Jingmenvirus

Jingmenvirus is a group of positive-sense single-stranded RNA viruses with segmented genomes. They are primarily associated with arthropods and are one of only two known segmented RNA viruses that infect animal hosts.[1][2][3] The first group member, the Jingmen tick virus (JMTV), was described in 2014.[4] Another member, the Guaico Culex virus (GCXV), has a highly unusual multicomponent architecture in which the genome segments are separately enclosed in different viral capsids.[5]

Jingmenvirus
Virus classification Edit this classification
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Kitrinoviricota
Class: Flasuviricetes
Order: Amarillovirales
Family: Flaviviridae (?)
(unranked): Jingmenvirus
Member viruses

Examples

Jingmen tick virus

The group's first member was described in 2014 and named the Jingmen tick virus (JMTV) because it was isolated from a tick sampled in Jingmen, China.[4] It is an enveloped spherical virus slightly larger than its closest viral relatives. The JMTV genome has four segments, two containing genes with sequence homology to non-structural proteins found in flaviviruses, including methyltransferase and RNA-dependent RNA polymerase. The putative structural proteins in the JMTV genome have no known homologs.[4] In addition to identification in ticks, JMTV has also been identified in low abundances in mosquitoes such as Aedes albopictus.[6]

Guaico Culex virus

The Guaico Culex virus (GCXV) was reported in 2016 after isolation from Culex mosquitoes found near Guaico, Trinidad.[5] Different virus isolates have four or five genome segments, though the fifth is not essential for viral proliferation. GCXV is a multicomponent (multipartite) virus in which each genome segment is enclosed in its small, enveloped viral capsid. At least three genome segments, containing genes for non-structural proteins and capsid components, must enter a cell to infect it and reproduce the virus successfully.[5] Before the discovery of GMXV, multicomponent architecture had previously been reported only in viruses that infect plants and fungi, and had never been observed in an enveloped virus.[1][5]

Other viruses

Genetic material that likely belongs to other jingmenviruses can be identified through bioinformatics. In some cases, such sequences were not recognized as viral or the segmented nature of the genome was not recognized before JMTV was described. For example, the reported genome of the dog parasite Toxocara canis was found to contain sequences with homology to JMTV, likely representing a viral infection in the parasite that was sequenced.[4][7] The Mogiana tick virus, first reported in 2011, is a similar example; its segmented genome was not recognized on first publication but was reanalyzed and identified as a jingmenvirus in 2017.[8]

Sequences with homology to JMTV have also been isolated from a red colobus monkey, suggesting the possibility of a segmented, possibly multicomponent virus capable of infecting primates.[5] A metagenomics study of arthropod flaviviruses identified five additional examples of likely jingmenvirus sequences.[9]

Evolution

Jingmenviruses are related to flaviviruses, which have non-segmented genomes transmitted in a single capsid. Homology has consistently been observed between the genes encoding non-structural proteins of jingmenviruses and flaviviruses, including RNA-dependent RNA polymerase. However, the genomic architecture of the homologous genes varies significantly; the canonical flavivirus genome consists of a single open reading frame (ORF) whose protein product is processed by proteases, whereas the non-structural jingmenvirus proteins are encoded on two genome segments, each containing one ORF. Although there are few known jingmenvirus sequences, the gene composition of the genome segments appears to be well-conserved.[4][5][9] By contrast, the putative jingmenvirus structural proteins that likely make up its capsids have no homology to known proteins.[4][5]

It is striking that the segmented jingmenviruses' closest known relatives are nonsegmented.[1][2] The evolutionary mechanisms underlying genome segmentation and especially multicomponent architecture are poorly understood. Although segmented genomes appear to have evolved several times in the virome, the evolutionary mechanism underlying this structure is unclear.[10][11] Likewise, It is unclear whether multicomponent architecture is a distinct evolutionary strategy or an artifact of the segmentation mechanism, possibly via the formation of defective interfering particles.[1][10]

