Orthornavirae

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Orthornavirae
Orthornavirae collage.png
Clockwise from top left: TEM of avian coronavirus, polio virus, bacteriophage Qβ, ebolavirus, tobacco mosaic virus, influenzavirus A, rotavirus, vesicular stomatitis virus. Center: phylogenetic tree of shared replication protein RdRp.
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom:Orthornavirae
Phyla and classes

Positive-strand RNA viruses

Negative-strand RNA viruses

Double-stranded RNA viruses

Ambisense RNA viruses

Orthornavirae is a kingdom of viruses that have genomes made of ribonucleic acid (RNA), including genes which encode an RNA-dependent RNA polymerase (RdRp). The RdRp is used to transcribe the viral RNA genome into messenger RNA (mRNA) and to replicate the genome. Viruses in this kingdom share a number of characteristics which promote rapid evolution, including high rates of genetic mutation, recombination, and reassortment.

Contents

Viruses in Orthornavirae belong to the realm Riboviria . They are descended from a common ancestor that may have been a non-viral molecule that encoded a reverse transcriptase instead of an RdRp for replication. The kingdom is subdivided into five phyla that separate member viruses based on their genome type, host range, and genetic similarity. Viruses with three genome types are included: positive-strand RNA viruses, negative-strand RNA viruses, and double-stranded RNA viruses.

Many of the most widely known viral diseases are caused by members of this kingdom, including coronaviruses, the Ebola virus, influenza viruses, the measles virus, and the rabies virus, as well as the first virus ever discovered, tobacco mosaic virus. In modern history, RdRp-encoding RNA viruses have caused numerous disease outbreaks, and they infect many economically important crops. Most eukaryotic viruses, including most human, animal, and plant viruses, are RdRp-encoding RNA viruses. In contrast, there are relatively few prokaryotic viruses in the kingdom.

Etymology

The first part of Orthornavirae comes from Greek ὀρθός [orthós], meaning straight, the middle part, rna, refers to RNA, and -virae is the suffix used for virus kingdoms. [1]

Characteristics

Structure

Genome type and replication cycle of different RNA viruses 18 2014 1695 Fig1 HTML.webp
Genome type and replication cycle of different RNA viruses

RNA viruses in Orthornavirae typically do not encode many proteins, but most positive-sense, single-stranded (+ssRNA) viruses and some double-stranded RNA (dsRNA) viruses encode a major capsid protein that has a single jelly roll fold, so named because the folded structure of the protein contains a structure that resembles a jelly roll. [2] Many also possess an envelope, a type of lipid membrane that typically surrounds the capsid. In particular, the viral envelope is near-universal among negative-sense, single-stranded (-ssRNA) viruses. [3] [4]

Genome

Viruses in Orthornavirae have three different types of genomes: dsRNA, +ssRNA, and -ssRNA. Single-stranded RNA viruses have either a positive or negative sense strand, and dsRNA viruses have both. This structure of the genome is important in terms of transcription to synthesize viral mRNA as well as replication of the genome, both of which are carried out by the viral enzyme RNA-dependent RNA polymerase (RdRp), also called RNA replicase. [1] [2]

Replication and transcription

Positive-strand RNA viruses

Positive-strand RNA viruses have genomes that can function as mRNA, so transcription is not necessary. However, +ssRNA will produce dsRNA forms as part of the process of replicating their genomes. From the dsRNA, additional positive strands are synthesized, which may be used as mRNA or for genomes for progeny. Because +ssRNA viruses create intermediate dsRNA forms, they have to avoid the host's immune system in order to replicate. +ssRNA viruses accomplish this by replicating in membrane-associated vesicles that are used as replication factories. [5] For many +ssRNA viruses, subgenomic portions of the genome will be transcribed to translate specific proteins, whereas others will transcribe a polyprotein that is cleaved to produce separate proteins. [6] [7]

