Duplodnaviria

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Duplodnaviria
Duplodnaviria virion morphology.jpg
Illustrated sample of Duplodnaviria virions
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(unranked): Virus
Realm: Duplodnaviria
Kingdom:Heunggongvirae
Subtaxa

See text

Synonyms [1] [2]
  • HK97-like group
  • HK97 major capsid protein supermodule

Duplodnaviria is a realm of viruses that includes all double-stranded DNA viruses that encode the HK97 fold major capsid protein. The HK97 fold major capsid protein (HK97 MCP) is the primary component of the viral capsid, which stores the viral deoxyribonucleic acid (DNA). Viruses in the realm also share a number of other characteristics, such as an icosahedral capsid, an opening in the viral capsid called a portal, a protease enzyme that empties the inside of the capsid prior to DNA packaging, and a terminase enzyme that packages viral DNA into the capsid.

Contents

Duplodnaviria was established in 2019 based on the shared characteristics of viruses in the realm. There are two groups of viruses in Duplodnaviria: tailed bacteriophages of the order Caudovirales , which infect prokaryotes, and herpesviruses of the order Herpesvirales , which infect animals. Tailed bacteriophages are very diverse and ubiquitous worldwide, and they may be the oldest lineage of viruses. Herpesviruses either share a common ancestor with tailed bacteriophages or are a breakaway group from within Caudovirales.

Tailed bacteriophages are important in marine ecology by recycling nutrients in organic material from their hosts and are the focus of much research, and herpesviruses are associated with a variety of diseases in animals, including humans. A common feature among viruses in Duplodnaviria is that many are able to persist in their host for long periods of time without replicating while still being able to resurface in the future. Examples of this include the herpes simplex virus, which causes recurring infections, and the varicella zoster virus, which initially causes chickenpox early in life then shingles later in life.

Etymology

The name Duplodnaviria is a portmanteau of duplo, the Latin word for double, dna, from deoxyribonucleic acid (DNA), referencing that all members of the realm at founding had double-stranded DNA genomes, and -viria, which is the suffix used for virus realms. Duplodnaviria is monotypic, having only one kingdom, Heunggongvirae, so both the realm and kingdom have the same definition. Heunggongvirae takes the first part of its name from Cantonese 香港 [Hēunggóng], meaning and approximately pronounced "Hong Kong", which is a reference to Escherichia virus HK97 , the founding member of the HK97 (Hong Kong 97) fold MCP viruses, and the suffix -virae, which is the suffix used for virus kingdoms. [2]

Characteristics

All viruses in Duplodnaviria contain a distinct icosahedral capsid that is composed of a major capsid protein that contains a unique folded structure, called the HK97 fold, named after the folded structure of the MCP of the bacteriophage species Escherichia virus HK97. Despite having significant variation across Duplodnaviria, the base structure of the protein is retained among all species in the realm. Other shared proteins that involve the structure and assembly of capsids include a portal protein that the opening of the capsid is made of, a protease that empties the capsid before DNA is inserted, and the terminase enzyme that inserts the DNA into the capsid. [1] [2] [3]

After HK97 MCPs have been synthesized by the host cell's ribosomes, the viral capsid is assembled from them with the proteins bonding to each other. The inside of the capsid contains scaffold proteins that guide the geometric construction of the capsid. In the absence of separate scaffolding proteins, the delta domain of HK97 MCP, which faces toward the inside of the capsid, acts as a scaffold protein. [1] [3] [4]

A cylindrical opening in the capsid, called a portal, that serves as the entrance and exit for viral DNA is created with portal proteins at one of the 12 vertices of the capsid. The scaffold protein, which may be the delta domain of HK97 MCP, is removed from the inside of the capsid by the capsid maturation protease, which may also be a part of the scaffolding, breaking it and itself down to smaller molecules in a process called proteolysis that leaves the inside of the capsid empty. [3] [4]

At the same time as capsid assembly, replication of the viral DNA occurs, creating concatemers, long molecules of DNA containing numerous copies of the viral genome. The enzyme terminase, made of two subunits, large and small, finds the viral DNA inside of the cell via the small subunit, cuts the concatemers, and creates the termini, or endings, of the genomes. Terminase recognizes a packaging signal in the genome and cuts the nucleic acid, creating a free end that it binds to. [3]