References
  1. Holmes, Edward C. (September 2016). "The Expanding Virosphere". Cell Host & Microbe. 20 (3): 279–280. doi:10.1016/j.chom.2016.08.007. PMID 27631697.
  2. Attar, Naomi (6 September 2016). "Animal viruses in pieces". Nature Reviews Microbiology. 14 (10): 606–7. doi:10.1038/nrmicro.2016.133. PMID 27595788.
  3. Michalakis, Yannis (September 2020). "The Curious Strategy of Multipartite Viruses" (PDF). Annual Review of Virology. 7 (1): 203–218. doi:10.1146/annurev-virology-010220-063346. PMID 32991271. S2CID 222161056.
  4. Qin, X.-C.; Shi, M.; Tian, J.-H.; Lin, X.-D.; Gao, D.-Y.; He, J.-R.; Wang, J.-B.; Li, C.-X.; Kang, Y.-J.; Yu, B.; Zhou, D.-J.; Xu, J.; Plyusnin, A.; Holmes, E. C.; Zhang, Y.-Z. (21 April 2014). "A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors". Proceedings of the National Academy of Sciences. 111 (18): 6744–6749. Bibcode:2014PNAS..111.6744Q. doi:10.1073/pnas.1324194111. PMC 4020047. PMID 24753611.
  5. Ladner, Jason T.; Wiley, Michael R.; Beitzel, Brett; Auguste, Albert J.; Dupuis, Alan P.; Lindquist, Michael E.; Sibley, Samuel D.; Kota, Krishna P.; Fetterer, David; Eastwood, Gillian; Kimmel, David; Prieto, Karla; Guzman, Hilda; Aliota, Matthew T.; Reyes, Daniel; Brueggemann, Ernst E.; St. John, Lena; Hyeroba, David; Lauck, Michael; Friedrich, Thomas C.; O’Connor, David H.; Gestole, Marie C.; Cazares, Lisa H.; Popov, Vsevolod L.; Castro-Llanos, Fanny; Kochel, Tadeusz J.; Kenny, Tara; White, Bailey; Ward, Michael D.; Loaiza, Jose R.; Goldberg, Tony L.; Weaver, Scott C.; Kramer, Laura D.; Tesh, Robert B.; Palacios, Gustavo (September 2016). "A Multicomponent Animal Virus Isolated from Mosquitoes". Cell Host & Microbe. 20 (3): 357–367. doi:10.1016/j.chom.2016.07.011. PMC 5025392. PMID 27569558.
  6. Parry R, James ME, Asgari S (2021). "Uncovering the Worldwide Diversity and Evolution of the Virome of the Mosquitoes Aedes aegypti and Aedes albopictus". Microorganisms. 9 (8): 1653. doi:10.3390/microorganisms9081653. PMC 8398489. PMID 34442732.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  7. Tetteh, KK; Loukas, A; Tripp, C; Maizels, RM (September 1999). "Identification of abundantly expressed novel and conserved genes from the infective larval stage of Toxocara canis by an expressed sequence tag strategy". Infection and Immunity. 67 (9): 4771–9. doi:10.1128/IAI.67.9.4771-4779.1999. PMC 96808. PMID 10456930.
  8. Villa, Erika C.; Maruyama, Sandra R.; de Miranda-Santos, Isabel K. F.; Palacios, Gustavo; Ladner, Jason T. (4 May 2017). "Complete Coding Genome Sequence for Mogiana Tick Virus, a Jingmenvirus Isolated from Ticks in Brazil". Genome Announcements. 5 (18): e00232–17. doi:10.1128/genomeA.00232-17. PMC 5477184. PMID 28473376.
  9. Shi, Mang; Lin, Xian-Dan; Vasilakis, Nikos; Tian, Jun-Hua; Li, Ci-Xiu; Chen, Liang-Jun; Eastwood, Gillian; Diao, Xiu-Nian; Chen, Ming-Hui; Chen, Xiao; Qin, Xin-Cheng; Widen, Steven G.; Wood, Thomas G.; Tesh, Robert B.; Xu, Jianguo; Holmes, Edward C.; Zhang, Yong-Zhen; Ou, J.-H. J. (15 January 2016). "Divergent Viruses Discovered in Arthropods and Vertebrates Revise the Evolutionary History of the Flaviviridae and Related Viruses". Journal of Virology. 90 (2): 659–669. doi:10.1128/JVI.02036-15. PMC 4702705. PMID 26491167.
  10. Lucía-Sanz, Adriana; Manrubia, Susanna (9 November 2017). "Multipartite viruses: adaptive trick or evolutionary treat?". npj Systems Biology and Applications. 3 (1): 34. doi:10.1038/s41540-017-0035-y. PMC 5680193. PMID 29263796.
  11. Sicard, Anne; Michalakis, Yannis; Gutiérrez, Serafín; Blanc, Stéphane; Hobman, Tom C. (3 November 2016). "The Strange Lifestyle of Multipartite Viruses". PLOS Pathogens. 12 (11): e1005819. doi:10.1371/journal.ppat.1005819. PMC 5094692. PMID 27812219.
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