Bunyavirales

Bunyavirales is an order of negative-sense single-stranded RNA viruses. It is the only order in the class Ellioviricetes.[2] It was formerly known as Bunyaviridae family of viruses. The name Bunyavirales derives from Bunyamwera,[3] where the original type species Bunyamwera orthobunyavirus was first discovered.[4] Ellioviricetes is named in honor of late virologist Richard M. Elliott for his early work on bunyaviruses.[5]

Bunyavirales
Isolated male diagnosed with Crimean-Congo hemorrhagic fever
Virus classification
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Negarnaviricota
Subphylum: Polyploviricotina
Class: Ellioviricetes
Order: Bunyavirales
Families[1]

In 2017, the ICTV reclassified the family Bunyaviridae as Bunyavirales, a taxonomic shift from a family of viruses to an order of viruses.[6][7] The body made these decisions in a 2016 convening in Budapest.[7] Primary reasons for this alteration revolve around these observations: approximately half of viruses in the former Bunyaviridae were at the time unassigned to a genus; novel viruses discovered that were characteristic of and clustered around Bunyaviridae based on phylogenetic analyses had bi-segmented genomes (as opposed to Bunyaviridae's tri-segmentation); and plant viruses also lacking tri-segmentation were previously known to be "bunya-like" yet were not properly assigned to the family Bunyaviridae based upon the past taxonomic classifications. All five genera formerly in the family Bunyaviridae (Hantavirus, Nairovirus, Orthobunyavirus, Phlebovirus, Tospovirus) are now novel viral families, some of which have been combined. These new families include: Hantaviridae, Feraviridae, Fimoviridae, Jonviridae, Nairoviridae, Peribunyaviridae, Phasmaviridae, Phenuiviridae, and Tospoviridae.

This order of viruses belong to the fifth group of the Baltimore classification, the so-called negative-sense single-stranded ribonucleic acid (−)ssRNA. They have enveloped RNA viruses. Though generally found in arthropods or rodents, certain viruses in this order occasionally infect humans. Some of them also infect plants.[8]

A majority of bunyaviruses are vector-borne. With the exception of Hantaviruses and Arenaviruses, all viruses in the Bunyavirales order are transmitted by arthropods (mosquitos, tick, or sandfly). Hantaviruses are transmitted through contact with deer mice feces. Incidence of infection is closely linked to vector activity, for example, mosquito-borne viruses are more common in the summer.[8]

Human infections with certain members of Bunyavirales, such as Crimean-Congo hemorrhagic fever orthonairovirus, are associated with high levels of morbidity and mortality, consequently handling of these viruses must occur with a Biosafety level 4 laboratory. They are also the cause of severe fever with thrombocytopenia syndrome.[9]

Hantavirus is another medically-important member of the family Hantaviridae. It is found worldwide, and relatively common in Korea, broader Scandinavia (including Finland), Russia, western North America and parts of South America. It is associated with high fever, lung edema and pulmonary failure. The mortality rate varies significantly depending on the form, being up to 50% in New World hantaviruses (the Americas), up to 15% in Old World hantaviruses (Asia and Europe), and as little as 0.1% in Puumala virus (mostly broader Scandinavia).[10] The antibody reaction plays an important role in decreasing levels of viremia.

Virology

Classification

There are currently 383 virus species recognised in this order, organized into the following 12 families:

Plants can host bunyaviruses from the Tospoviridae and Fimoviridae families (tomato, pigeonpea, melon, wheat, raspberry, redbud, rose).

Members of some families appear to be insect-specific, e.g. the phasmavirids, first isolated from phantom midges,[11] and since identified in diverse insects including moths, wasps and bees, and other true flies.

Structure

Bunyavirus morphology is somewhat similar to that of the Paramyxoviridae family; Bunyavirales form enveloped, spherical virions with diameters of 90–100 nm. These viruses contain no matrix proteins.