The terminase, now bound to the concatemer, attaches itself to the capsid portal and begins translocating the DNA from outside the capsid to the inside, using energy generated from ATP hydrolysis by the large subunit. As more DNA is inserted into the capsid, the capsid expands in size, becomes thinner, and its surface becomes flatter and more angular. Once the genome is completely inside, terminase cuts the concatemer again, completing packaging. Terminase then detaches itself from the portal and proceeds to repeat this process until all genomes in the concatemer have been packaged. [3]

For tailed bacteriophages, after DNA packaging, the tail of the virion, which was assembled separately, is attached to the capsid, commonly called the "head" of tailed bacteriophages, at the portal. Tailed bacteriophages also sometimes have "decoration" proteins that attach to the capsid's surface in order to reinforce the capsid's structure. After the virion is fully assembled inside the host cell, it leaves the cell. [3] Tailed bacteriophages leave the cell via lysis, rupturing of the cell membrane, that causes cell death, [5] and herpesviruses leave by budding from the host cell membrane, using the membrane as a viral envelope that covers the capsid. [6]

Phylogenetics

Tailed bacteriophages are potentially the oldest lineage of viruses in the world because they are ubiquitous worldwide, only infect prokaryotes, and have a high level of diversity. Their highly divergent virion structures may point to this or may indicate separate origins. The origin of Herpesvirales is unclear, but there are two likely scenarios. First, ancestral lineages of Caudoviricetes may have produced clades at various times that were capable of infecting eukaryotes, and the strong similarity that Herpesvirales has with Caudoviricetes may indicate that it is a more recent descendant of one such lineage. The second likely scenario is that Herpesvirales is a breakaway clade from within Caudoviricetes, which is supported by one of the Caudoviricetes subfamilies, Tevenvirinae , showing a relatively high genetic relation to herpesviruses based on certain protein amino acid sequences. [7] It has been suggested that Duplodnaviria predates the last universal common ancestor (LUCA) of cellular life and that viruses in the realm were present in the LUCA. [8]

The HK97 fold MCP appears to have been created from a DUF1884 protein family domain that was inserted into a strand-helix-strand-strand (SHS2) fold protein related to the dodecin protein family. The resulting protein was then acquired by a mobile genetic element, leading to the creation of duplodnaviruses. [8] Outside of Duplodnaviria, an HK97-like fold is only found in encapsulins, a type of prokaryotic nanocompartment that encapsulate a variety of cargo proteins related to the oxidative stress response. Encapsulins assemble into icosahedrons like the capsids of duplodnaviruses, but the HK97 MCP in viruses is much more divergent and widespread than in encapsulins, which form a narrow monophyletic clade. As such, it is more likely that encapsulins are derived from viruses than vice versa. Archaea of the phylum Thermoproteota (formerly Crenarchaeota) contain encapsulins but are not known to be infected by tailed bacteriophages though, so the relation between encapsulins and Duplodnaviria remains unresolved. [9]

The ATPase subunit of Duplodnaviria terminases that generates energy for packaging viral DNA has the same general structural design of the P-loop fold as the packaging ATPases of double jelly roll fold MCP viruses in the realm Varidnaviria but are otherwise not directly related to each other. While viruses in Duplodnaviria make use of the HK97 fold for their major capsid proteins, the major capsid proteins of viruses in Varidnaviria instead are marked by single or double vertical jelly roll folds. [2]

Classification

Duplodnaviria contains only one kingdom, and this kingdom is subdivided into two phyla. This taxonomy can be visualized as follows: [10]

  • Kingdom: Heunggongvirae
  • Phylum: Peploviricota
  • Class: Herviviricetes
  • Phylum: Uroviricota

As all viruses in the realm are double-stranded DNA (dsDNA) viruses, the realm belongs to Group I: dsDNA viruses of Baltimore classification, a classification system based on a virus's manner of messenger RNA (mRNA) production, often used alongside standard virus taxonomy, which is based on evolutionary history. [2] Realms are the highest level of taxonomy used for viruses and Duplodnaviria is one of six, the other five being Adnaviria , Monodnaviria , Riboviria , Ribozyviria and Varidnaviria . [10]

