Positive-strand RNA virus

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Positive-strand RNA virus
HCV EM picture 2.png
Hepatitis C virus
Virus classification
Group:
Group IV ((+)ssRNA)
Kingdom: Phylum: Class
Synonyms
  • Positive-sense RNA virus

Positive-strand RNA viruses (+ssRNA 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.

Contents

Positive-strand RNA viruses are divided between the phyla Kitrinoviricota , Lenarviricota , and Pisuviricota (specifically classes Pisoniviricetes and Stelpavirictes ) all of which are in the kingdom Orthornavirae and realm Riboviria . [1] They are monophyletic and descended from a common RNA virus ancestor. In the Baltimore classification system, +ssRNA viruses belong to Group IV. [2]

Positive-sense RNA viruses include pathogens such as the Hepatitis C virus, West Nile virus, dengue virus, and the MERS, SARS, and SARS-CoV-2 coronaviruses, [3] as well as less clinically serious pathogens such as the coronaviruses and rhinoviruses that cause the common cold. [4] [5] [6]

Genome

Positive-strand RNA virus genomes usually contain relatively few genes, usually between three and ten, including an RNA-dependent RNA polymerase. [4] Coronaviruses have the largest known RNA genomes, between 27 and 32 kilobases in length, and likely possess replication proofreading mechanisms in the form of an exoribonuclease within nonstructural protein nsp14. [7]

Replication

Life cycle of Japanese encephalitis virus a +ssRNA virus: attachment, endocytosis, membrane fusion, uncoating, translation, RNA replication, assembly, maturation, and release. Pathogens-07-00068-g002.webp
Life cycle of Japanese encephalitis virus a +ssRNA virus: attachment, endocytosis, membrane fusion, uncoating, translation, RNA replication, assembly, maturation, and release.

Positive-strand RNA viruses have genetic material that can function both as a genome and as messenger RNA; it can be directly translated into protein in the host cell by host ribosomes. [8] The first proteins to be expressed after infection serve genome replication functions; they recruit the positive-strand viral genome to viral replication complexes formed in association with intracellular membranes. These complexes contain proteins of both viral and host cell origin, and may be associated with the membranes of a variety of organelles—often the rough endoplasmic reticulum, [9] but also including membranes derived from mitochondria, vacuoles, the Golgi apparatus, chloroplasts, peroxisomes, plasma membranes, autophagosomal membranes, and novel cytoplasmic compartments. [4]

The replication of the positive-sense RNA genome proceeds through double-stranded RNA intermediates, and the purpose of replication in these membranous invaginations may be the avoidance of cellular response to the presence of dsRNA. In many cases subgenomic RNAs are also created during replication. [8] After infection, the entirety of the host cell's translation machinery may be diverted to the production of viral proteins as a result of the very high affinity for ribosomes by the viral genome's internal ribosome entry site (IRES) elements; in some viruses, such as poliovirus and rhinoviruses, normal protein synthesis is further disrupted by viral proteases degrading components required to initiate translation of cellular mRNA. [6]

All positive-strand RNA virus genomes encode RNA-dependent RNA polymerase, a viral protein that synthesizes RNA from an RNA template. Host cell proteins recruited by +ssRNA viruses during replication include RNA-binding proteins, chaperone proteins, and membrane remodeling and lipid synthesis proteins, which collectively participate in exploiting the cell's secretory pathway for viral replication. [4]

Recombination

Mechanisms of replicative and nonreplicative RNA recombination. Viruses-11-00859-g004.png
Mechanisms of replicative and nonreplicative RNA recombination.

