Adnan BALKAYA, Abdullah GÜLLER, Mustafa USTA, Zeynelabidin KURT

Türkiye’nin Bingöl ili Bal Arı Kolonilerinde Deforme kanat virüsü ve Kronik arı felci virüsü’nün Prevalansı

Bal arılarını infekteleyen virüsler dünyanın her yerinde bal arılarının her gelişim evresinde infeksiyona neden olan ve ekonomik zarara yol açan hastalıklardır. Bu araştırmada dünya çapında yaygın olan iki bal arısı virüsünün (deforme kanat virüsü [DWV] ve kronik arı paraliz virüsü [CBPV]) varlığı ve yaygınlığını belirlemek için bir survey çalışması gerçekleştirilmiştir. Viral RNA’yı belirlemek amacıyla Bingöl ili sınırlarındaki 9 farklı lokaliteden toplam 128 arılık ziyaret edilmiştir. Toplanan 384 bal arısı örneği her virüse özgü genom spesifik primerler kullanılarak moleküler olarak (revers-transkriptaz polimeraz zincir reaksiyonu, RT-PCR) testlenmiştir. 128 arılığın 28’i (%21.87) DWV için pozitif reaksiyon vermiştir fakat hiçbir arılıkta CBPV patojeni tespit edilmemiştir. Pozitif örneklerden rastgele seçilen birinin klonlanarak ortaya çıkarılan 702 bazlık nükleotit dizisi gen bankasına MZ357973 ulaşım numarasıyla kaydedilmiştir. NCBI veri tabanındaki BLASTn analizine göre, Bingöl ilinde belirlenen DWV etmeninin nükleotit dizisi aynı virüsün diğer izolatlarıyla kıyaslandığında %77.82-98.45 arasında değişen nükleotit benzerliği göstermiştir. Ayrıca, farklı orijinlerden izolatların kullanıldığı filogenetik ağaca dayanarak bizim izolatımız Türkiye’den ErzincanDWV izolatıyla yakın filogenetik ilişki içerisinde olduğu tespit edilmiştir. Literatür taramalarına göre, bu çalışma Bingöl ilinde DWV ve CBPV yaygınlığını ve varlığını DNA temelli yöntemlerle ortaya koyan ilk kayıt niteliğindedir

Anahtar Kelimeler:

DWV, CBPV, Yayılım, Türkiye, Apis mellifera

Prevalence of Deformed wing virus and Chronic bee paralysis virus in Honey Bee Colonies of Bingöl province, Turkey

Viruses infecting honey bees are diseases that cause infection and economic damage in every developmental stage of honey bees all over the world. In this study, a survey was conducted to determine the presence and prevalence of two worldwide common honeybee viruses (deformed wing virus [DWV] and chronic bee paralysis virus [CBPV]). 128 apiaries from 9 different localities in the province of Bingöl were visited to determine viral RNA. Collected 384 honey bee samples were tested molecularly (reverse-transcriptase polymerase chain reaction, RTPCR) using genome-specific primers specific to each virus. In molecular tests, 28 of 128 apiaries (21.87%) gave a positive reaction for DWV, but no CBPV pathogen was detected in any apiary. The 711 bp nucleotide sequence revealed by cloning one of the randomly selected positive samples was registered in the gene bank with the accession number MZ357973. According to the BLASTn analysis in the NCBI database, the nucleotide sequence of the DWV agent determined in Bingöl Province showed nucleotide similarity between 77.82-98.45% when compared to other isolates of the same virus. In addition, our isolate was found to be in a close phylogenetic relationship with the Erzincan-DWV isolate from Turkey, based on the phylogenetic tree using isolates from different origins. According to our literature screening, this study is the first record that reveals the prevalence and the presence of DWV and CBPV in Bingöl Province with DNA-based approaches.

