| Riboviria | |
|---|---|
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| Clockwise from top left:TEM ofavian coronavirus,polio virus,bacteriophage Qβ,Ebolavirus,tobacco mosaic virus,Influenza A virus,Rotavirus,HIV-1. Center:homologousRT andRdRps with conserved palm domain. | |
Virus classification | |
| (unranked): | Virus |
| Realm: | Riboviria |
| Kingdoms | |
Riboviria is arealm ofviruses that includes all viruses that use a homologous RNA-dependent polymerase for replication. It includesRNA viruses thatencode anRNA-dependent RNA polymerase, as well asreverse-transcribing viruses (with either RNA or DNA genomes) that encode anRNA-dependent DNA polymerase. RNA-dependent RNA polymerase (RdRp), also called RNA replicase, produces RNA (ribonucleic acid) from RNA. RNA-dependent DNA polymerase (RdDp), also called reverse transcriptase (RT), produces DNA (deoxyribonucleic acid) from RNA. Theseenzymes are essential forreplicating the viral genome andtranscribing viral genes intomessenger RNA (mRNA) fortranslation of viralproteins.
Riboviria was established in 2018 to accommodate all RdRp-encoding RNA viruses and was expanded a year later to also include RdDp-encoding viruses. These two groups of viruses are assigned to two separate kingdoms:Orthornavirae for RdRp-encoding RNA viruses, andPararnavirae for RdDp-encoding viruses, i.e. all reverse-transcribing viruses. Most identifiedeukaryotic viruses belong to the realm, including most human, animal, and plant viruses. Historically, fewprokaryotic RNA viruses had been discovered to be included in the realm, but in the 2020smetagenomic andmetatranscriptomic studies have discovered many prokaryotic RNA viruses.
Many of the most widely known viral diseases are caused by viruses inRiboviria, which includescoronaviruses,ebola virus,HIV,influenza viruses, and therabies virus. These viruses and others in the realm have been prominent throughout history, includingTobacco mosaic virus, which was the first virus to be discovered. Many reverse-transcribing viruses integrate their genome into the genome of their host as part of their replication cycle. As a result of that, it is estimated that about 7–8% of the human genome originates from these viruses.
Riboviria is aportmanteau ofribo, which refers to ribonucleic acid, and the suffix -viria, which is the suffix used for virus realms.[1] Members of the realm are calledribovirians.[2]
All members ofRiboviria contain a gene that encodes for an RNA-dependent polymerase, also called RNA-directed polymerase. There are two types of RNA-dependent polymerases: RNA-dependent RNA polymerase (RdRp), also called RNA replicase, which synthesizes RNA from RNA, and RNA-dependent DNA polymerase (RdDp), also called reverse transcriptase (RT), which synthesizes DNA from RNA.[3] For viruses inRiboviria, in a typical virus particle, called a virion, the RNA-dependent polymerase is bound to the viral genome in some manner and begins transcription of the viral genome afterentering a cell. As part of avirus's life cycle, the RNA-dependent polymerase also synthesizes copies of the viral genome as part of the process of creating new viruses.
Riboviria contains three types of viruses that replicate via RdRp: single-stranded RNA (ssRNA) viruses, which are either positive (+) or negative (-)sense, and double-stranded RNA viruses (dsRNA), all of which belong to the kingdomOrthornavirae. +ssRNA viruses have genomes that can functionally act as mRNA, and a negative-sense strand can also be created to form dsRNA from which mRNA is transcribed from the negative strand.[4] The negative-sense strands of the genomes of -ssRNA viruses and dsRNA viruses act as templates from which RdRp creates mRNA.[5][6]
There are two types of viruses inRiboviria that replicate via reverse transcription: single-stranded RNA (ssRNA-RT) viruses, all of which belong to the orderOrtervirales, and double-stranded DNA (dsDNA-RT) viruses, which belong to the familyCaulimoviridae, also inOrtervirales, and the familyHepadnaviridae of the orderBlubervirales. Reverse-transcribing viruses all belong to the kingdomPararnavirae. ssRNA-RT viruses have their positive-sense genome transcribed by RdDp to synthesize a negative-sense complementary DNA (-cDNA) strand. The +RNA strand is degraded and later replaced by RdDp with a +DNA strand to synthesize a linear dsDNA copy of the viral genome. This genome is thenintegrated into the host cell's DNA.[7]
For dsDNA-RT viruses, a pregenomic +RNA strand is transcribed from the relaxed circular DNA (rcDNA), which is in turn used by RdDp to transcribe a -cDNA strand. The +RNA strand is degraded and replaced in a similar manner as +ssRNA-RT viruses to synthesize rcDNA. The rcDNA genome is later repaired by the host cell's DNA repair mechanisms to synthesize a covalently closed circular DNA (cccDNA) genome.[8] The integrated genome of +ssRNA-RT viruses and the cccDNA of dsDNA-RT viruses are then transcribed into mRNA by the host cell enzymeRNA polymerase II.[7][8]
Viral mRNA istranslated by the host cell'sribosomes to produce viral proteins. In order to produce more viruses, viral RNA-dependent polymerases use copies of the viral genome as templates to replicate the viral genome. For +ssRNA viruses, an intermediate dsRNA genome is created from which +ssRNA is synthesized from the negative strand.[4] For -ssRNA viruses, genomes are synthesized from complementary positive-sense strands.[6] dsRNA viruses replicate their genomes from mRNA by synthesizing a complementary negative-sense strand to form genomic dsRNA.[5] For dsDNA-RT viruses, pregenomic RNA created from the cccDNA is retrotranscribed into new dsDNA genomes.[8] For +ssRNA-RT viruses, the genome is replicated from the integrated genome.[7] After replication and translation, the genome and viral proteins are assembled into complete virions, which thenleave the host cell.