Negative-strand RNA viruses

Negative-strand RNA viruses have genomes that function as templates from which mRNA can be synthesized directly by RdRp. [8] Replication is the same process but executed on the positive sense antigenome, during which RdRp ignores all transcription signals so that a complete -ssRNA genome can be synthesized. [9] -ssRNA viruses vary between those that initiate transcription by the RdRp creating a cap on the 5'-end (usually pronounced "five prime end") of the genome or by snatching a cap from host mRNA and attaching it to the viral RNA. [10] For many -ssRNA viruses, at the end of transcription, RdRp stutters on a uracil in the genome, synthesizing hundreds of adenines in a row as part of creating a polyadenylated tail for the mRNA. [11] Some -ssRNA viruses are essentially ambisense, and have proteins encoded by both the positive and negative strand, so mRNA is synthesized directly from the genome and from a complementary strand. [12]

Double-stranded RNA viruses

For dsRNA viruses, RdRp transcribes mRNA by using the negative strand as a template. Positive strands may also be used as templates to synthesize negative strands for the construction of genomic dsRNA. dsRNA is not a molecule produced by cells, so cellular life has evolved mechanisms to detect and inactivate viral dsRNA. To counter this, dsRNA viruses typically retain their genomes inside of viral capsid in order to evade the host's immune system. [13]

Evolution

RNA viruses in Orthornavirae experience a high rate of genetic mutations because RdRp is prone to making errors in replication since it typically lacks proofreading mechanisms to repair errors. [note 1] Mutations in RNA viruses are often influenced by host factors such as dsRNA-dependent adenosine deaminases, which edit viral genomes by changing adenosines to inosines. [14] [15] Mutations in genes that are essential for replication lead to a reduced number of progeny, so viral genomes typically contain sequences that are highly conserved over time with relatively few mutations. [16]

Many RdRp-encoding RNA viruses also experience a high rate of genetic recombination, though rates of recombination vary significantly, with lower rates in -ssRNA viruses and higher rates in dsRNA and +ssRNA viruses. There are two types of recombination: copy choice recombination and reassortment. Copy choice recombination occurs when the RdRp switches templates during synthesis without releasing the prior, newly created RNA strand, which generates a genome of mixed ancestry. Reassortment, which is restricted to viruses with segmented genomes, has segments from different genomes packaged into a single virion, or virus particle, which also produces hybrid progeny. [14] [17]

For reassortment, some segmented viruses package their genomes into multiple virions, which produces genomes that are random mixtures of parents, whereas for those that are packaged into a single virion, typically individual segments are swapped. Both forms of recombination can only occur if more than one virus is present in a cell, and the more alleles are present, the more likely recombination is to occur. A key difference between copy choice recombination and reassortment is that copy choice recombination can occur anywhere in a genome, whereas reassortment swaps fully-replicated segments. Therefore, copy choice recombination can produce non-functional viral proteins whereas reassortment cannot. [14] [17] [18] [19]

The mutation rate of a virus is associated with the rate of genetic recombinations. Higher mutation rates increase both the number of advantageous and disadvantageous mutations, whereas higher rates of recombination allows for beneficial mutations to be separated from deleterious ones.[ vague ] Therefore, higher rates of mutations and recombinations, up to a certain point, improve viruses' ability to adapt. [14] [20] Notable examples of this include reassortments that enable cross-species transmission of influenza viruses, which have led to numerous pandemics, as well as the emergence of drug-resistance influenza strains via mutations that were reassorted. [19]

Phylogenetics

Phylogenetic tree with phylum branches highlighted. Negarnaviricota (brown), Duplornaviricota (green), Kitrinoviricota (pink), Pisuviricota (blue), and Lenarviricota (yellow) MBio.02329-18.F1.large.jpg
Phylogenetic tree with phylum branches highlighted. Negarnaviricota (brown), Duplornaviricota (green), Kitrinoviricota (pink), Pisuviricota (blue), and Lenarviricota (yellow)