Keywords:

DWV, CBPV, Turkey, Apis mellifera, Prevelence,

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Adams, M. J., Lefkowitz, E. J., King, A. M. Q., & Carstens, E. B. (2014). Recently agreed changes to the statutes of the international committee on taxonomy of viruses. Archives of Virology, 159, 175-180.
Ai, H., Yan, X., & Han, R. (2012). Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. Journal of invertebrate pathology, 109(1), 160-164.
Allen MF, Ball BV, 1996. The incidence and world distribution of honey bee viruses. Bee World, 77: 141–162.
Antúnez, K., Anido, M., Garrido-Bailon, E., Botias, C., Zunino, P., Martínez-Salvador, A., ... & Higes, M. (2012). Low prevalence of honeybee viruses in Spain during 2006 and 2007. Research in Veterinary Science, 93(3), 1441-1445.
Avalos, J., Rosero, H., Maldonado, G., & Reynaldi, F. J. (2019). Honey bee louse (Braula schmitzi) as a honey bee virus vector?. Journal of Apicultural Research, 58(3), 427-429.
Ayşegül, U.S.T.A., & Yıldırım, Y. (2022). Investigation of deformed wing virus, black queen cell virus and acute bee paralysis virus infections by using reverse transcriptase-polymerase chain reaction (RT-PCR) technique in honey bees. Ankara Üniversitesi Veteriner Fakültesi Dergisi. https://doi.org/10.33988/auvfd.824882.
Bacandritsos, N., Granato, A., Budge, G., Papanastasiou, I., Roinioti, E., Caldon, M., ... & Mutinelli, F. (2010). Sudden deaths and colony population decline in Greek honey bee colonies. Journal of invertebrate pathology, 105(3), 335-340.
Bailey, L., Ball, B. V., & Perry, J. N. (1981). The prevalence of viruses of honey bees in Britain. Annals of Applied Biology, 97(1), 109-118.
Bailey L, Ball BV, 1991. Honeybee pathology. Academic Press, London, United Kingdom.
Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., & Nowotny, N. (2006). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and environmental microbiology, 72(4), 2414-2420.
Budge, G. E., Simcock, N. K., Holder, P. J., Shirley, M. D., Brown, M. A., Van Weymers, P. S., ... & Rushton, S. P. (2020). Chronic bee paralysis as a serious emerging threat to honey bees. Nature Communications, 11(1), 2164.
ÇAĞIRGAN, A. A., & Yazici, Z. (2021). The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and theirphylogenetic analysis. Turkish Journal of Veterinary & Animal Sciences, 45(1), 44-55..
Cagirgan, A. A., Yildirim, Y., & Usta, A. (2020). Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medycyna Weterynaryjna, 76(08)..
Celle, O., Blanchard, P., Olivier, V., Schurr, F., Cougoule, N., Faucon, J. P., & Ribière, M. (2008). Detection of Chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread. Virus research, 133(2), 280-284..
Chen, G., Wu, Y., Deng, J., Wen, Z., Wang, S., Chen, Y., ... & Zheng, H. (2021). Seasonal variation of viral infections between the eastern honey bee (Apis cerana) and the western honey bee (Apis mellifera). Microbiologyopen, 10(1), e1162.
Chen, Y. (2011). Viruses and viral diseases of the honey bee, Apis mellifera. Recent Advances in Entomological Research: From Molecular Biology to Pest Management, 105-120.
Chen, Y., Smith, I. B., Collins, A. M., Pettis, J. S., & Feldlaufer, M. F. (2004). Detection of deformed wing virus infection in honey bees, Apis mellifera L., in the United States. American Bee Journal, 144(7), 557-559..
De Miranda, J. R., & Genersch, E. (2010). Deformed wing virus. Journal of invertebrate pathology, 103, S48-S61..
De Miranda, J. R., & Fries, I. J. J. O. I. P. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of invertebrate pathology, 98(2), 184-189.
Desai, S. D., Eu, Y. J., Whyard, S., & Currie, R. W. (2012). Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double‐stranded RNA ingestion. Insect molecular biology, 21(4), 446-455.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L. P., Decourtye, A., Kretzschmar, A., ... & Alaux, C. (2013). Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter?. PloS one, 8(8), e72016.