Genome

Bunyaviridae have tripartite genomes consisting of a large (L), medium (M), and small (S) RNA segment. These RNA segments are single-stranded, and exist in a helical formation within the virion. Besides, they exhibit a pseudo-circular structure due to each segment's complementary ends. The L segment encodes the RNA Dependent RNA-polymerase, necessary for viral RNA replication and mRNA synthesis. The M segment encodes the viral glycoproteins, which project from the viral surface and aid the virus in attaching to and entering the host cell. The S segment encodes the nucleocapsid protein (N).[12]

Most of the Bunyaviridae have negative sense L and M segment. The S segment of the genus Phlebovirus,[13] and both M and S segment of the genus Tospovirus are ambisense.[14] Ambisense means that some of the genes on the RNA strand are negative sense and others are positive sense. The ambisense S segment codes for the viral nucleoprotein (N) in the negative sense and a nonstructural protein (NSs) in the positive sense. The ambisense M segment codes for glycoprotein (GP) in the negative sense and a nonstructural protein (NSm) in the positive sense.[14]

Total genome size ranges from 10.5 to 22.7 kbp.[15]

Replication

This ambisense arrangement requires two rounds of transcription to be carried out. First, the negative-sense RNA is transcribed to produce mRNA and a full-length replicative intermediate. From this intermediate, a subgenomic mRNA encoding the small segment nonstructural protein is produced while the polymerase produced following the first round of transcription can now replicate the full-length RNA to produce viral genomes.

Bunyavirus RNA replicates in the cytoplasm, while the viral proteins transit through the ER and Golgi apparatus. Mature virions bud from the Golgi apparatus into vesicles which are transported to the cell surface.

Diseases in humans

Bunyaviruses that cause disease in humans include:

Bunyaviruses have segmented genomes, making them capable of rapid recombination and increasing the risk of outbreak.[16] The bunyavirus that causes severe fever with thrombocytopenia syndrome can undergo recombination both by reassortment of genome segments and by intragenic homologous recombination.[17][18] Bunyaviridae are transmitted by hematophagous arthropods including mosquitoes, midges, flies, and ticks. The viral incubation period is about 48 hours. Symptomatic infection typically causes non-specific flu-like symptoms with fever lasting for about three days. Because of their non-specific symptoms, Bunyavirus infections are frequently mistaken for other illnesses. For example, Bwamba fever is often mistaken for malaria.[19]

Prevention

Prevention depends on the reservoir, amplifying hosts and how the viruses are transmitted, i.e. the vector, whether ticks or mosquitoes and which animals are involved.

Preventive measures include general hygiene, limiting contact with vector saliva, urine, feces, or bedding.

There is no licensed vaccine for bunyaviruses.

As precautions Cache Valley virus and Hantavirus research should be conducted in BSL-2 (or higher), Rift Valley Fever virus research is conducted in BSL-3 (or higher), Congo-Crimean Hemorrhagic Fever virus research be conducted in BSL-4 laboratories, per CDC.

Timeline

1940s: Crimean–Congo hemorrhagic fever is discovered in Russia

1951: 3,000 cases of Hantavirus were reported in South Korea in 1951, a time when UN forces were fighting on the 38th parallel during the Korean War

1956: Cache Valley virus isolated in Culiseta inornata mosquitoes in Utah

1960: La Crosse virus was first recognized in a fatal case of encephalitis in La Crosse, Wisconsin

1977: Rift Valley Fever virus caused approximately 200,000 cases and 598 deaths in Egypt

