The Genetic Characterization of Lake Sinai Virus in Colony Losses Apiaries in Türkiye

Year 2024, Volume: 8 Issue: 2, 129 - 136, 25.10.2024

Dilek Muz , Mustafa Necati Muz

https://doi.org/10.47748/tjvr.1500593

Abstract

Objective: Honeybees (Apis mellifera) have a unique role in natural pollination and maintaining biodiversity in the ecosystem. The alarming increase in unexpected colony losses, mysterious bee deaths, and the tragic extinction of entire colonies (Colony collapsed disorder- CCD) have sounded a global alarm, demanding immediate attention and collaborative action to address these critical challenges in bee breeding. Diseases, parasites, and pathogens significantly threaten colony health. Türkiye is a significant honey producer, providing an ideal environment for beekeeping due to its unique eco-geographical features. Unexpected colony losses and bee deaths are also questions of concern for beekeepers in Türkiye.
Material Method: In this study investigated honey bee viruses in apiaries experiencing sudden bee death losses and CCD-like symptoms between 2021 and 2023 in Türkiye, involving genetic analysis of the LSV RdRp gene region. The honeybee and varroa samples were obtained from 52 colonies in 26 apiaries complaining of unexpected bee deaths and CCD-like symptoms between May 2021 and September 2023.
Result: The results showed a high DWV, BQCV, and LSV prevalence, respectively. The sampled apiaries were infested mild-moderate- high grade with Varroa mites. Following PCR results, DWV, BQCV, LSV, IAPV, CBPV, and SBV positivity was detected at 69.2% (n=18), 50% (n=13), 38.46% (n=10), 26.9% (n=7), 19.2% (n=5) and 3.8% (n=1), respectively. High rates of multiple virus coexisting and high varroa infestation were noted in colonies with heavy losses and CCD-like complaints. The RdRp gene from two LSV samples (TrLSV-6474, TrLSV-6517) was sequenced. Turkish LSV samples (TrLSVs) showed a 72.88% homology of each other and clustered LSV4 branches in the phylogenetic tree. Turkish LSV sequences showed a closer similarity rate than reference sequences in GenBank with Asian Korean, Chinese, and Japanese LSV sequences.
Conclusion: Further investigation is needed to comprehend the implications of elevated LSV populations on colony losses. The execution of genetic research with a more extensive sample size can significantly enhance the demonstration of species diversity and provide valuable insights into the influence of LSV variants on honeybee health and the management of diseases.

Keywords

Honeybee, Virus, Lake Sinai virus, RdRp gene

Ethical Statement

.

Supporting Institution

The authors declared that this study has received no financial support.

Project Number

.

Thanks

.