Interactions with hosts

Viral shunt

Tailed bacteriophages are ubiquitous worldwide and are a major cause of death among prokaryotes. Infection may lead to cell death via lysis, the rupturing of the cell membrane. As a result of lysis, organic material from the killed prokaryotes is released into the environment, contributing to a process called viral shunt. Tailed bacteriophages shunt nutrients from organic material away from higher trophic levels so that they can be consumed by organisms in lower trophic levels, which has the effects of recycling nutrients and promoting increased diversity among marine life. [11]

Disease

Herpesviruses are associated with a wide range of diseases in their hosts, including a respiratory tract illness in chickens, [12] a respiratory and reproductive illness in cattle, [13] and tumors in sea turtles. [14] In humans, herpesviruses usually cause various epithelial diseases such as herpes simplex, chickenpox and shingles, and Kaposi's sarcoma. [15] [16] [17] Initial infection causes acute symptoms and leads to lifelong infection via latency. Herpesviruses may emerge from their latency to cause illnesses, which may have severe symptoms such as encephalitis and pneumonia. [18] [19]

Latency

Lytic and lysogenic cycles of tailed bacteriophages Phage2.JPG
Lytic and lysogenic cycles of tailed bacteriophages

Viruses in Duplodnaviria have two different types of replication cycles, called the lytic cycle, whereby infection leads directly to virion formation and exit from the host cell, and the lysogenic cycle, whereby a latent infection retains the viral DNA inside of the host cell without virion formation, either as an episome or via integration into the host cell's DNA, with the possibility of returning to the lytic cycle in the future. Viruses that can replicate through the lysogenic cycle are called temperate or lysogenic viruses. Tailed bacteriophages vary in their temperateness, whereas all herpesviruses are temperate and able to avoid detection by the host's immune system, causing lifelong infections. [20] [21]

History

Tailed bacteriophages were discovered independently by Frederick Twort in 1915 and Félix d'Hérelle in 1917, and they have been the focus of much research since then. [22] Diseases in humans caused by herpesviruses have been recognized for much of recorded history, and person-to-person transmission of the herpes simplex virus, the first herpesvirus discovered, was first recognized in 1893 by Émile Vidal. [23] [24]

Over time, the two groups were increasingly found to share many characteristics, and their genetic relation was formalized with the establishment of Duplodnaviria in 2019. The creation of the kingdom, phyla, and classes of the realm in the same year has also created a framework to more easily allow major reorganization of Caudovirales, which is growing in size significantly and which may require tailed bacteriophages to be promoted to the rank of class or higher. [2]

See also

Related Research Articles

<span class="mw-page-title-main">DNA virus</span> Virus that has DNA as its genetic material

A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and those that have one strand of DNA in their genome, called single-stranded DNA (ssDNA) viruses. dsDNA viruses primarily belong to two realms: Duplodnaviria and Varidnaviria, and ssDNA viruses are almost exclusively assigned to the realm Monodnaviria, which also includes some dsDNA viruses. Additionally, many DNA viruses are unassigned to higher taxa. Reverse transcribing viruses, which have a DNA genome that is replicated through an RNA intermediate by a reverse transcriptase, are classified into the kingdom Pararnavirae in the realm Riboviria.

<i>Parvoviridae</i> Family of viruses

Parvoviruses are a family of animal viruses that constitute the family Parvoviridae. They have linear, single-stranded DNA (ssDNA) genomes that typically contain two genes encoding for a replication initiator protein, called NS1, and the protein the viral capsid is made of. The coding portion of the genome is flanked by telomeres at each end that form into hairpin loops that are important during replication. Parvovirus virions are small compared to most viruses, at 23–28 nanometers in diameter, and contain the genome enclosed in an icosahedral capsid that has a rugged surface.

<i>Escherichia virus T4</i> Species of bacteriophase

Escherichia virus T4 is a species of bacteriophages that infect Escherichia coli bacteria. It is a double-stranded DNA virus in the subfamily Tevenvirinae from the family Myoviridae. T4 is capable of undergoing only a lytic lifecycle and not the lysogenic lifecycle. The species was formerly named T-even bacteriophage, a name which also encompasses, among other strains, Enterobacteria phage T2, Enterobacteria phage T4 and Enterobacteria phage T6.

