Пикобирнавирусы: распространенность, генетическое разнообразие, методы детекции

Обзор посвящен пикобирнавирусам (ПБВ) – мелким безоболочечным изометрическим вирусам, таксономически относящимся к роду Picobirnavirus (PBV) семейства Picobirnaviridae, с геномом, представленным двумя сегментами двуцепочечной РНК. На основании публикаций за 1988–2019 гг. представлена информация о распространенности пикобирнавирусов в природе, о широком спектре поражаемых хозяев. Раскрыт оппортунистический характер ПБВ инфекции и подчеркивается отсутствие ясной картины в понимании роли ПБВ в качестве этиологического агента диареи, поскольку эти вирусы выявляются и при отсутствии симптомов заболевания. Рассматривается концепция, обосновывающая представление о ПБВ инфекции как о хроническом заболевании, обусловленном длительной персистенцией вируса в организме хозяина. Причины высокой частоты выявления ПБВ у людей и животных объясняются влиянием таких факторов, как стрессовый синдром, физиологическое состояние, иммунный статус и возраст хозяина при первичном инфицировании. Отмечается возможный зоонозный характер ПБВ инфекции человека, природа которого объясняется способностью этих вирусов к межвидовой трансмиссии, приобретенной в ходе эволюции благодаря реассортации сегментов генома разных вирусов, инфицировавших одного хозяина. Приводятся данные, доказывающие принадлежность ПБВ к вирусам эукариот, а также ставящая эти факты под сомнение гипотеза о возможной принадлежности ПБВ к вирусам бактерий. Подчеркнута необходимость активизации работ по выявлению ПБВ в связи с их широким распространением, несмотря на сложность из-за отсутствия системы для их культивирования. В качестве основных способов их детекции рассмотрены две стратегии ОТ-ПЦР ПБВ. Приведена характеристика геномов отдельных представителей рода, выделенных от разных хозяев. Акцент сделан на целесообразности разработки праймеров с более широкой специфичностью для увеличения диапазона выявляемых представителей рода ПБВ в связи с огромным разнообразием их генотипов. Подчеркивается важность эффективного мониторинга распространенности ПБВ для изучения их зоонозного и антропонозного потенциала с помощью метагеномного анализа, а также возможность использования этих вирусов в качестве перспективного маркера для мониторинга за чистотой окружающей среды.

1. Adriaenssens E.M., Farkas K., Harrison C., Jones D.L., Allison H.E., McCarthy A.J. Viromic analysis of wastewater input to a river catchment reveals a diverse assemblage of RNA viruses. mSystems. 2018; 3(3):1-18. DOI 10.1128/mSystems.00025-18.

2. Bányai K., Jakab F., Reuter G., Bene J., Uj M., Melegh B., Szücs G. Sequence heterogeneity among human picobirnaviruses detected in a gastroenteritis outbreak. Arch. Virol. 2003;148:2281-2291. DOI 10.1007/s00705-003-0200-z.

3. Bányai K., Martella V., Bogdán A., Forgách P., Jakab F., Meleg E., Bíró H., Melegh B., Szucs G. Genogroup I picobirnaviruses in pigs: evidence for genetic diversity and relatedness to human strains. J. Gen. Virol. 2008;89:534-539. DOI 10.1099/vir.0.83134-0.

4. Bodewes R., van der Giessen J., Haagmans B.L., Osterhaus A.D.M.E., Smits S.L. Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J. Virol. 2013;87(13): 7758-7764. DOI 10.1128/JVI.00568-13.

5. Boros Á., Polgár B., Pankovics P., Fenyvesi H., Engelmann P., Phan T.G., Delwart E., Reuter G. Multiple divergent picobirnaviruses with functional prokaryotic Shine–Dalgarno ribosome binding sites present in cloacal sample of a diarrheic chicken. Virol. J. 2018; 525:62-72. DOI 10.1016/j.virol.2018.09.008.

6. Carruyo G.M., Mateu G., Martínez L.C., Pujol F.H., Nates S.V., Liprandi F., Ludert J.E. Molecular characterization of porcine picobirnaviruses and development of a specific reverse transcription-PCR assay. J. Clin. Microbiol. 2008;46:2402-2405. DOI 10.1128/JCM.00655-08.