References

• Amakpe F, De Smet L, Brunain M, et al. Discovery of Lake Sinai virus and an unusual strain of acute bee paralysis virus in West African apiaries. Apidologie. 2016; 47:35-47.
• Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl Environ. Microbiol. 2006; 72(4):2414-20.
• Cepero A, Ravoet J, Gómez-Moracho T, et al. Holistic screening of collapsing honey bee colonies in Spain: A case study. BMC Res Notes. 2014; 7(1):649
• Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J, Feldlaufer M. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J Inverteb Pathol. 2004; 87(2-3):84-93.
• Cornman RS, Tarpy DR, Chen Y, et al. Pathogen webs in collapsing honey bee colonies. PLoS One. 2012; 7(6):e43562.
• Čukanová E, Moutelíková R, Prodělalová J. First detection of Lake Sinai virus in the Czech Republic: a potential member of a new species. Arch Virol. 2022; 167(11):2213-2222.
• Çağırgan AA, Kaplan M, Pekmez K, Arslan F. Türkiye’de Varroa akarlarında Lake Sinai Virus (LSV)’ un ilk tespiti. Atatürk Üniv Vet Bil Derg. 2022;17(1):16-19.
• D’Alvise P, Seeburger V, Gihring K, Kieboom M, Hasselmann M. Seasonal dynamics and co‐occurrence patterns of honey bee pathogens revealed by high‐throughput RT‐qPCR analysis. Ecol Evol. 2019; 9(18):10241-10252.
• Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Predictive Markers of Honey Bee Colony Collapse. PloS One. 2012; 7:0032151.
• Daughenbaugh KF, Martin M, Brutscher LM, et al. Honey bee infecting Lake Sinai viruses. Viruses. 2015; 7(6):3285-3309.
• Faurot-Daniels C, Glenny W, Daughenbaugh KF, McMenamin AJ, Burkle LA, Flenniken ML. Longitudinal monitoring of honey bee colonies reveals dynamic nature of virus abundance and indicates a negative impact of Lake Sinai virus 2 on colony health. PLoS One. 2020; 15(9):e0237544.
• Genersch E. Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol. 2010; 87:87-97.
• Genersch E, Aubert M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res. 2010; 41(6):54.
• Giray T, Kence M, Oskay D, Döke MA, Kence A. Scientific note: colony losses survey in Turkey and causes of bee deaths. Apidologie. 2010; 41;451-453.
• Glenny W, Cavigli I, Daughenbaugh KF, Radford R, Kegley SE, Flenniken ML. Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLoS One. 2017; 12:e0182814.
• Hou C, Liang H, Chen C, et al. Lake Sinai virus is a diverse, globally distributed but not emerging multi-strain honeybee virus. Mol Ecol. 2023; 32(14):3859-3871.
• Kalaycı G, Cagirgan AA, Kaplan, et al. The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Univ Vet Fac Derg. 2020; 26(5):671-677.
• Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980; 16:111-120.
• Klein AM, Vaissière BE, Cane JH, et al. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 2007; 274(1608):303-313.
• Martin SJ, Ball BV, Carreck NL. Te role of deformed wing virus in the initial collapse of varroa infested honey bee colonies in the UK. J Apic Res. 2013; 52:251-258.
• Mayack C, Hakanoğlu H. Honey bee pathogen prevalence and interactions within the Marmara Region of Turkey. Vet Sci. 2022; 9:573.
• McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Curr Opin Insect Sci. 2015; 8:121-129.
• Muz MN. Colony collapse disorder in honeybees. T Parazitol Derg. 2008; 32(3):271-275.
• Muz D, Muz MN. Survey of the occurrence of Deformed Wing Virus and multiple parasites of queens (Apis mellifera L.) in apiaries with collapsed colonies in Hatay, Turkey. J Apicult Res. 2009; 48(3):204-208.
• Muz D, Muz MN. Investigation of some pathogens "Colony Loss Syndrome" resembled losses apiaries in Tekirdağ. Kocatepe Vet J. 2017; 10(1):21-28.
• Muz MN, Özdemir N, Muz D. Global honeybee health and veterinary medicine. Bulletin of Veterinary Pharmacology and Toxicology Association. 2019; 10(1):24-30.
• Muz D, Muz MN. Investigation of honey bee colony losses in Thrace region. 4th International Eurasian Conference on Science, Engineering and Technology. December 14-16; 2022.
• Muz D, Muz MN. Israel Acute Bee Paralysis Virus prevalence in apiaries with colony loss in Türkiye. Uludağ Bee J. 2023a; 23(1):105-114.
• Muz D, Muz MN. Acute bee paralysis virus field isolates from apiaries suffering colony losses in Türkiye. J Apic Res. 2023b; 20:1-7.
• Neumann P, Carreck N. Honey bee colony losses. J Apicul Res. 2010; 49(1):1-6.
• Nguyen TT, Yoo MS, Truong AT, et al. Prevalence and genome features of lake sinai virus isolated from Apis mellifera in the Republic of Korea. PLoS One. 2024; 19(3):e0299558.
• Peck DT, Smith ML, Seeley TD. Varroa destructor mites can nimbly climb from flowers onto foraging honey bees. PLoS One. 2016; 11:e0167798.
• Palacios G, Hui J, Quan PL, et al. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol. 2008; 82(13):6209-6217.
• Ramsey SD, Ochoa R, Bauchan G, et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA. 2019; 116:1792-1801.
• Ravoet J, De Smet L, Wenseleers T, De Graaf DC. Genome sequence heterogeneity of Lake Sinai virus found in honey bees and Orf1/RdRP-based polymorphisms in a single host. Virus Res. 2015; 201:67-72.
• Rinkevich FD, Danka RG, Healy KB. Influence of Varroa mite (Varroa destructor) management practices on insecticide sensitivity in the honey bee (Apis mellifera). Insects. 2017; 8:9.
• Runckel C, Flenniken ML, Engel JC, et al. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One. 2011; 6(6):e20656.
• Ryabov EV, Wood GR, Fannon JM, et al. A virulent strain of Deformed Wing Virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathogens. 2014;10.
• Stoltz D, Shen XR, Boggis C, Sisson G. Molecular diagnosis of Kashmir bee virus infection. J Apicul Res. 1995; 34(3):153-160.
• Tamura K, Stecher G, Kumar S. MEGA 11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021; 38(7):3022-3027.
• Tozkar CO, Kence M, Kence A, Huang Q, Evans JD. Metatranscriptomic analyses of honey bee colonies. Front Genet. 2015; 6:100.
• Walker PJ, Siddell SG, Lefkowitz EJ, et al. Changes to virus taxonomy and the statutes ratified by the International Committee on Taxonomy of Viruses (2020). Arch Virol. 2020; 165(11):2737-2748.