Bats of the subtropical climate zone of the Krasnodar Territory of Russia as a possible reservoir of zoonotic viral infections

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Abstract

Emerging and reemerging infections pose a grave global health threat. The emergence of the SARS-CoV-2 virus and the resulting COVID-19 pandemic have demonstrated the importance of studying of zoonotic viruses directly in natural foci. For SARS-like coronaviruses, as well as for many other zoonotic pathogens (including hemorrhagic fevers and rabies agents), the main reservoir are horseshoe bats (Rhinolophus spp.), which are widely distributed in Eurasia and Africa. Their range also covers the southern regions of Russia, including the North Caucasus and Crimea. Large colonies of these animals are located on the territory of Sochi National Park (SNP; subtropical zone of Krasnodar Territory, Greater Sochi region, North Caucasus). In total, according to long-term observations, up to 23 species of bats were registered here, including the great (Rh. ferrumequinum), the lesser (Rh. hipposideros), and the Mediterranean (Rh. euryale) horseshoe bats.
This review provides information on zoonotic viruses associated with species of bats distributed in the subtropical zone of Krasnodar Territory of Russia, and analyzes their possible role as a natural reservoir of emerging and reemerging infections. Studying the circulation of zoonotic viruses in bats is an important element of monitoring viral populations in natural foci.

About the authors

S. V. Lenshin

FSBRI «Research Institute of Medical Primatology» of the Ministry of Higher Education and Science of Russia

Email: lenshin-s@mail.ru
ORCID iD: 0000-0001-6815-2869

Lenshin Sergey V.; Master of Science, Scientist of laboratory of infectious virology

354376, Sochi

Russian Federation

A. V. Romashin

FSBI «Sochi National Park» of the Ministry of Natural Resources and Environment of Russia

Email: romashin@sochi.com
ORCID iD: 0000-0003-4751-1484

Romashin Aleksey V.; PhD, Leading scientist

354002, Sochi

Russian Federation

O. I. Vyshemirsky

FSBRI «Research Institute of Medical Primatology» of the Ministry of Higher Education and Science of Russia

Email: olegvyshem@mail.ru
ORCID iD: 0000-0002-5345-8926

Vishemirsky Oleg I.; PhD, Leading Scientist of laboratory of infectious virology

354376, Sochi

Russian Federation

D. K. Lvov

FSBI «National Research Centre for Epidemiology and Microbiology named after honorary academician N.F. Gamaleya» of the Ministry of Health of Russia

Email: dk_lvov@mail.ru
ORCID iD: 0000-0001-8176-6582

Lvov Dmitry K., Academician of RAS, prof. Head of department of Ecology of Viruses, D.I. Ivanovsky institute of virology

Moscow, 123098

Russian Federation

S. V. Alkhovsky

FSBI «National Research Centre for Epidemiology and Microbiology named after honorary academician N.F. Gamaleya» of the Ministry of Health of Russia

Author for correspondence.
Email: salkh@ya.ru

Alkhovsky Sergey V.; Dr. of Sci. (Biology), head of the laboratory of biotechnology, D.I. Ivanovsky institute of virology