7. Cascio A., Bosco M., Vizzi E., Giammanco A., Ferraro D., Arista S. Identification of Picobirnavirus from faeces of Italian children suffering from acute diarrhea. Eur. J. Epidemiol. 1996;12:545-547. DOI 10.1007/BF00144011.

8. Collier A.M., Lyytinen O.L., Guo Y.R., Toh Y., Poranen M.M., Tao Y.J. Initiation of RNA polymerization and polymerase encapsidation by a small dsRNA virus. PLoS Pathog. 2016;12(4):1-26. DOI 10.1371/journal.ppat.1005523.

9. Conceicao-Neto N., Mesquita J.R., Zeller M., Yinda C.K., Álvares F., Roque S., Petrucci-Fonseca F., Godinho R., Heylen E., Van Ranst M., Matthijnssens J. Reassortment among picobirnaviruses found in wolves. Arch. Virol. 2016;161(10):2859-2862. DOI 10.1007/s00705-016-2987-4.

10. Dabrowska K., Switała-Jelen K., Opolski A., Weber-Dabrowska B., Gorski A. Bacteriophage penetration in vertebrates. J. Appl. Microbiol. 2005;98:7-13. DOI 10.1111/j.1365-2672.2004.02422.x.

11. Delmas B., Attoui H., Ghosh S., Malik Y.S., Mundt E., Vakharia V.N., ICTV Report Consortium. ICTV virus taxonomy profile: Picobirnaviridae. J. Gen. Virol. 2019;100:133-134. DOI 10.1099/jgv.0.001186.

12. Duquerroy S., Da Costa B., Henry C., Vigouroux A., Libersou S., Lepault J., Navaza J., Delmas B., Rey F.A. The picobirnavirus crystal structure provides functional insights into virion assembly and cell entry. EMBO J. 2009;28(11):1655-1665. DOI 10.1038/emboj.2009.109.

13. Duraisamy R., Akiana J., Davoust B., Mediannikov O., Michelle C., Robert C., Desnues C. Detection of novel RNA viruses from freeliving gorillas, Republic of the Congo: genetic diversity of picobirnaviruses. Virus Genes. 2018;54(2):256-271. DOI 10.1007/s11262-018-1543-6.

14. Epifanova N.V., Lukovnikova L.B., Golitsyna L.N., Fomina S.G., Zverev V.V., Ponomareva N.V., Parfenova O.V., Novikov D.V., Volkova M.A., Novikova N.A. Etiological structure of viral intestinal infections in children in Nizhny Novgorod. Meditsynskii Almanah = Medical Almanac. 2010;2(11):233-236. (in Russian)

15. Fregolente M.C., de Castro-Dias E., Martins S.S., Spilki F.R., Allegretti S.M., Gatti M.S. Molecular characterization of picobirnaviruses fromnewhosts. Virus Res. 2009;143(1):134-136. DOI 10.1016/j.virusres.2009.03.006.

16. Gallagher C.A., Navarro R., Cruz K., Aung M.S., Ng A., Bajak E., Beierschmitt A., Lawrence M., Dore K.M., Ketzis J., Malik Y.S., Kobayashi N., Ghosh S. Detection of picobirnaviruses in vervet monkeys (Chlorocebus sabaeus): molecular characterization of complete genomic segment-2. Virus Res. 2017;230:13-18. DOI 10.1016/j.virusres.2016.12.021.

17. Gallimore C.I., Appleton H., Lewis D., Green J., Brown D.W. Detection and characterisation of bisegmented double-stranded RNA viruses (picobirnaviruses) in human faecal specimens. J. Med. Virol. 1995a;45(2):135-140. DOI 10.1002/jmv.1890450204.

18. Gallimore C.I., Green J., Casemore D.P., Brown D.W. Detection of a picobirnavirus associated with Cryptosporidium positive stools from humans. Arch. Virol. 1995b;140(7):1275-1278. DOI 10.1007/bf01322752.