<span class="mw-page-title-main">Caudovirales</span> Class of viruses

Caudoviricetes is an class of viruses known as the tailed bacteriophages. Under the Baltimore classification scheme, the Caudoviricetes are group I viruses as they have double stranded DNA (dsDNA) genomes, which can be anywhere from 18,000 base pairs to 500,000 base pairs in length. The virus particles have a distinct shape; each virion has an icosahedral head that contains the viral genome, and is attached to a flexible tail by a connector protein. The order encompasses a wide range of viruses, many containing genes of similar nucleotide sequence and function. However, some tailed bacteriophage genomes can vary quite significantly in nucleotide sequence, even among the same genus. Due to their characteristic structure and possession of potentially homologous genes, it is believed these bacteriophages possess a common origin.

<i>Herpesviridae</i> Family of DNA viruses

Herpesviridae is a large family of DNA viruses that cause infections and certain diseases in animals, including humans. The members of this family are also known as herpesviruses. The family name is derived from the Greek word ἕρπειν, referring to spreading cutaneous lesions, usually involving blisters, seen in flares of herpes simplex 1, herpes simplex 2 and herpes zoster (shingles). In 1971, the International Committee on the Taxonomy of Viruses (ICTV) established Herpesvirus as a genus with 23 viruses among four groups. As of 2020, 115 species are recognized, all but one of which are in one of the three subfamilies. Herpesviruses can cause both latent and lytic infections.

<span class="mw-page-title-main">Baltimore classification</span> Virus classification system made by David Baltimore

Baltimore classification is a system used to classify viruses based on their manner of messenger RNA (mRNA) synthesis. By organizing viruses based on their manner of mRNA production, it is possible to study viruses that behave similarly as a distinct group. Seven Baltimore groups are described that take into consideration whether the viral genome is made of deoxyribonucleic acid (DNA) or ribonucleic acid (RNA), whether the genome is single- or double-stranded, and whether the sense of a single-stranded RNA genome is positive or negative.

<span class="mw-page-title-main">Herpes simplex virus</span> Species of virus

Herpes simplex virus1 and 2, also known by their taxonomical names Human alphaherpesvirus 1 and Human alphaherpesvirus 2, are two members of the human Herpesviridae family, a set of viruses that produce viral infections in the majority of humans. Both HSV-1 and HSV-2 are very common and contagious. They can be spread when an infected person begins shedding the virus.

<i>Gammaherpesvirinae</i> Subfamily of viruses

Gammaherpesvirinae is a subfamily of viruses in the order Herpesvirales and in the family Herpesviridae. Viruses in Gammaherpesvirinae are distinguished by reproducing at a more variable rate than other subfamilies of Herpesviridae. Mammals serve as natural hosts. There are 43 species in this subfamily, divided among 7 genera with three species unassigned to a genus. Diseases associated with this subfamily include: HHV-4: infectious mononucleosis. HHV-8: Kaposi's sarcoma.

Salmonella virus P22 is a bacteriophage in the Podoviridae family that infects Salmonella typhimurium. Like many phages, it has been used in molecular biology to induce mutations in cultured bacteria and to introduce foreign genetic material. P22 has been used in generalized transduction and is an important tool for investigating Salmonella genetics.

HHV Capsid Portal Protein, or HSV-1 UL-6 protein, is the protein which forms a cylindrical portal in the capsid of Herpes simplex virus (HSV-1). The protein is commonly referred to as the HSV-1 UL-6 protein because it is the transcription product of Herpes gene UL-6.

<span class="mw-page-title-main">Viral tegument</span> Cluster of proteins that lines the space between the envelope and nucleocapsid of all herpesviruses

A viral tegument or tegument, more commonly known as a viral matrix, is a cluster of proteins that lines the space between the envelope and nucleocapsid of all herpesviruses. The tegument generally contains proteins that aid in viral DNA replication and evasion of the immune response, typically with inhibition of signalling in the immune system and activation of interferons. The tegument is usually released shortly after infection into the cytoplasm. These proteins are usually formed within the late phase of the viral infectious cycle, after viral genes have been replicated. Much information regarding viral teguments has been gathered from studying herpes simplex virus.