The exact origin of Orthornavirae is not well established, but the viral RdRp shows a relation to the reverse transcriptase (RT) enzymes of group II introns that encode RTs and retrotransposons, the latter of which are self-replicating DNA sequences that integrate themselves into other parts of the same DNA molecule. [1] [2] A larger study (2022) where new lieneages (phyla) were described, has suggested that RNA viruses descend from the RNA world, suggesting that retroelements (retrotransposons and group II introns) originated from an ancestor related to the phylum Lenarviricota and that members of a newly discovered Taraviricota lineage (phylum) would be the ancestors of all RNA viruses. According to this study the genomes of both dsRNA, +ssRNA and -ssRNA evolved independently and were altered several times in evolution. [21]

Classification

RNA viruses that encode RdRp are assigned to the kingdom Orthornavirae, which contains six official phyla, six unofficial phyla [21] and several taxa that are unassigned to a phylum due to lack of information. The five phyla are separated based on the genome types, host ranges, and genetic similarity of member viruses. [1] [22]

The unassigned taxa are listed hereafter (-viridae denotes family and -virus denotes genus). [1] [22]

The kingdom contains three groups in the Baltimore classification system, which groups viruses together based on their manner of mRNA synthesis, and which is often used alongside standard virus taxonomy, which is based on evolutionary history. Those three groups are Group III: dsRNA viruses, Group IV: +ssRNA viruses, and Group V: -ssRNA viruses. [1] [2]

Disease

RNA viruses are associated with a wide range of disease, including many of the most widely known viral diseases. Notable disease-causing viruses in Orthornavirae include: [22]

Animal viruses in Orthornavirae include orbiviruses, which cause various diseases in ruminants and horses, including Bluetongue virus , African horse sickness virus , Equine encephalosis virus , and epizootic hemorrhagic disease virus . [24] The vesicular stomatitis virus causes disease in cattle, horses, and pigs. [25] Bats harbor many viruses including ebolaviruses and henipaviruses, which also can cause disease in humans. [26] Similarly, arthropod viruses in the Flavivirus and Phlebovirus genera are numerous and often transmitted to humans. [27] [28] Coronaviruses and influenza viruses cause disease in various vertebrates, including bats, birds, and pigs. [29] [30]

Plant viruses in the kingdom are numerous and infect many economically important crops. Tomato spotted wilt virus is estimated to cause more than US$1 billion in damages annually, affecting more than 800 plant species including chrysanthemum, lettuce, peanut, pepper, and tomato. Cucumber mosaic virus infects more than 1,200 plant species and likewise causes significant crop losses. Potato virus Y causes significant reductions in yield and quality for pepper, potato, tobacco, and tomato, and Plum pox virus is the most important virus among stone fruit crops. Brome mosaic virus , while not causing significant economic losses, is found throughout much of the world and primarily infects grasses, including cereals. [22] [31]

History

Diseases caused by RNA viruses in Orthornavirae have been known throughout much of history, but their cause was only discovered in modern times. As a whole, RNA viruses were discovered during a time period of major advancements in molecular biology, including the discovery of mRNA as the immediate carrier of genetic information for protein synthesis. [32] Tobacco mosaic virus was discovered in 1898 and was the first virus to be discovered. [33] Viruses in the kingdom that are transmitted by arthropods have been a key target in the development of vector control, which often aims to prevent viral infections. [34] In modern history, numerous disease outbreaks have been caused by RdRp-encoding RNA viruses, including outbreaks caused by coronaviruses, ebola, and influenza. [35]

Orthornavirae was established in 2019 as a kingdom within the realm Riboviria, intended to accommodate all RdRp-encoding RNA viruses. Prior to 2019, Riboviria was established in 2018 and included only RdRp-encoding RNA viruses. In 2019, Riboviria was expanded to also include reverse transcribing viruses, placed under the kingdom Pararnavirae , so Orthornavirae was established to separate RdRp-encoding RNA viruses from reversing transcribing viruses. [1] [36]

Notes

  1. ↑ The exception is that some members of the order Nidovirales encode proofreading exoribonuclease activity as part of a protein that is distinct from RdRp.
  2. ↑ Excluding deltaviruses, which do not encode RdRp and which therefore are not included in Orthornavirae.