19. Ganesh B., Banyai K., Masachessi G., Mladenova Z., Nagashima S., Ghosh S., Pativada M., Kumar R., Kobayashi N. Genogroup I picobirnavirus in diarrhoeic foals: can the horse serve as a natural reservoir for human infection? Vet. Res. 2011b;42(1):52. DOI 10.1186/1297-9716-42-52.

20. Ganesh B., Masachessi G., Mladenova Z. Animal picobirnavirus. Virus Dis. 2014;25(2):223-238. DOI 10.1007/s13337-014-0207-y.

21. Ganesh B., Nagashima S., Ghosh S., Nataraju S.M., Rajendran K., Manna B., Ramamurthy T., Niyogi S.K., Kanungo S., Sur D., Kobayashi N., Krishnan T. Detection and molecular characterization of multiple strains of Picobirnavirus causing mixed infection in a diarrhoeic child: emergence of prototype Genogroup II-like strain in Kolkata, India. Int. J. Mol. Epidemiol. Genet. 2011a;2(1):61-72.

22. Ganesh B., Nataraju S.M., Rajendran K., Ramamurthy T., Kanungo S., Manna B., Nagashima S., Sur D., Kobayashi N., Krishnan T. Detection of closely related picobirnaviruses among diarrhoeic children in Kolkata: evidence of zoonoses? Infect. Genet. Evol. 2010;10(4): 511-516. DOI 10.1016/j.meegid.2010.02.008.

23. Ghosh S., Kobayashi N., Nagashima S., Naik T.N. Molecular characterization of full-length genomic segment 2 of a bovine picobirnavirus (PBV) strain: evidence for high genetic diversity with genogroup I PBVs. J. Gen. Virol. 2009;90(10):2519-2524. DOI 10.1099/vir.0.013987-0.

24. Ghosh S., Shiokawa K., Aung M.S., Malik Y.S., Kobayashi N. High detection rates of picobirnaviruses in free roaming rats (Rattus spp.): molecular characterization of complete gene segment-2. Infect. Genet. Evol. 2018;65:131-135. DOI 10.1016/j.meegid.2018.07.024.

25. Giordano M.O., Martinez L.C., Rinaldi D., Gúinard S., Naretto E., Casero R., Yacci M.R., Depetris A.R., Medeot S.I., Nates S.V. Detection of picobirnavirus in HIV-infected patients with diarrhea in Argentina. J. Acquir. Immune Defic. Syndr. 1998;18(4):380-383. DOI 10.1097/00042560-199808010-00010.

26. Giordano M.O., Martinez L.C., Rinaldi D., Espul C., Martinez N., Isa M.B., Depetris A.R., Medeot S.I., Nates S.V. Diarrhea and enteric emerging viruses in HIV-infected patients. AIDS Res. Hum. Retrov. 1999;15(16):1427-1432. DOI 10.1089/088922299309937.

27. Giordano M.O., Martinez L.C., Masachessi G., Barril P.A., Ferreyra L.J., Isa M.B., Valle M.C., Massari P.U., Nates S.V. Evidence of closely related Picobirnavirus strains circulating in humans and pigs in Argentina. J. Infect. 2011;62:45-51. DOI 10.1016/j.jinf.2010.09.031.

28. Giordano M.O., Masachessi G., Martinez L.C., Barril P.A., Ferreyra L.J., Isa M.B., Nates S.V. Two instances of large genome profile picobirnavirus occurrence in Argentinian infants with diarrhea over a 26-year period (1977–2002). J. Infect. 2008;56(5):371-375. DOI 10.1016/j.jinf.2008.02.017.

29. González G.G., Pujol F.H., Liprandi F., Deibis L., Ludert J.E. Prevalence of enteric viruses in human immunodeficiency virus seropositive patients in Venezuela. J. Med. Virol. 1998;55(4):288-292. DOI 10.1002/(sici)1096-9071(199808)55:4<288::aid-jmv6>3.0.co;2-x.