Moscow, 123098

Russian Federation

References

  1. Simmons N.B. Order Chiroptera. In: Wilson D.E., Reeder D.M., eds. Mammal Species World a Taxon and Geographic Reference. Baltimore: Johns Hopkins University Press; 2005: 312–529. https://doi.org/10.1093/acprof:osobl/9780199207114.003.0001.
  2. Racey P.A. The prolonged storage and survival of spermatozoa in Chiroptera. J. Reprod. Fertil. 1979; 56(1): 391–402. https://doi.org/10.1530/jrf.0.0560391.
  3. Cowled C., Stewart C.R., Likic V.A., Friedländer M.R., Tachedjian M., Jenkins K.A., et al. Characterization of novel microRNAs in the Black flying fox (Pteropus alecto) by deep sequencing. BMC Genomics. 2014; 15(1): 682. https://doi.org/10.1186/1471-2164-15-682.
  4. Banerjee A., Baker M.L., Kulcsar K., Misra V., Plowright R., Mossman K. Novel insights into immune systems of bats. Front. Immunol. 2020; 11: 26. https://doi.org/10.3389/fimmu.2020.00026.
  5. Lagunas-Rangel F.A. Why do bats live so long? Possible molecular mechanisms. Biogerontology. 2020; 21(1): 1–11. https://doi.org/10.1007/s10522-019-09840-3.
  6. Крускоп С.В. Отряд Chiroptera. В кн.: Павлинов И.Я., Лисовский А.А., ред. Млекопитающие России: Систематико-географический справочник. Сборник трудов Зоологического музея МГУ. Выпуск 52. Москва: КМК; 2012: 73–126.
  7. Baloun D.E., Guglielmo C.G. Energetics of migratory bats during stopover: a test of the torpor-assisted migration hypothesis. J. Exp. Biol. 2019; 222: jeb196691. https://doi.org/10.1242/jeb.196691.
  8. Khan M.S., Hossain J., Gurley E.S., Nahar N., Sultana R., Luby S.P. Use of infrared camera to understand bats’ access to date palm sap: implications for preventing Nipah virus transmission. Ecohealth. 2010; 7(4): 517–25. https://doi.org/10.1007/s10393-010-0366-2.
  9. Calisher C.H., Childs J.E., Field H.E., Holmes K.V., Schountz T. Bats: Important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 2006; 19(3): 531–45. https://doi.org/10.1128/CMR.00017-06.
  10. Wang L., Cowled C. Bats and Viruses: A New Frontier of Emerging Infectious Diseases. New York: John Wiley & Sons, Inc; 2015: 23–45. https://doi.org/10.1002/9781118818824.
  11. Ang B.S.P., Lim T.C.C., Wang L. Nipah Virus Infection. J. Clin. Microbiol. 2018; 56: e01875-17. https://doi.org/10.1128/jcm.01875-17.
  12. Selvey L., Sheridan J. Outbreak of severe respiratory disease in humans and horses due to a previously unrecognized paramyxovirus. J. Travel. Med. 1995; 2(4): 275. https://doi.org/10.1111/j.1708-8305.1995.tb00679.x.
  13. Hasan S., Ahmad S.A., Masood R., Saeed S. Ebola virus: A global public health menace: A narrative review. J. Family Med. Prim. Care. 2019; 8(7): 2189–201. https://doi.org/10.4103/jfmpc.jfmpc_297_19.
  14. Singh R.K., Dhama K., Chakraborty S., Tiwari R., Natesan S., Khandia R., et al. Nipah virus: epidemiology, pathology, immunobiology and advances in diagnosis, vaccine designing and control strategies – a comprehensive review. Vet. Q. 2019; 39(1): 26–55. https://doi.org/10.1080/01652176.2019.1580827.
  15. L’vov D.K., Tsyrkin Y.M., Karas F.R., Timopheev E.M., Gromashevski V.L., Veselovskaya O.V., et al. “Sokuluk” virus, a new group B arbovirus isolated from Vespertilio pipistrellus Schreber, 1775, bat in the Kirghiz S.S.R. Arch. Gesamte Virusforsch. 1973; 41(3): 170–4. https://doi.org/10.1007/bf01252762.
  16. Альховский С.В., Львов Д.К., Щелканов М.Ю., Дерябин П.Г., Щетинин А.М., Самохвалов Е.И., и др. Генетическая характеристика вируса Узун-Агач (UZAV – Uzun-Agach virus) (Bunyaviridae, Nairovirus), изолированного в Казахстане от остроухой ночницы Myotis blythii oxygnathus Monticelli, 1885 (Chiroptera; Vespertilionidae). Вопросы вирусологии. 2014; 59(5): 23–6.
  17. Альховский С.В., Львов Д.К., Щелканов М.Ю., Щетинин А.М., Дерябин П.Г., Самохвалов Е.И., и др. Таксономия вируса Иссык-Куль (Issyk-Kul virus, ISKV; Bunyaviridae, Nairovirus), возбудителя Иссык-Кульской лихорадки, изолированного от летучих мышей (Vespertilionidae) и клещей Argas (Carios) vespertilionis (Latreille, 1796). Вопросы вирусологии. 2013; 58(5): 11–5.