Dolezal, A. G., Hendrix, S. D., Scavo, N. A., Carrillo-Tripp, J., Harris, M. A., Wheelock, M. J., ... & Toth, A. L. (2016). Honey bee viruses in wild bees: viral prevalence, loads, and experimental inoculation. PloS one, 11(11), e0166190.
Eyer, M., Chen, Y. P., Schäfer, M. O., Pettis, J., & Neumann, P. (2009). Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie, 40(4), 419-428.
Svanella-Dumas, L., Dulucq, M. J., Candresse, T., Gentit, P., & Foissac, X. (2000, July). Polyvalent detection of fruit tree tricho, capillo and foveaviruses by nested RT-PCR using degenerated and inosine containing primers (PDO RT-PCR). In XVIII International Symposium on Virus and Virus-like Diseases of Temperate Fruit Crops-Top Fruit Diseases 550 (pp. 37-44).
Forsgren, E., De Miranda, J. R., Isaksson, M., Wei, S., & Fries, I. (2009). Deformed wing virus associated with Tropilaelaps mercedesae infesting European honey bees (Apis mellifera). Experimental and Applied Acarology, 47, 87-97.
Gauthier, L., Tentcheva, D., Tournaire, M., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2007). Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie, 38(5), 426-435.
Genersch, E., & Aubert, M. (2010). Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Veterinary research, 41(6).
Güller, A., Mustafa, U. S. T. A., Çakar, G., & Zeynelabidin, K. U. R. T. (2021). Molecular characterization of Deformed wing viruses identified in honeybee (Apis mellifera L.) colonies in Erzincan province of Turkey. Avrupa Bilim ve Teknoloji Dergisi, (27), 186-192.
Gülmez, Y., Bursalı, A., & Tekin, S. (2009). First molecular detection and characterization of deformed wing virus (DWV) in honeybees (Apis mellifera L.) and mite (Varroa destructor) in Turkey. African Journal of Biotechnology, 8(16).
Okur Gumusova, S., Albayrak, H., Kurt, M., & Yazici, Z. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6), 779-785.
Haddad, N., Al-Gharaibeh, M., Nasher, A., Anaswah, E., Alammari, Y., & Horth, L. (2018). Scientific note: molecular detection of pathogens in unhealthy colonies of Apis mellifera jemenitica. Apidologie, 49(1), 84-88.
Haddad, N., Brake, M., Migdadi, H., & de Miranda, J. R. (2008). First detection of honey bee viruses in Jordan by RT-PCR. Jordan Journal of Agricultural Sciences, 4(3), 242-247.
Highfield, A., Kevill, J., Mordecai, G., Hunt, J., Henderson, S., Sauvard, D., ... & Schroeder, D. C. (2020). Detection and replication of Moku virus in honey bees and social wasps. Viruses, 12(6), 607.
Kalayci, G., Cagirgan, A. A., Kaplan, M., Pekmez, K., Beyazit, A., Ozkan, B., ... & Arslan, F. (2020). The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 26(5).
Karapınar, Z., Oğuz, B., Dinçer, E., & Öztürk, C. (2018). Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. Medycyna Weterynaryjna, 74 (7), 460-465.
Kutlu, M.A. & Ekmen, F. (2003). Presence of Nosema disease and infection rate in honey bees (Apis mellifera L.) in Bingöl region. Technical Beekeeping, 79: 24-26.
Kutlu, M. A. & Gül, A. (2020). Bingöl ilinde yaşanan koloni kayıpları (arı ölümleri), nedenleri ve öneriler. Türk Tarım ve Doğa Bilimleri Dergisi, 7(4), 867-873.
Li, Z., Huang, S., Huang, W. F., Geng, H., Zhao, Y., Li, M., ... & Su, S. (2016). A scientific note on detection of honeybee viruses in the darkling beetle (Alphitobius diaperinus, Coleoptera: Tenebrionidae), a new pest in Apis cerana cerana colonies. Apidologie, 47, 759-761.
Li, B., Deng, S., Yang, D., Hou, C., & Diao, Q. (2017). Complete sequences of the RNA 1 and RNA 2 segments of chronic bee paralysis virus strain CBPV-BJ detected in China. Archives of virology, 162, 2451-2456.
Martin, S. J., & Brettell, L. E. (2019). Deformed wing virus in honeybees and other insects. Annual review of virology, 6, 49-69.