30. Górski A., Kniotek M., Perkowska-Ptasińska A., Mróz A., Przerwa A., Gorczyca W., Da̧ browska K., Weber-Da̧ browska B., Nowaczyk M. Bacteriophages and transplantation tolerance. Transplant. Proc. 2006;38:331-333. DOI 10.1016/j.transproceed.2005.12.073.

31. Green J., Gallimore C.I., Clewley J.P., Brown D.W. Genomic characterisation of the large segment of a rabbit picobirnavirus and comparison with the atypical picobirnavirus of Cryptosporidium parvum. Arch. Virol. 1999;144(12):2457-2465. DOI 10.1007/s007050050658.

32. Khramtsov N.V., Woods K.M., Nesterenko M.V., Dykstra C.C., Upton S.J. Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Mol. Microbiol. 1997;26(2):289-300. DOI 10.1046/j.1365-2958.1997.5721933.x.

33. King A.M.Q., Adams M.J., Carstens E.B., Lefkowitz E.J. (Eds.). Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses. Pt. II. The Viruses. (Family Picobirnaviridae). Elsevier; Acad. Press, 2012;535-539.

34. Kleymann A., Becker A.A.M.J., Malik Y.S., Kobayashi N., Ghosh S. Detection and molecular characterization of picobirnaviruses (PBVs) in the mongoose: identification of a novel PBV using an alternative genetic code. Viruses. 2020;12(1):99. DOI 10.3390/v12010099.

35. Knox M.A., Gedye K.R., Hayman D.T.S. The challenges of analysing highly diverse picobirnavirus sequence data. Viruses. 2018;10(12): 1-13. DOI 10.3390/v10120685.

36. Krishnamurthy S.R., Wang D. Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses. Virology. 2018;516:108-114. DOI 10.1016/j.virol.2018.01.006.

37. Kuhar U., Vengust G., Jamnikar-Ciglenecki U. Complete genome sequence of roe deer picobirnavirus strain PBV/roe_deer/SLO/D38 14/2014. Genome Announc. 2017;5(50):e01329-17. DOI 10.1128/genomeA.01329-17.

38. Kunz A.F., Possatti F., de Freitas J.A., Alfieri A.A., Takiuchi E. High detection rate and genetic diversity of picobirnavirus in a sheep flock in Brazil. Virus Res. 2018;255:10-13. DOI 10.1016/j.virusres.2018.06.016.

39. Kylla H., Dutta T.K., Roychoudhury P., Subudhi P.K. Coinfection of diarrheagenic bacterial and viral pathogens in piglets of Northeast region of India. Vet. World. 2019;12(2):224-230. Publ. online 2019, Feb 9. DOI 10.14202/vetworld.2019.224-230.

40. Lambden P.R., Cooke S.J., Caul E.O., Clarke I.N. Cloning of noncultivatable human rotavirus by single primer amplification. J. Virol. 1992;66:1817-1822.

41. Li L., Giannitti F., Low J., Keyes C., Ullmann L.S., Deng X., Aleman M., Pesavento P.A., Pusterla N., Delwart E. Exploring the virome of diseased horses. J. Gen. Virol. 2015; 96(9):2721-2733. DOI 10.1099/vir.0.000199.

42. Lojkić I., Biđin M., Prpić J., Šimić I., Krešić N., Bedeković T. Faecal virome of red foxes from peri-urban areas. Comp. Immunol. Microbiol. Infect. Dis. 2016;45:10-15. DOI 10.1016/j.cimid.2016.01.005.

43. Ludert J.E., Liprandi F. Identification of viruses with bi- and trisegmented double-stranded RNA genome in faeces of children with gastroenteritis. Res.Virol. 1993;144:219-224. DOI 10.1016/S0923-2516(06)80032-4.

44. Luo X.L., Lu S., Jin D., Yang J., Wu S.S., Xu J. Marmota himalayana in the Qinghai–Tibetan plateau as a special host for bi-segmented and unsegmented picobirnaviruses. Emerg. Microbes. Infect. 2018;7(1): 20. DOI 10.1038/s41426-018-0020-6.

