with a conserved 11-residue deletion of the C terminus was not capable of rescuing p6.9-null AcMNPV, while a chimeric Betabaculovirus P6.9 containing the P6.9 C-terminal region of an Alphabaculovirus strain was able to do so. This implies that the C terminus of baculovirus P6.9 contains sequence elements essential for virion formation. Such elements may possibly interact with species- or genus-specific domains of other nucleocapsid proteins during virus assembly.

scholarly journals Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

2019 ◽  
Vol 116 (39) ◽  
pp. 19585-19592 ◽  
Author(s):  
Julien Guglielmini ◽  
Anthony C. Woo ◽  
Mart Krupovic ◽  
Patrick Forterre ◽  
Morgan Gaia
Keyword(s):  
Phylogenetic Trees ◽  
Dna Viruses ◽  
Double Stranded Dna ◽  
Virion Morphogenesis ◽  
Eukaryotic Dna ◽  
Dsdna Viruses ◽  
Virion Formation ◽  
Intense Debate ◽  
Core Genes

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.

scholarly journals Temperature effects on virion volume and genome length in dsDNA viruses

2016 ◽  
Vol 12 (3) ◽  
pp. 20160023 ◽  
Author(s):  
Rachel L. Nifong ◽  
James F. Gillooly
Keyword(s):  
Environmental Temperature ◽  
Size Variation ◽  
Genome Length ◽  
Dsdna Virus ◽  
Dna Viruses ◽  
Double Stranded Dna ◽  
Virus Size ◽  
Dsdna Viruses ◽  
Gene Overlap ◽  
Growth And Reproduction

Heterogeneity in rates of survival, growth and reproduction among viruses is related to virus particle (i.e. virion) size, but we have little understanding of the factors that govern the four to five orders of magnitude in virus size variation. Here, we analyse variation in virion size in 67 double-stranded DNA viruses (i.e. dsDNA) that span all major biomes, and infect organisms ranging from single-celled prokaryotes to multicellular eukaryotes. We find that two metrics of virion size (i.e. virion volume and genome length) decrease by about 55-fold as the temperature of occurrence increases from 0 to 40°C. We also find that gene overlap increases exponentially with temperature, such that smaller viruses have proportionally greater gene overlap at higher temperatures. These results indicate dsDNA virus size increases with environmental temperature in much the same way as the cell or genome size of many host species.

scholarly journals Architect of Virus Assembly: the Portal Protein Nucleates Procapsid Assembly in Bacteriophage P22

2019 ◽  
Vol 93 (9) ◽  
Author(s):  
Tina Motwani ◽  
Carolyn M. Teschke
Keyword(s):  
Virus Assembly ◽  
Genetic Material ◽  
Scaffolding Protein ◽  
Scaffolding Proteins ◽  
Bacteriophage P22 ◽  
Particle Assembly ◽  
Portal Protein ◽  
Double Stranded Dna ◽  
Dsdna Viruses

ABSTRACTTailed double-stranded DNA (dsDNA) bacteriophages, herpesviruses, and adenoviruses package their genetic material into a precursor capsid through a dodecameric ring complex called the portal protein, which is located at a unique 5-fold vertex. In several phages and viruses, including T4, Φ29, and herpes simplex virus 1 (HSV-1), the portal forms a nucleation complex with scaffolding proteins (SPs) to initiate procapsid (PC) assembly, thereby ensuring incorporation of only one portal ring per capsid. However, for bacteriophage P22, the role of its portal protein in initiation of procapsid assembly is unclear. We have developed anin vitroP22 assembly assay where portal protein is coassembled into procapsid-like particles (PLPs). Scaffolding protein also catalyzes oligomerization of monomeric portal protein into dodecameric rings, possibly forming a scaffolding protein-portal protein nucleation complex that results in one portal ring per P22 procapsid. Here, we present evidence substantiating that the P22 portal protein, similarly to those of other dsDNA viruses, can act as an assembly nucleator. The presence of the P22 portal protein is shown to increase the rate of particle assembly and contribute to proper morphology of the assembled particles. Our results highlight a key function of portal protein as an assembly initiator, a feature that is likely conserved among these classes of dsDNA viruses.IMPORTANCEThe existence of a single portal ring is essential to the formation of infectious virions in the tailed double-stranded DNA (dsDNA) phages, herpesviruses, and adenoviruses and, as such, is a viable antiviral therapeutic target. How only one portal is selectively incorporated at a unique vertex is unclear. In many dsDNA viruses and phages, the portal protein acts as an assembly nucleator. However, early work on phage P22 assemblyin vivoindicated that the portal protein did not function as a nucleator for procapsid (PC) assembly, leading to the suggestion that P22 uses a unique mechanism for portal incorporation. Here, we show that portal protein nucleates assembly of P22 procapsid-like particles (PLPs). Addition of portal rings to an assembly reaction increases the rate of formation and yield of particles and corrects improper particle morphology. Our data suggest that procapsid assembly may universally initiate with a nucleation complex composed minimally of portal and scaffolding proteins (SPs).

scholarly journals Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure

2018 ◽  
Author(s):  
Nicholas P. Stone ◽  
Gabriel Demo ◽  
Emily Agnello ◽  
Brian A. Kelch
Keyword(s):  
Major Capsid Protein ◽  
Extreme Environment ◽  
Structural Basis ◽  
Genome Packaging ◽  
Virus Capsid ◽  
Dna Viruses ◽  
Double Stranded Dna ◽  
High Internal Pressure ◽  
Extracellular Environment ◽  
Catch Bonds

SUMMARYThe capsids of double-stranded DNA viruses protect the viral genome from the harsh extracellular environment, while maintaining stability against the high internal pressure of packaged DNA. To elucidate how capsids maintain stability in an extreme environment, we used cryoelectron microscopy to determine the capsid structure of the thermostable phage P74-26 to 2.8-Å resolution. We find the P74-26 capsid exhibits an overall architecture that is very similar to those of other tailed bacteriophages, allowing us to directly compare structures to derive the structural basis for enhanced stability. Our structure reveals ‘lasso’-like interactions that appear to function like catch bonds. This architecture allows the capsid to expand during genome packaging, yet maintain structural stability. The P74-26 capsid has T=7 geometry despite being twice as large as mesophilic homologs. Capsid capacity is increased through a novel mechanism with a larger, flatter major capsid protein. Our results suggest that decreased icosahedral complexity (i.e. lower T number) leads to a more stable capsid assembly.

scholarly journals Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

2018 ◽  
Author(s):  
Julien Guglielmini ◽  
Anthony Woo ◽  
Mart Krupovic ◽  
Patrick Forterre ◽  
Morgan Gaia
Keyword(s):  
Phylogenetic Trees ◽  
Dna Viruses ◽  
Double Stranded Dna ◽  
Virion Morphogenesis ◽  
History Of ◽  
Eukaryotic Dna ◽  
Dsdna Viruses ◽  
Virion Formation

AbstractGiant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution and potential roles in the emergence of modern eukaryotes remain a subject of intense debate. Since the characterization of the mimivirus in 2003, many big and giant viruses have been discovered at a steady pace, offering a vast material for evolutionary investigations. In parallel, phylogenetic tools are constantly being improved, offering more rigorous approaches for reconstruction of deep evolutionary history of viruses and their hosts. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of two superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were seemingly transferred from two clades of NCLDVs to proto-eukaryotes, giving rise to two of the three eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.

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