Viruses ofAmbiviricota have ambisense, circular ssRNA genomes. Their genomes contain at least twoopen reading frames (ORFs) andribozymes in opposite sense orientations of the genome—one positive-sense portion of the genome and one negative-sense portion of the genome. For that reason, they are not considered positive-sense or negative-sense but ambisense. Ambiviricots encode RdRp, but unlike other viruses ofOrthornavirae, they replicate their genome viarolling circle replication, a form of replication used for circular genomes.[9][10] Apart from ambiviricots, some other ssRNA viruses are ambisense because they contain ORFs on both sense strands, includinginfluenza viruses andcoronaviruses, but these viruses replicate in the manners typical of -ssRNA and +ssRNA viruses, respectively, so they are still considered -ssRNA and +ssRNA viruses.[11]
Phylogenetic analysis of RNA polymerases is used to study the evolutionary history ofRiboviria because it is the only gene preserved among all ribovirians.[2] The reverse transcriptases of kingdomPararnavirae show a relation to the RTs ofgroup II introns that encode RTs and non-long terminal repeat (LTR)retrotransposons, which are self-replicating DNA sequences.[3][12] More specifically, the two orders of the kingdom,Blubervirales andOrtervirales, appear to have evolved from two different retrotransposon families on two separate occasions by acquiring host proteins and using them for virion formation.[2] The origin ofOrthornavirae is less clear and different hypotheses exist. In the first hypothesis, viruses ofOrthornavirae also originate from retroelements such as group II introns and non-LTR retrotransposons.[12][13] In the second hypothesis, both retroelements and the viral RdRp are descended from a capsidless RNA replicon that was present in theRNA world.[14][15]
The unclassified phylumTaraviricota may be such capsidless RNA ancestors as it appears to be the basal lineage from which allOrthornavirae phyla are descended from.[13][16] The phylumArtimaviricota, so-called "hot spring riboviruses", encode an RdRp that is very distantly related to the RdRp ofOrthornavirae and which, based on analysis of its structure, may be an intermediate between RdRps and RTs.[2][17]
Ribovirians generally have no relation to viral agents outside the realm, with a few exceptions. Viruses of the kingdomShotokuvirae in the realmMonodnaviria appear to have come into existence on multiple, independent occasions. These monodnavirians originate from multiplerecombination events in which bacterial and archaealplasmids merged withcomplementary DNA copies of positive-sense RNA viruses, which enabled these plasmids to obtain capsid proteins needed to form virions.[18] Additionally, the ribovirian phylumAmbiviricota appears to have a chimeric origin in which a ribovirian and a ribozyme-containingviroid orribozyvirian recombined to form a new lineage.[2][10]
Riboviria contains two kingdoms:Orthornavirae andPararnavirae, the latter of which is monotypic down to the rank of class. This taxonomy can be visualized hereafter.[19]
Additionally,Riboviria contains oneincertae sedis order and twoincertae sedis families that are unassigned to higher taxa. Additional information about them is needed to know their exact placement in higher taxa. Theincertae sedis order isTombendovirales, and the twoincertae sedis families arePolymycoviridae andTonesaviridae.[3][19]
Riboviria partially mergesBaltimore classification with virus taxonomy as it includes the Baltimore groups for RNA viruses and reverse-transcribing viruses in the realm. Baltimore classification is a system used to classify viruses based on their manner of mRNA production. It is often used alongside standard virus taxonomy, which is based on evolutionary history. All members of five Baltimore groups belong toRiboviria: Group III: dsRNA viruses, Group IV: +ssRNA viruses, Group V: -ssRNA viruses, Group VI: ssRNA-RT viruses, and Group VII: dsDNA-RT viruses. Realms are the highest level of taxonomy used for viruses andRiboviria is one of seven. The others areAdnaviria,Duplodnaviria,Monodnaviria,Ribozyviria,Singelaviria, andVaridnaviria.[12][19][20]
Ribovirians are associated with a wide range of diseases, including many of the most widely known viral diseases. Widely-known ribovirians include:
Animal viruses inRiboviria includeorbiviruses, which cause various diseases in ruminants and horses, includingBluetongue virus,African horse sickness virus,Equine encephalosis virus, andepizootic hemorrhagic disease virus.[45] Thevesicular stomatitis virus causes disease in cattle, horses, and pigs.[46] Bats harbor many viruses includingebolaviruses andhenipaviruses, which also can cause disease in humans.[47] Similarly, arthropod viruses in theFlavivirus andPhlebovirus genera are numerous and often transmitted to humans.[48][49] Coronaviruses and influenza viruses cause disease in various vertebrates, including bats, birds, and pigs.[50][51] The familyRetroviridae contains many viruses that causeleukemia,immunodeficiency, and other cancers and immune system-related diseases in animals.[52][53]
Plant viruses in the realm are numerous and infect many economically important crops.Tomato spotted wilt virus is estimated to cause more than US$1 billion in damages annually, and it infects 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, andPlum pox virus is the most important virus among stone fruit crops.Brome mosaic virus is found throughout much of the world and primarily infects grasses, including cereals, though it does not cause significant economic losses.[19][54]
Many reverse-transcribing viruses inRiboviria integrate their genome into the DNA of their host by means of the retroviral enzyme integrase. This endogenization is part of their replication cycle, as mRNA is produced from the integrated DNA. Endogenization is a form ofhorizontal gene transfer between unrelated organisms, and it is estimated that about 7–8% of the human genome consists of retroviral DNA. Endogenization can be used to study the evolutionary history of viruses as it shows an approximate time period when a virus first became endogenized into the host's genome as well as the rate of evolution for the viruses since endogenization first occurred.[55]
Diseases caused by viruses inRiboviria have been known for much of recorded history, though their cause was only discovered in modern times. Tobacco mosaic virus was discovered in 1898 and was the first virus to be discovered.[56] Viruses transmitted by arthropods have been central in the development ofvector control, which often aims to prevent viral infections.[57] In modern history, numerous disease outbreaks have been caused by various members of the realm, including coronaviruses, ebola, and influenza.[58] HIV especially has had dramatic effects on society as it causes a sharp decline in life expectancy and significant stigma for infected persons.[59][60]
For a long time, the relation between many viruses inRiboviria could not be established due to the high amount of genetic divergence among RNA viruses. With the development of viralmetagenomics, many additional RNA viruses were identified, helping to fill in the gaps of their relations.[12] This led to the establishment ofRiboviria in 2018 to accommodate all RdRp-encoding RNA viruses based on phylogenetic analysis that they were related.[1] A year later, all reverse-transcribing viruses were added to the realm. The kingdoms were also established in 2019, separating the two RNA-dependent polymerase branches.[3] When the realm was founded, it mistakenly included twoviroid families,Avsunviroidae andPospiviroidae, and the genusDeltavirus, which were removed in 2019 because they use host cell enzymes for replication and not RdRp or RdDp.[61]
Traditionally,Riboviria mainly included eukaryotic viruses with few prokaryotic viruses.[17] Metagenomic and metatranscriptomic research in the 2020s however have discovered many viruses, including many bacterial RNA viruses.[13][62] These discoveries have mainly occurred in marine environments, where many novel lineages of microbial eukaryotic and prokaryotic RNA viruses have been discovered.[16] Leviviruses, a group of bacterial RNA viruses that previously constituted the familyLeviviridae, were promoted to the rank of class,Leviviricetes, due to the large number of leviviruses discovered.[17] Numerous novel phyla ofOrthornavirae were discovered in the 2020s, including the possibly basal lineageTaraviricota.[13][63] The ecological role of these novel marine viruses is relatively unexplored, but they may be involved in the recycling of nutrients in a process calledviral shunt.[16]