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.

<span class="mw-page-title-main">RNA virus</span> Subclass of viruses

An RNA virus is a virus characterized by a ribonucleic acid (RNA) based genome. The genome can be single-stranded RNA (ssRNA) or double-stranded (dsRNA). Notable human diseases caused by RNA viruses include influenza, SARS, MERS, COVID-19, Dengue virus, hepatitis C, hepatitis E, West Nile fever, Ebola virus disease, rabies, polio, mumps, and measles.

<span class="mw-page-title-main">Reverse transcriptase</span> Enzyme which generates DNA

A reverse transcriptase (RT) is an enzyme used to convert RNA genome to DNA, a process termed reverse transcription. Reverse transcriptases are used by viruses such as HIV and hepatitis B to replicate their genomes, by retrotransposon mobile genetic elements to proliferate within the host genome, and by eukaryotic cells to extend the telomeres at the ends of their linear chromosomes. Contrary to a widely held belief, the process does not violate the flows of genetic information as described by the classical central dogma, as transfers of information from RNA to DNA are explicitly held possible.

Virus classification is the process of naming viruses and placing them into a taxonomic system similar to the classification systems used for cellular organisms.

<span class="mw-page-title-main">Genetic recombination</span> Production of offspring with combinations of traits that differ from those found in either parent

Genetic recombination is the exchange of genetic material between different organisms which leads to production of offspring with combinations of traits that differ from those found in either parent. In eukaryotes, genetic recombination during meiosis can lead to a novel set of genetic information that can be further passed on from parents to offspring. Most recombination occurs naturally and can be classified into two types: (1) interchromosomal recombination, occurring through independent assortment of alleles whose loci are on different but homologous chromosomes ; & (2) intrachromosomal recombination, occurring through crossing over.

<span class="mw-page-title-main">Reassortment</span> Type of nonhereditary genetic change involving swapping of DNA or RNA

Reassortment is the mixing of the genetic material of a species into new combinations in different individuals. Several different processes contribute to reassortment, including assortment of chromosomes, and chromosomal crossover. It is particularly used when two similar viruses that are infecting the same cell exchange genetic material. In particular, reassortment occurs among influenza viruses, whose genomes consist of eight distinct segments of RNA. These segments act like mini-chromosomes, and each time a flu virus is assembled, it requires one copy of each segment.

<i>Geminiviridae</i> Family of viruses

Geminiviridae is a family of plant viruses that encode their genetic information on a circular genome of single-stranded (ss) DNA. There are 520 species in this family, assigned to 14 genera. Diseases associated with this family include: bright yellow mosaic, yellow mosaic, yellow mottle, leaf curling, stunting, streaks, reduced yields. They have single-stranded circular DNA genomes encoding genes that diverge in both directions from a virion strand origin of replication. According to the Baltimore classification they are considered class II viruses. It is the largest known family of single stranded DNA viruses.

<i>Nidovirales</i> Order of positive-sense, single-stranded RNA viruses

Nidovirales is an order of enveloped, positive-strand RNA viruses which infect vertebrates and invertebrates. Host organisms include mammals, birds, reptiles, amphibians, fish, arthropods, molluscs, and helminths. The order includes the families Coronaviridae, Arteriviridae, Roniviridae,Tobaniviridae, and Mesoniviridae.

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">H5N1 genetic structure</span> Genetic structure of Influenza A virus

The genetic structure of H5N1, a highly pathogenic avian influenza virus, is characterized by a segmented RNA genome consisting of eight gene segments that encode for various viral proteins essential for replication, host adaptation, and immune evasion.