Numerous positive-strand RNA viruses can undergo genetic recombination when at least two viral genomes are present in the same host cell. [10] The capability for recombination among +ssRNA virus pathogens of humans is common. RNA recombination appears to be a major driving force in determining genome architecture and the course of viral evolution among Picornaviridae (e.g. poliovirus). [11] In the Retroviridae (e.g. HIV), genome damage appears to be avoided during reverse transcription by strand switching, a form of recombination. [12] [13] [14] Recombination occurs in the Coronaviridae (e.g. SARS). [15] Recombination in RNA viruses appears to be an adaptation for coping with genome damage. [10] Recombination can also occur infrequently between +ssRNA viruses of the same species but of divergent lineages. The resulting recombinant viruses may sometimes cause an outbreak of infection in humans, as in the case of SARS and MERS. [15]

Positive-strand RNA viruses are common in plants. In tombusviruses and carmoviruses, RNA recombination occurs frequently during replication. [16] The ability of the RNA-dependent RNA polymerase of these viruses to switch RNA templates suggests a copy choice model of RNA recombination that may be an adaptive mechanism for coping with damage in the viral genome. [16] Other +ssRNA viruses of plants have also been reported to be capable of recombination, such as Brom mosaic bromovirus [17] and Sindbis virus. [18]

Classification

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).

Positive-strand RNA viruses are found in three phyla: Kitrinoviricota, Lenarviricota, and Pisuviricota, each of which are assigned to the kingdom Orthornavirae in the realm Riboviria . In the Baltimore classification system, which groups viruses together based on their manner of mRNA synthesis, +ssRNA viruses are group IV.[ citation needed ]

Kitrinoviricota

The first +ssRNA phylum is Kitrinoviricota . The phylum contains what have been referred to as the "alphavirus supergroup" and "flavivirus supergroup" along with various other short-genome viruses. Four classes in the phylum are recognized: Alsuviricetes , the alphavirus supergroup, which contains a large number of plant viruses and arthropod viruses; Flasuviricetes, which contains flaviviruses, Magsaviricetes , which contains nodaviruses and sinhaliviruses; and Tolucaviricetes , which primarily contains plant viruses. [19] [20]

Lenarviricota

Lenarviricota is the second +ssRNA phylum. It contains the class Leviviricetes , which infect prokaryotes, and the apparent descendants of leviviruses, which infect eukaryotes. The phylum is divided into four classes: Leviviricetes, which contains leviviruses and their relatives, Amabiliviricetes, which contains narnaviruses and their relatives, Howeltoviricetes, which contains mitoviruses and their relatives, and Miaviricetes, which contains botourmiaviruses and their relatives. Based on phylogenetic analysis of RdRp, all other RNA viruses are considered to comprise a sister clade in relation to Lenarviricota. [19] [20]

Pisuviricota

False-color Transmission electron micrograph of a SARS-CoV-2 virion. Coronaviruses like SARS-CoV-2 fall in the phylum Pisuviricota. Novel Coronavirus SARS-CoV-2 (50960620707) (cropped).jpg
False-color Transmission electron micrograph of a SARS-CoV-2 virion. Coronaviruses like SARS-CoV-2 fall in the phylum Pisuviricota .

The third phylum that contains +ssRNA viruses is Pisuviricota , which has been informally called the "picornavirus supergroup". The phylum contains a large assemblage of eukaryotic viruses known to infect animals, plants, fungi, and protists. The phylum contains three classes, two of which contain only +ssRNA viruses: Pisoniviricetes , which contains nidoviruses, picornaviruses, and sobeliviruses, and Stelpaviricetes , which contains potyviruses and astroviruses. The third class is Duplopiviricetes , whose members are double-stranded RNA viruses that are descended from +ssRNA viruses. [19] [20]

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.

<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.

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

<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.

<span class="mw-page-title-main">SARS-related coronavirus</span> Species of coronavirus causing SARS and COVID-19

Betacoronavirus pandemicum is a species of virus consisting of many known strains. Two strains of the virus have caused outbreaks of severe respiratory diseases in humans: severe acute respiratory syndrome coronavirus 1, the cause of the 2002–2004 outbreak of severe acute respiratory syndrome (SARS), and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the cause of the pandemic of COVID-19. There are hundreds of other strains of SARSr-CoV, which are only known to infect non-human mammal species: bats are a major reservoir of many strains of SARSr-CoV; several strains have been identified in Himalayan palm civets, which were likely ancestors of SARS-CoV-1.

<span class="mw-page-title-main">Picornavirus</span> Family of viruses

Picornaviruses are a group of related nonenveloped RNA viruses which infect vertebrates including fish, mammals, and birds. They are viruses that represent a large family of small, positive-sense, single-stranded RNA viruses with a 30 nm icosahedral capsid. The viruses in this family can cause a range of diseases including the common cold, poliomyelitis, meningitis, hepatitis, and paralysis.