  18. Kuz’min V., Botvinkin A.D., Poleschuk E.M., Orciari L.A., Rupprecht C.E. Bat rabies surveillance in the former Soviet Union. Dev. Biol. (Basel). 2006; 125: 273–82.
  19. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J. H. et al. Bats Are Natural Reservoirs of SARS-like Coronaviruses. Science. 2005; 310(5748):676–79. doi: 10.1126/science.1118391.
  20. Drexler J.F., Corman V.M., Drosten C. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Res. 2014; 101: 45–56. https://doi.org/10.1016/j.antiviral.2013.10.013.
  21. Groot R.J., Baker S.C., Baric R., Enjuanes L., Gorbalenya A.E., Holmes K.V., et al. «Family Coronaviridae». In: King A.M., 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. London: Elsevier; 2012: 806–28.
  22. Woo P.C., Huang Y., Lau S.K., Yuen K.Y. Coronavirus genomics and bioinformatics analysis. Viruses. 2010; 2(8): 1804–20. https://doi.org/10.3390/v2081803.
  23. Львов Д.К., Гулюкин М.И., Забережный А.Д., Гулюкин А.М. Формирование популяционного генофонда потенциально угрожающих биобезопасности зоонозных вирусов. Вопросы вирусологии. 2020; 65(5): 243–58. https://doi.org/10.36233/0507-4088-2020-65-5-1.
  24. Haake C., Cook S., Pusterla N., Murphy B. Coronavirus Infections in companion animals: virology, epidemiology, clinical and pathologic features. Viruses. 2020; 12(9): 1023. https://doi.org/10.3390/v12091023.
  25. Schulz L.L., Tonsor G.T. Assessment of the economic impacts of porcine epidemic diarrhea virus in the United States. J. Anim. Sci. 2015; 93(11): 5111–8. https://doi.org/10.2527/jas.2015-9136.
  26. Colvero L.P., Villarreal L.Y., Torres C.A., Brañdo P.E. Assessing the economic burden of avian infectious bronchitis on poultry farms in Brazil. Rev. Sci. Tech. 2015; 34(3): 993–9. https://doi.org/10.20506/rst.34.3.2411.
  27. Яцышина С.Б., Мамошина М.В., Шипулина О.Ю., Подколзин А.Т., Акимкин В.Г. Анализ циркуляции коронавирусов человека. Вопросы вирусологии. 2020; 65(5): 267–76. https://doi.org/10.36233/0507-4088-2020-65-5-3.
  28. Львов Д.К., Бурцева Е.И., Колобухина Л.В., Федякина И.Т., Бовин Н.В., Игнатьева А.В. и др. Особенности циркуляции вирусов гриппа и ОРВИ в эпидемическом сезоне 2019–2020 гг. в отдельных регионах России. Вопросы вирусологии. 2020; 65(6): 335–49. https://doi.org/10.36233/0507-4088-2020-65-6-4.
  29. Rabaan A.A., Al-Ahmed S.H., Haque S., Sah R., Tiwari R., Malik Y.S., et al. SARS-CoV-2, SARS-CoV, and MERS-COV: A comparative overview. Infez. Med. 2020; 28(2): 174–84.
  30. Fehr A.R., Perlman S. Coronaviruses: An Overview of Their Replication and Pathogenesis. Methods Mol. Biol. 2015; 1282: 1–23. https://doi.org/10.1007/978-1-4939-2438-7_1.
  31. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in Southern China. Science. 2003; 302: 276–8. https://doi.org/10.1126/science.1087139.
  32. Banerjee A., Kulcsar K., Misra V., Frieman M., Mossman K. Bats and coronaviruses. Viruses. 2019; 11(1): 41. https://doi.org/10.3390/v11010041.
  33. European Centre for Disease Prevention and Control. Distribution of confirmed cases of MERS-CoV by place of infection and month of onset. Available at: https://www.ecdc.europa.eu/en/publications-data/distribution-confirmed-cases-mers-cov-place-infectionand-month-onset-march-2012 (accessed January 14, 2021).
  34. Middle East respiratory syndrome coronavirus (MERS-CoV) – Republic of Korea. Available at: https://www.who.int/csr/don/01-june2015-mers-korea/en/ (accessed January 14, 2021).
  35. Falzarano D., Kamissoko B., de Wit E., Maïga O., Cronin J., Samaké K., et al. Dromedary camels in northern Mali have high seropositivity to MERS-CoV. One Health. 2017; 3: 41–3. https://doi.org/10.1016/j.onehlt.2017.03.003.