<span class="mw-page-title-main">RNA-dependent RNA polymerase</span> Enzyme that synthesizes RNA from an RNA template

RNA-dependent RNA polymerase (RdRp) or RNA replicase is an enzyme that catalyzes the replication of RNA from an RNA template. Specifically, it catalyzes synthesis of the RNA strand complementary to a given RNA template. This is in contrast to typical DNA-dependent RNA polymerases, which all organisms use to catalyze the transcription of RNA from a DNA template.

<span class="mw-page-title-main">Double-stranded RNA viruses</span> Type of virus according to Baltimore classification

Double-stranded RNA viruses are a polyphyletic group of viruses that have double-stranded genomes made of ribonucleic acid. The double-stranded genome is used as a template by the viral RNA-dependent RNA polymerase (RdRp) to transcribe a positive-strand RNA functioning as messenger RNA (mRNA) for the host cell's ribosomes, which translate it into viral proteins. The positive-strand RNA can also be replicated by the RdRp to create a new double-stranded viral genome.

<span class="mw-page-title-main">Viral disease</span> Animal or plant disease resulting from a viral infection

A viral disease occurs when an organism's body is invaded by pathogenic viruses, and infectious virus particles (virions) attach to and enter susceptible cells.

<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. Viruses are found in almost every ecosystem on Earth and are the most numerous type of biological entity. 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 11,000 of the millions of virus species have been described in detail. The study of viruses is known as virology, a subspeciality of microbiology.

Amalgaviridae is a family of double-stranded RNA viruses. Member viruses infect plants and are transmitted vertically via seeds. The name derives from amalgam which refers to amalgaviruses possessing characteristics of both partitiviruses and totiviruses. There are ten species in the family.

<span class="mw-page-title-main">Positive-strand RNA virus</span> Class of viruses in the Baltimore classification

Positive-strand RNA viruses are a group of related viruses that have positive-sense, single-stranded genomes made of ribonucleic acid. The positive-sense genome can act as messenger RNA (mRNA) and can be directly translated into viral proteins by the host cell's ribosomes. Positive-strand RNA viruses encode an RNA-dependent RNA polymerase (RdRp) which is used during replication of the genome to synthesize a negative-sense antigenome that is then used as a template to create a new positive-sense viral genome.

<span class="mw-page-title-main">Negative-strand RNA virus</span> Phylum of viruses

Negative-strand RNA viruses are a group of related viruses that have negative-sense, single-stranded genomes made of ribonucleic acid (RNA). They have genomes that act as complementary strands from which messenger RNA (mRNA) is synthesized by the viral enzyme RNA-dependent RNA polymerase (RdRp). During replication of the viral genome, RdRp synthesizes a positive-sense antigenome that it uses as a template to create genomic negative-sense RNA. Negative-strand RNA viruses also share a number of other characteristics: most contain a viral envelope that surrounds the capsid, which encases the viral genome, −ssRNA virus genomes are usually linear, and it is common for their genome to be segmented.

<i>Riboviria</i> Realm of viruses

Riboviria is a realm of viruses that includes all viruses that use a homologous RNA-dependent polymerase for replication. It includes RNA viruses that encode an RNA-dependent RNA polymerase, as well as reverse-transcribing viruses that encode an RNA-dependent DNA polymerase. RNA-dependent RNA polymerase (RdRp), also called RNA replicase, produces RNA from RNA. RNA-dependent DNA polymerase (RdDp), also called reverse transcriptase (RT), produces DNA from RNA. These enzymes are essential for replicating the viral genome and transcribing viral genes into messenger RNA (mRNA) for translation of viral proteins.

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>Monodnaviria</i> Realm of viruses

Monodnaviria is a realm of viruses that includes all single-stranded DNA viruses that encode an endonuclease of the HUH superfamily that initiates rolling circle replication of the circular viral genome. Viruses descended from such viruses are also included in the realm, including certain linear single-stranded DNA (ssDNA) viruses and circular double-stranded DNA (dsDNA) viruses. These atypical members typically replicate through means other than rolling circle replication.

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