<i>Bunyavirales</i> Order of RNA viruses

Bunyavirales is an order of segmented negative-strand RNA viruses with mainly tripartite genomes. Member viruses infect arthropods, plants, protozoans, and vertebrates. It is the only order in the class Ellioviricetes. The name Bunyavirales derives from Bunyamwera, where the original type species Bunyamwera orthobunyavirus was first discovered. Ellioviricetes is named in honor of late virologist Richard M. Elliott for his early work on bunyaviruses.

<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.

<span class="mw-page-title-main">Viral replication</span> Formation of biological viruses during the infection process

Viral replication is the formation of biological viruses during the infection process in the target host cells. Viruses must first get into the cell before viral replication can occur. Through the generation of abundant copies of its genome and packaging these copies, the virus continues infecting new hosts. Replication between viruses is greatly varied and depends on the type of genes involved in them. Most DNA viruses assemble in the nucleus while most RNA viruses develop solely in cytoplasm.

<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.

<i>Murine leukemia virus</i> Species of virus

The murine leukemia viruses are retroviruses named for their ability to cause cancer in murine (mouse) hosts. Some MLVs may infect other vertebrates. MLVs include both exogenous and endogenous viruses. Replicating MLVs have a positive sense, single-stranded RNA (ssRNA) genome that replicates through a DNA intermediate via the process of reverse transcription.

<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.

<i>Cowpea chlorotic mottle virus</i> Species of virus

Cowpea chlorotic mottle virus, known by the abbreviation CCMV, is a virus that specifically infects the cowpea plant, or black-eyed pea. The leaves of infected plants develop yellow spots, hence the name "chlorotic". Similar to its "brother" virus, Cowpea mosaic virus (CPMV), CCMV is produced in high yield in plants. In the natural host, viral particles can be produced at 1–2 mg per gram of infected leaf tissue. Belonging to the bromovirus genus, cowpea chlorotic mottle virus (CCMV) is a small spherical plant virus. Other members of this genus include the brome mosaic virus (BMV) and the broad bean mottle virus (BBMV).

<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">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.

<i>Orthornavirae</i> Kingdom of 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.