  36. Alexandersen S., Kobinger G.P., Soule G., Wernery U. Middle East respiratory syndrome coronavirus antibody reactors among camels in Dubai, United Arab Emirates, in 2005. Transbound. Emerg. Dis. 2014; 61(2): 105–108. https://doi.org/10.1111/tbed.12212.
  37. Alshukairi A.N., Zheng J., Zhao J., Nehdi A., Baharoon S.A., Layqah L., et al. High prevalence of MERS-CoV infection in camel workers in Saudi Arabia. mBio. 2018; 9(5): e01985-18. https://doi.org/10.1128/mbio.01985-18.
  38. Anthony S.J., Gilardi K., Menachery V.D., Goldstein T., Ssebide B., Mbabazi R., et al. Further evidence for bats as the evolutionary source of middle east respiratory syndrome coronavirus. mBio. 2017; 8(2): e00373-17. https://doi.org/10.1128/mbio.00373-17.
  39. Reusken C.B., Messadi L., Feyisa A., Ularamu H., Godeke G.J., Danmarwa A., et al. Geographic distribution of MERS coronavirus among dromedary camels, Africa. Emerg. Infect. Dis. 2014; 20(8): 1370–4. https://doi.org/10.3201/eid2008.140590.
  40. Corman V.M., Jores J., Meyer B., Younan M., Liljander A., Said M.Y., et al. Antibodies against MERS coronavirus in dromedary camels, Kenya, 1992–2013. Emerg. Infect. Dis. 2014; 20(8): 1319–22. https://doi.org/10.3201/eid2008.140596.
  41. Zhu N., Zhang D., Wang W., Li X., Yang B., Song J., et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N. Engl. J. Med. 2020; 382(8): 727–33. https://doi.org/10.1056/nejmoa2001017.
  42. Li X., Wang W., Zhao X., Zai J., Zhao Q., Li Y., et al. Transmission dynamics and evolutionary history of 2019-nCoV. J. Med. Virol. 2020; 92(5): 501–11. https://doi.org/10.1002/jmv.25701.
  43. World Health Organization. Coronavirus disease (COVID-19) Situation Report – 146. Available at: https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200614-covid-19-sitrep-146.pdf?sfvrsn=5b89bdad_4 (accessed January 14, 2021).
  44. Zhou P., Yang X.L., Wang X.G., Hu B., Zhang L., Zhang W., et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579(7798): 270–3. https://doi.org/10.1038/s41586-020-2012-7.
  45. Львов Д.К., Альховский С.В., Колобухина Л.В., Бурцева Е.И. Этиология эпидемической вспышки COVID-19 в г. Ухань (провинция Хубэй, Китайская Народная Республика), ассоциированной с вирусом 2019-nCoV (Nidovirales, Coronaviridae, Coronavirinae, Betacoronavirus, подрод Sarbecovirus): уроки эпидемии SARS-CoV. Вопросы вирусологии. 2020; 65(1): 6–15. https://doi.org/10.36233/0507-4088-2020-65-1-6-15.
  46. Львов Д.К., Альховский С.В. Истоки пандемии COVID-19: экология и генетика коронавирусов (Betacoronavirus: Coronaviridae) SARS-CoV, SARS-CoV-2 (подрод Sarbecovirus), MERS-CoV (подрод Merbecovirus). Вопросы вирусологии. 2020; 65(2): 62–70. https://doi.org/10.36233/0507-4088-2020-65-2-62-70.
  47. Газарян С.В. Эколого-фаунистический анализ населения рукокрылых (Chiroptera) Западного Кавказа: Автореф. дис. … канд. биол. наук. Москва; 2002.
  48. Иванов С.П., Фатерыга А.В., ред. Красная книга Республики Крым. Животные. Симферополь: Ариал; 2015.
  49. Drexler J.F., Gloza-Rausch F., Glende J., Corman V.M., Muth D., Goettsche M., et al. Genomic characterization of severe acute respiratory syndrome-related coronavirus in european bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J. Virol. 2010; 84(21): 11336–49. https://doi.org/10.1128/jvi.00650-10.
  50. Rihtaric D., Hostnik P., Steyer A., Grom J., Toplak I. Identification of SARS-like coronaviruses in horseshoe bats (Rhinolophus hipposideros) in Slovenia. Arch. Virol. 2010; 155(4): 507–14. https://doi.org/10.1007/s00705-010-0612-5.
  51. Monchatre-Leroy E., Boué F., Boucher J.M., Renault C., Moutou F., Ar Gouilh M., et al. Identification of alpha and beta Coronavirus in wildlife species in France: bats, rodents, rabbits, and hedgehogs. Viruses. 2017; 9(12): 364. https://doi.org/10.3390/v9120364.

Copyright (c) 2021 Lenshin S.V., Romashin A.V., Vyshemirsky O.I., Lvov D.K., Alkhovsky S.V.

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