45. Malik Y.S., Kumar N., Sharma K., Dhama K., Shabbir M.Z., Ganesh B., Banyai K. Epidemiology, phylogeny, and evolution of emerging enteric Picobirnaviruses of animal origin and their relationship to human strains. BioMed. Res. Int. 2014;780752. DOI 10.1155/2014/780752.

46. Malik Y.S., Sharma A.K., Sharma K., Sircar S., Dhama K. RNA polymerase gene based RT-PCR assay with primers update for genus specific detection of picobirnaviruses. J. Anim. Plant Sci. 2017; 27(2):582-588.

47. Martínez L.C., Giordano M.O., Isa M.B., Alvarado L.F., Paván J.V., Rinaldi D., Nates S.V. Molecular diversity of partial-length genomic segment 2 of human picobirnavirus. Intervirology. 2003;46(4):207- 213. DOI 10.1159/000072429.

48. Martínez L.C., Masachessi G., Carruyo G., Ferreyra L.J., Barril P.A., Isa M.B., Giordano M.O., Ludert J.E., Nates S.V. Picobirnavirus causes persistent infection in pigs. Infect. Genet. Evol. 2010;10:984- 988. DOI 10.1016/j.meegid.2010.06.004.

49. Masachessi G., Ganesh B., Martinez L.C., Giordano M.O., Barril P.A., Isa M.B., Paván G.V., Mateos C.A., Nates S.V. Maintenance of picobirnavirus (PBV) infection in an adult orangutan (Pongo pygmaeus) and genetic diversity of excreted viral strains during a three-year period. Infect. Genet. Evol. 2015;29:196-202. DOI 10.1016/j.meegid.2014.11.019.

50. Masachessi G., Martinez L.C., Ganesh B., Giordano M.O., Barril P.A., Isa M.B., Ibars A., Pavan J.V., Nates S.V. Establishment and maintenance of persistent infection by picobirnavirus in greater rhea (Rhea Americana). Arch. Virol. 2012;157(11):2075-2082. DOI 10.1007/s00705-012-1400-1.

51. Masachessi G., Martínez L.C., Giordano M.O., Barril P.A., Isa B.M., Ferreyra L., Villareal D., Carello M., Asis C., Nates S.V. Picobirnavirus (PBV) natural hosts in captivity and virus excretion pattern in infected animals. Arch. Virol. 2007;152(5):989-998. DOI 10.1007/s00705-006-0900-2.

52. McDonald S.M., Nelson M.I., Turner P.E., Patton J.T. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat. Rev. Microbiol. 2016;14(7):448-460. DOI 10.1038/nrmicro.2016.46.

53. Navarro J.O., Candido M., de Almeida-Queiroz S.R., Buzinaro M.D.G., Livonesi M.C., Fernandes A.M., de Sousa R.L.M. Genetic diversity of bovine Picobirnavirus, Brazil. Virus Genes. 2018;54(5):724-728. DOI 10.1007/s11262-018-1586-8.

54. Ng T.F., Vega E., Kondov N.O., Markey C., Deng X., Gregoricus N., Vinje J., Delwart E. Divergent picobirnaviruses in human feces. Genome Announc. 2014;2(3):e00415-14.

55. Novikova N.A., Epifanova N.V., Fedorova O.F., Golitsyna L.N., Kupriianova N.V. Detection of picobirnaviruses by electrophoresis of RNA in polyacrylamide gel. Voprosy Virusologii = Problems of Virology. 2003;48(6):41-43. (in Russian)

56. Ochoa W.F., Havens W.M., Sinkovits R.S., Nibert M.L., Ghabrial S.A., Baker T.S. Partitivirus structure reveals a 120-subunit, helix-rich capsid with distinctive surface arches formed by quasisymmetric coat-protein dimers. Structure. 2008;16(5):776-786. DOI 10.1016/j.str.2008.02.014.

57. Omotajo D., Tate T., Cho H., Choudhary M. Distribution and diversity of ribosome binding sites in prokaryotic genomes. BMC Genom. 2015;16(1):604. DOI 10.1186/s12864-015-1808-6.