References

  1. "Current ICTV Taxonomy Release | ICTV". ictv.global. Retrieved 3 April 2023.
  2. Baltimore D (September 1971). "Expression of animal virus genomes". Bacteriological Reviews. 35 (3): 235–41. doi:10.1128/MMBR.35.3.235-241.1971. PMC   378387 . PMID   4329869.
  3. Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, Wang W, Song H, Huang B, Zhu N, Bi Y, Ma X, Zhan F, Wang L, Hu T, Zhou H, Hu Z, Zhou W, Zhao L, Chen J, Meng Y, Wang J, Lin Y, Yuan J, Xie Z, Ma J, Liu WJ, Wang D, Xu W, Holmes EC, Gao GF, Wu G, Chen W, Shi W, Tan W (February 2020). "Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding". Lancet. 395 (10224): 565–574. doi: 10.1016/S0140-6736(20)30251-8 . PMC   7159086 . PMID   32007145.
  4. 1 2 3 4 Nagy PD, Pogany J (December 2011). "The dependence of viral RNA replication on co-opted host factors". Nature Reviews. Microbiology. 10 (2): 137–149. doi:10.1038/nrmicro2692. PMC   7097227 . PMID   22183253.
  5. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT (August 2003). "Host factors in positive-strand RNA virus genome replication". Journal of Virology. 77 (15): 8181–8186. doi:10.1128/JVI.77.15.8181-8186.2003. PMC   165243 . PMID   12857886.
  6. 1 2 Modrow S, Falke D, Truyen U, Schätzl H (2013). "Viruses with Single-Stranded, Positive-Sense RNA Genomes". Molecular Virology. Berlin, Heidelberg: Springer. pp. 185–349. doi:10.1007/978-3-642-20718-1_14. ISBN   978-3-642-20718-1. S2CID   82608215.
  7. Smith EC, Denison MR (5 December 2013). "Coronaviruses as DNA wannabes: a new model for the regulation of RNA virus replication fidelity". PLOS Pathogens. 9 (12): e1003760. doi: 10.1371/journal.ppat.1003760 . PMC   3857799 . PMID   24348241.
  8. 1 2 "Positive stranded RNA virus replication". ViralZone. Retrieved 8 September 2016.
  9. Andronov L, Han M, Zhu Y, Balaji A, Roy AR, Barentine AE, Patel P, Garhyan J, Qi LS, Moerner WE (May 2024). "Nanoscale cellular organization of viral RNA and proteins in SARS-CoV-2 replication organelles". Nature Communications. 15 (1): 4644. Bibcode:2024NatCo..15.4644A. doi:10.1038/s41467-024-48991-x. PMC   11143195 . PMID   38821943.
  10. 1 2 Barr JN, Fearns R (June 2010). "How RNA viruses maintain their genome integrity". The Journal of General Virology. 91 (Pt 6): 1373–87. doi: 10.1099/vir.0.020818-0 . PMID   20335491.
  11. Muslin C, Mac Kain A, Bessaud M, Blondel B, Delpeyroux F (September 2019). "Recombination in Enteroviruses, a Multi-Step Modular Evolutionary Process". Viruses. 11 (9): 859. doi: 10.3390/v11090859 . PMC   6784155 . PMID   31540135.
  12. Hu WS, Temin HM (November 1990). "Retroviral recombination and reverse transcription". Science. 250 (4985): 1227–33. Bibcode:1990Sci...250.1227H. doi:10.1126/science.1700865. PMID   1700865.
  13. Rawson JM, Nikolaitchik OA, Keele BF, Pathak VK, Hu WS (November 2018). "Recombination is required for efficient HIV-1 replication and the maintenance of viral genome integrity". Nucleic Acids Research. 46 (20): 10535–10545. doi:10.1093/nar/gky910. PMC   6237782 . PMID   30307534.
  14. Bernstein H, Bernstein C, Michod RE (January 2018). "Sex in microbial pathogens". Infection, Genetics and Evolution. 57: 8–25. Bibcode:2018InfGE..57....8B. doi: 10.1016/j.meegid.2017.10.024 . PMID   29111273.
  15. 1 2 Su S, Wong G, Shi W, Liu J, Lai AC, Zhou J, et al. (June 2016). "Epidemiology, Genetic Recombination, and Pathogenesis of Coronaviruses". Trends in Microbiology. 24 (6): 490–502. doi: 10.1016/j.tim.2016.03.003 . PMC   7125511 . PMID   27012512.
  16. 1 2 Cheng CP, Nagy PD (November 2003). "Mechanism of RNA recombination in carmo- and tombusviruses: evidence for template switching by the RNA-dependent RNA polymerase in vitro". Journal of Virology. 77 (22): 12033–47. doi:10.1128/jvi.77.22.12033-12047.2003. PMC   254248 . PMID   14581540.
  17. Kolondam B, Rao P, Sztuba-Solinska J, Weber PH, Dzianott A, Johns MA, Bujarski JJ (2015). "Co-infection with two strains of Brome mosaic bromovirus reveals common RNA recombination sites in different hosts". Virus Evolution. 1 (1): vev021. doi:10.1093/ve/vev021. PMC   5014487 . PMID   27774290.
  18. Weiss BG, Schlesinger S (August 1991). "Recombination between Sindbis virus RNAs". Journal of Virology. 65 (8): 4017–25. doi:10.1128/JVI.65.8.4017-4025.1991. PMC   248832 . PMID   2072444.
  19. 1 2 3 Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini M, Kuhn JH (18 October 2019). "Create a megataxonomic framework, filling all principal taxonomic ranks, for realm Riboviria" (docx). International Committee on Taxonomy of Viruses (ICTV). Retrieved 14 August 2020.
  20. 1 2 3 Wolf YI, Kazlauskas D, Iranzo J, Lucia-Sanz A, Kuhn JH, Krupovic M, Dolja VV, Koonin EV (27 November 2018). "Origins and Evolution of the Global RNA Virome". mBio. 9 (6): e02329-18. doi:10.1128/mBio.02329-18. PMC   6282212 . PMID   30482837.