Mockel, N., Gisder, S., & Genersch, E. (2011). Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. Journal of General Virology, 92(2), 370-377.
Mutinelli, F. (2011). The spread of pathogens through trade in honey bees and their products (including queen bees and semen): overview and recent developments. Revue Scientifique et Technique-OIE, 30(1), 257.
Nielsen, S. L., Nicolaisen, M., & Kryger, P. (2008). Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie, 39(3), 310-314.
Porrini, C., Mutinelli, F., Bortolotti, L., Granato, A., Laurenson, L., Roberts, K., ... & Lodesani, M. (2016). The status of honey bee health in Italy: Results from the nationwide bee monitoring network. PLoS One, 11(5), e0155411.
Posada-Florez, F., Childers, A. K., Heerman, M. C., Egekwu, N. I., Cook, S. C., Chen, Y., ... & Ryabov, E. V. (2019). Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Scientific reports, 9(1), 12445.
Reynaldi, F. J., Sguazza, G. H., Albicoro, F. J., Pecoraro, M. R., & Galosi, C. M. (2013). First molecular detection of co-infection of honey bee viruses in asymptomatic Bombus atratus in South America. Brazilian journal of biology, 73, 797-800.
Ribière, M., Triboulot, C., Mathieu, L., Aurières, C., Faucon, J. P., & Pépin, M. (2002). Molecular diagnosis of chronic bee paralysis virus infection. Apidologie, 33(3), 339-351.
Rodríguez, M., Vargas, M., Antúnez, K., Gerding, M., Ovídio Castro, F., & Zapata, N. (2014). Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean journal of agricultural research, 74(2), 170-177.
Rüstemoğlu, M., & Sipahioğlu, H. M. (2016). Occurrence and molecular characterization of acute bee paralysis virus (ABPV) in honeybee (Apis mellifera) colonies in Hakkari province. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi. 26 (2), 174 – 182.
Rüstemoğlu, M. (2019). Uluslararası Arıcılık Araştırmaları ve Sürdürülebilir Kırsal Kalkınma Stratejileri Kongresi. 11-13 Ekim 2019. Bingöl, Türkiye.
Rüstemoğlu, M., & Sipahioğlu, H. M. (2019). Occurrence and prevalence of six honey bee viruses in Hakkari (Turkey) and their genomic divergence. Munis Entomology & Zoology, 14(2), 574-583.
Rüstemoğlu, M. (2020). Isolation And Characterization Of Two Important Honeybee-Killing Virus Species, Deformed Wing Virus (Dwv) And Black Queen Cell Virus (Bqcv) From Messor concolor Ants (Hymenoptera: Formicidae). Applied Ecology and Environmental Research. 18(5):7407-7415.
Sanpa, S., & Chantawannakul, P. (2009). Survey of six bee viruses using RT-PCR in Northern Thailand. Journal of Invertebrate Pathology, 100(2), 116-119.
Simeunović, P., Stevanović, J., Vidanović, D., Nišavić, J., Radović, D., Stanišić, L., & Stanimirović, Z. (2014). A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from Serbia using real-time RT-PCR. Acta Veterinaria, 64(1), 81-92.
Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2004). Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and environmental microbiology, 70(12), 7185-7191.
Toplak, I., Jamnikar Ciglenečki, U., Aronstein, K., & Gregorc, A. (2013). Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses, 5(9), 2282-2297.
Traiyasut, P., Mookhploy, W., Kimura, K., Yoshiyama, M., Khongphinitbunjong, K., & Chantawannakul, P. (2016). First detection of honey bee viruses in wax moth. Chiang Mai Journal of Science, 43(4).
Traynor, K. S., Rennich, K., Forsgren, E., Rose, R., Pettis, J., Kunkel, G., ... & Vanengelsdorp, D. (2016). Multiyear survey targeting disease incidence in US honey bees. Apidologie, 47, 325-347.
Teixeira, E. W., Chen, Y., Message, D., Pettis, J., & Evans, J. D. (2008). Virus infections in Brazilian honey bees. Journal of Invertebrate Pathology, 99(1), 117-119.
Yang X , Cox-Foster D, 2007. Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology, 134:405.