2017: Bunyavirales order is created

References
  1. "Virus Taxonomy: 2018 Release" (html). International Committee on Taxonomy of Viruses (ICTV). October 2018. Retrieved 30 January 2019.
  2. Virus Taxonomy: 2018 Release, International Committee on Taxonomy of Viruses, retrieved 2018-12-02
  3. "ICTV 9th Report (2011) Bunyaviridae" (html). International Committee on Taxonomy of Viruses (ICTV). Retrieved 31 January 2019. Bunya: from Bunyamwera, place in Uganda, where type virus was isolated.
  4. Smithburn, K. C.; Haddow, A. J.; Mahaffy, A. F. (March 1946). "A Neurotropic Virus Isolated from Aedes Mosquitoes Caught in the Semliki Forest". The American Journal of Tropical Medicine and Hygiene. s1-26 (2): 189–208. doi:10.4269/ajtmh.1946.s1-26.189. ISSN 1476-1645. OCLC 677158400. PMID 21020339.
  5. Wolf, Yuri; Krupovic, Mart; Zhang, Yong Zhen; Maes, Piet; Dolja, Valerian; Koonin, Eugene V.; Kuhn, Jens H. "Megataxonomy of negative-sense RNA viruses" (docx). International Committee on Taxonomy of Viruses (ICTV). Retrieved 12 January 2019.
  6. Adams, Michael J.; Lefkowitz, Elliot J.; King, Andrew M. Q.; Harrach, Balázs; Harrison, Robert L.; Knowles, Nick J.; Kropinski, Andrew M.; Krupovic, Mart; Kuhn, Jens H. (2017-08-01). "Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017)". Archives of Virology. 162 (8): 2505–2538. doi:10.1007/s00705-017-3358-5. ISSN 0304-8608. PMID 28434098.
  7. "Taxonomy". International Committee on Taxonomy of Viruses (ICTV). Retrieved 2017-09-29.
  8. Plyusnin, A; Elliott, RM, eds. (2011). Bunyaviridae: Molecular and Cellular Biology. Caister Academic Press. ISBN 978-1-904455-90-5.
  9. Yu XJ, Liang MF, Zhang SY, et al. (April 2011). "Fever with thrombocytopenia associated with a novel bunyavirus in China". N. Engl. J. Med. 364 (16): 1523–32. doi:10.1056/NEJMoa1010095. PMC 3113718. PMID 21410387.
  10. Walter Muranyi; Udo Bahr; Martin Zeier; Fokko J. van der Woude (2005). "Hantavirus Infection". Journal of the American Society of Nephrology. 16 (12): 3669–3679. doi:10.1681/ASN.2005050561. PMID 16267154.
  11. Ballinger, MJ; Bruenn, JA; Hay, J; Czechowski, D; Taylor, DJ (2014). "Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes". J Virol. 88 (16): 8783–94. doi:10.1128/JVI.00531-14. PMC 4136290. PMID 24850747.
  12. Ariza, A.; Tanner, S. J.; Walter, C. T.; Dent, K. C.; Shepherd, D. A.; Wu, W.; Matthews, S. V.; Hiscox, J. A.; Green, T. J. (2013-06-01). "Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization". Nucleic Acids Research. 41 (11): 5912–5926. doi:10.1093/nar/gkt268. ISSN 0305-1048. PMC 3675483. PMID 23595147.
  13. Elliott, Richard M; Brennan, Benjamin (April 2014). "Emerging phleboviruses". Current Opinion in Virology. 5 (100): 50–57. doi:10.1016/j.coviro.2014.01.011. PMC 4031632. PMID 24607799.
  14. Lima, R. N.; De Oliveira, A. S.; Leastro, M. O.; Blawid, R.; Nagata, T.; Resende, R. O.; Melo, F. L. (7 July 2016). "The complete genome of the tospovirus Zucchini lethal chlorosis virus". Virology Journal. 13 (1): 123. doi:10.1186/s12985-016-0577-4. PMC 4936248. PMID 27388209.
  15. "00.011. Bunyaviridae". ICTVdB—The Universal Virus Database, version 4. 2006. Retrieved 2009-01-01.
  16. Horne, Kate McElroy; Vanlandingham, Dana L. (2014-11-13). "Bunyavirus-Vector Interactions". Viruses. 6 (11): 4373–4397. doi:10.3390/v6114373. ISSN 1999-4915. PMC 4246228. PMID 25402172.
  17. Lv Q, Zhang H, Tian L, Zhang R, Zhang Z, Li J, Tong Y, Fan H, Carr MJ, Shi W. Novel sub-lineages, recombinants and reassortants of severe fever with thrombocytopenia syndrome virus. Ticks Tick Borne Dis. 2017 Mar;8(3):385-390. doi: 10.1016/j.ttbdis.2016.12.015. Epub 2017 Jan 3. PMID: 28117273
  18. He CQ, Ding NZ. Discovery of severe fever with thrombocytopenia syndrome bunyavirus strains originating from intragenic recombination. J Virol. 2012 Nov;86(22):12426-30. doi: 10.1128/JVI.01317-12. Epub 2012 Aug 29. PMID: 22933273
  19. Patrick R. Murray, Ken S. Rosenthal and Michael A. Pfaller (2008-12-24). Medical Microbiology, 6e (6 ed.). Philadelphia: Mosby. ISBN 9780323054706.
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