<span class="mw-page-title-main">Virus</span> Infectious agent that replicates in cells

A virus is a submicroscopic infectious agent that replicates only inside the living cells of an organism. Viruses infect all life forms, from animals and plants to microorganisms, including bacteria and archaea. Since Dmitri Ivanovsky's 1892 article describing a non-bacterial pathogen infecting tobacco plants and the discovery of the tobacco mosaic virus by Martinus Beijerinck in 1898, more than 9,000 of the millions of virus species have been described in detail. Viruses are found in almost every ecosystem on Earth and are the most numerous type of biological entity. The study of viruses is known as virology, a subspeciality of microbiology.

<i>Herpesvirales</i> Order of viruses

The Herpesvirales is an order of dsDNA viruses with animal hosts, characterised by a common morphology consisting of an icosahedral capsid enclosed in a glycoprotein-containing lipid envelope. Common infections in humans caused by members of this order include cold sores, genital herpes, chickenpox, shingles, and glandular fever. Herpesvirales is the sole order in the class Herviviricetes, which is the sole class in the phylum Peploviricota.

Tristromaviridae is a family of viruses. Archaea of the genera Thermoproteus and Pyrobaculum serve as natural hosts. Tristromaviridae is the sole family in the order Primavirales. There are two genera and three species in the family.

Escherichia virus CC31, formerly known as Enterobacter virus CC31, is a dsDNA bacteriophage of the subfamily Tevenvirinae responsible for infecting the bacteria family of Enterobacteriaceae. It is one of two discovered viruses of the genus Karamvirus, diverging away from the previously discovered T4virus, as a clonal complex (CC). CC31 was first isolated from Escherichia coli B strain S/6/4 and is primarily associated with Escherichia, even though is named after Enterobacter.

Ranid herpesvirus 1 (RaHV-1), also known as the Lucké tumor herpesvirus (LTHV), is a double-stranded DNA virus within the order Herpesvirales. The virus was initially observed within renal tumors in 1934 by Baldwin Lucké, and more recently has become identifiable through the use of PCR in samples isolated from frog tumors. RaHV-1 causes renal tumors within the northern leopard frog, Rana pipiens. The virus has not yet been isolated in vitro within cell lines, meaning that while its existence and symptoms are fairly evident, its methods of transmission, cell infection, and reproduction are largely unknown.

In virology, realm is the highest taxonomic rank established for viruses by the International Committee on Taxonomy of Viruses (ICTV), which oversees virus taxonomy. Six virus realms are recognized and united by specific highly conserved traits:

<i>Varidnaviria</i> Realm of viruses

Varidnaviria is a realm of viruses that includes all DNA viruses that encode major capsid proteins that contain a vertical jelly roll fold. The major capsid proteins (MCP) form into pseudohexameric subunits of the viral capsid, which stores the viral deoxyribonucleic acid (DNA), and are perpendicular, or vertical, to the surface of the capsid. Apart from this, viruses in the realm also share many other characteristics, such as minor capsid proteins (mCP) with the vertical jelly roll fold, an ATPase that packages viral DNA into the capsid, and a DNA polymerase that replicates the viral genome.

<span class="mw-page-title-main">Archaeal virus</span>

An archaeal virus is a virus that infects and replicates in archaea, a domain of unicellular, prokaryotic organisms. Archaeal viruses, like their hosts, are found worldwide, including in extreme environments inhospitable to most life such as acidic hot springs, highly saline bodies of water, and at the bottom of the ocean. They have been also found in the human body. The first known archaeal virus was described in 1974 and since then, a large diversity of archaeal viruses have been discovered, many possessing unique characteristics not found in other viruses. Little is known about their biological processes, such as how they replicate, but they are believed to have many independent origins, some of which likely predate the last archaeal common ancestor (LACA).

<i>Adnaviria</i> Realm of viruses

Adnaviria is a realm of viruses that includes archaeal viruses that have a filamentous virion and a linear, double-stranded DNA genome. The genome exists in A-form (A-DNA) and encodes a dimeric major capsid protein (MCP) that contains the SIRV2 fold, a type of alpha-helix bundle containing four helices. The virion consists of the genome encased in capsid proteins to form a helical nucleoprotein complex. For some viruses, this helix is surrounded by a lipid membrane called an envelope. Some contain an additional protein layer between the nucleoprotein helix and the envelope. Complete virions are long and thin and may be flexible or a stiff like a rod.

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Further reading