58. Pereira H.G., Fialho A.M., Flewett T.H., Teixeira J.M.S., Andrade Z.P. Novel viruses in human faeces. Lancet. 1988a;332(8602):103-104. DOI 10.1016/S0140-6736(88)90032-3.

59. Pereira H.G., Flewett T.H., Candeias J.A.N., Barth O.M. A virus with a bisegmented double-stranded RNA genome in rat (Oryzomys nigripes) intestines. J. Gen. Virol. 1988b;69:2749-2754. DOI 10.1099/0022-1317-69-11-2749.

60. Pereira H.G., Linhares A.C., Candeias J.A., Glass R.I. National laboratory surveillance of viral agents of gastroenteritis in Brazil. Bull. Pan. Am. Health Organ. 1993;27:224-233.

61. Reed C.А., Langlais C., Wang I.-N., Young R. A2 expression and assembly regulates lysis in Qβ infections. Microbiol. (Reading, England). 2013;159:507-514. DOI 10.1099/mic.0.064790-0.

62. Ribeiro S.R., Bezerra D.A.., Kaiano J.H., de Souza Oliveira D., Silvestre R.V., Gabbay Y.B., Ganesh B., Mascarenhas J.D. Genogroup I avian picobirnavirus detected in Brazilian broiler chickens: a molecular epidemiology study. J. Gen. Virol. 2014;95(1):117-122. DOI 10.1099/vir.0.054783-0.

63. Rosen B.I., Fang Z.-Y., Glass R.I., Monroe S.S. Cloning of human picobirnavirus genomic segments and development of an RT-PCR detection assay. Virology. 2000;277(2):316-329. DOI 10.1006/viro.2000.0594.

64. Shi M., Lin X.D., Chen X., Tian J.H., Chen L.J., Li K., Wang W., Eden J.S., Shen J.J., Liu L., Holmes E.C., Zhang Y.Z. The evolutionary history of vertebrate RNA viruses. Nature. 2018;556(7700): 197-202. DOI 10.1038/s41586-018-0012-7.

65. Shi M., Lin X.D., Tian J.H., Chen L.J., Chen X., Li C.X., Qin X.C., Li J., Cao J.P., Eden J.S., Buchmann J., Wang W., Xu J., Holmes E.C., Zhang Y.Z. Redefining the invertebrate RNA virosphere. Nature. 2016;540(7634):539-543. DOI 10.1038/nature20167.

66. Smits S.L., Poon L.L., van Leeuwen M., Lau P.N., Perera H.K., Peiris J.S., Simon J.H., Osterhaus A.D. Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg. Infect. Dis. 2011;17(12): 2328-2330. DOI 10.3201/eid1712.110934.

67. Smits S.L., Schapendonk C.M., van Beek J., Vennema H., Schürch A.C., Schipper D., Bodewes R., Haagmans B.L., Osterhaus A.D., Koopmans M.P. New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg. Infect. Dis. 2014;20(7):1218-1222. DOI 10.3201/eid2007.140190.

68. Smits S.L., van Leeuwen M., Schapendonk C.M., Schürch A.C., Bodewes R., Haagmans B.L., Osterhaus A.D. Picobirnaviruses in the human respiratory tract. Emerg. Infect. Dis. 2012;18(9):1539- 1540. DOI 10.3201/eid1809.120507.

69. Symonds E.M., Griffin D.W., Breitbart M. Eukaryotic viruses in wastewater samples from the United States. Appl. Environ. Microbiol. 2009;75:1402-1409. DOI 10.1128/AEM.01899-08.

70. Takiuchi E., Macedo R., Kunz A.F., Gallego J.C., de Mello J.L., Otonel R.A., Alfieri A.A. Electrophoretic RNA genomic profiles of Brazilian Picobirnavirus (PBV) strains and molecular characterization of a PBV isolated from diarrheic calf. Virus Res. 2016;211(4):58-63. DOI 10.1016/j.virusres.2015.09.022.

71. Vainio E.J., Chiba S., Ghabrial S.A., Maiss E., Roossinck M., Sabanadzovic S., Suzuki N., Xie J., Nibert M. ICTV Report Consortium. ICTV Virus Taxonomy Profile: Partitiviridae. J. Gen. Virol. 2018; 99(1):17-18. DOI 10.1099/jgv.0.000985.

72. van Leeuwen M., Williams M.M., Koraka P., Simon J.H., Smits S.L., Osterhaus A.D. Human picobirnaviruses identified by molecular screening of diarrhea samples. J. Clin. Microbiol. 2010;48(5):1787- 1794. DOI 10.1128/JCM.02452-09.

73. Vanopdenbosch E., Wellemans G. Birna-type virus in diarrhoeic calf faeces. Vet. Rec. 1989;125(24):610.

74. Verma H., Mor S.K., Erber J., Goyal S.M. Prevalence and complete genome characterization of turkey picobirnaviruses. Infect. Genet. Evol. 2015;30:134-139. DOI 10.1016/j.meegid.2014.12.014.

75. Wakuda M., Pongsuwanna Y., Taniguchi K. Complete nucleotide sequences of two RNA segments of human picobirnavirus. J. Virol. Methods. 2005;126(1-2):165-169. DOI 10.1016/j.jviromet.2005.02.010.

76. Wang Y., Banyai K., Tu X., Jiang B. Simian genogroup I picobirnaviruses: prevalence, genetic diversity, and zoonotic potential. J. Clin. Microbiol. 2012;50:2779-2782. DOI 10.1128/JCM.00634-12.

77. Wilburn L., Yodmeeklin A., Kochjan P., Saikruang W., Kumthip K., Khamrin P., Maneekarn N. Molecular detection and characterization of picobirnaviruses in piglets with diarrhea in Thailand. Arch. Virol. 2016;162(4):1061-1066. DOI 10.1007/s00705-016-3190-3.

78. Wille M., Shi M., Klaassen M., Hurt A.C., Holmes E.C. Virome heterogeneity and connectivity in waterfowl and shorebird communities. ISME J. 2019;13(10):2603-2616. DOI 10.1038/s41396-019-0458-0.

79. Woo P.C.Y., Lau S.K.P., Bai R., Teng J.L.L., Lee P., Martelli P., Hui S.W., Yuen K.Y. Complete genome sequence of a novel picobirnavirus, otarine picobirnavirus, discovered in California sea lions. J. Virol. 2012;86(11):6377-6378. DOI 10.1128/JVI.00686-12.

80. Woo P.C.Y., Teng J.L.L., Bai R., Tang Y., Wong A.Y.P., Li K.S.M., Lam C.S.F., Fan R.Y.Y., Lau S.K.P., Yuen K.-Y. Novel picobirnaviruses in respiratory and alimentary tracts of cattle and monkeys with large intra- and inter-host diversity. Viruses. 2019;11(6):574. DOI 10.3390/v11060574.

81. Yinda C.K., Ghogomu S.M., Conceicao-Neto N., Beller L., Deboutte W., Vanhulle E., Maes P., Van Ranst M., Matthijnssens J. Cameroonian fruit bats harbor divergent viruses, including rotavirus H, bastroviruses, and picobirnaviruses using an alternative genetic code. Virus Evol. 2018;3(2):vey008. DOI 10.1093/ve/vey008.

82. Yinda C.K., Vanhulle E., Conceição-Neto N., Beller L., Deboutte W., Shi C., Ghogomu S.M., Maes P., Van Ranst M., Matthijnssens J. Gut virome analysis of Cameroonians reveals high diversity of enteric viruses, including potential interspecies transmitted viruses. mSphere. 2019;4(1):1-22. DOI 10.1128/mSphere.00585-18.

83. Zhang B., Tang C., Yue H., Ren Y., Song Z. Viral metagenomics analysis demonstrates the diversity of viral flora in piglet diarrhoeic faeces in China. J. Gen. Virol. 2014;95(7):1603-1611. DOI 10.1099/vir.0.063743-0.

84. Zhang S., Bai R., Feng R., Zhang H., Liu L. Detection and evolutionary analysis of picobirnaviruses in treated wastewater. Microb. Biotechnol. 2015;8(3):474-482. DOI 10.1111/1751-7915.12239.