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H SURREY the Food and Environment Research Agency Proquest Number: U583701 Epidemiology and Taxonomy of Honey Bee Viruses in England and Wales by Guido Cordoni Submitted for the degree of Doctor of Philosophy Faculty of Health and Medical Sciences University of Surrey August 2011 © Guido Cordoni 2011 ^ UNIVERSITY OF H fifa h SURREY The Food and Environment Research Agency ProQuest Number: U583701 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest U583701 Published by ProQuest LLO (2019). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLO. ProQuest LLO. 789 East Eisenhower Parkway P.Q. Box 1346 Ann Arbor, Ml 48106- 1346 This dissertation and the work to which it refers are the results of my own efforts. Any ideas, data, images or text resulting from the work of others (whether published or unpublished) are fully identified as such within the work and attributed to their originator in the text, bibliography or in footnotes. This thesis has not been submitted in whole or in part for any other academic degree or professional qualification. I agree that the University has the right to submit my work to a plagiarism detection service for originality checks. Contents Abstract 7 Acknowledgements 8 1 General introduction 10 1.1 Economic and environmental significance of honey bees 10 1.2 Basic honey bee biology 13 1.2.1 Life cycle 16 1.2.2 The nest 16 1.2.3 Honey bee defences against disease 16 1.3 Varroa destructor, an important vector of viral diseases 18 1.4 Colony Collapse Disorder (CCD) syndrome 21 1.5 Honey bee viruses 24 1.6 Dicisttvviridae, characteristics and genetics 29 1.6.1 Black queen cell virus (BQCV) 31 1.6.2 The Acute bee paralysis virus (ABPV)-Kashmir bee virus 31 (KBV)-Israeli acute paralysis virus (lAPV) complex 1.7 Iflaviridae characteristics and genetics 37 1.7.1 Sacbrood virus (SBV) 37 1.7.2 Deformed wing virus (DWV), Varroa destructor virus (VDV- 40 1) and Kakugo virus (KV) 1.7.3 Slow bee paralysis virus (SBPV) 43 1.8 Unassigned virus characteristics and genetics 44 1.9 Honey bee virus diagnostics 49 1.9.1 Serology 50 1.9.1.1 Protein Profile 50 1.9.1.2 Agarose Gel Immuno-diffusion (AGID) 51 1.9.1.3 Enzyme Linked Immuno Sorbent Assay (ELISA) 51 1.9.2 Molecular biology 52 1.9.2.1 Reverse Transcriptase PCR (rt-PCR) 53 1.9.2.2 Real Time rt-PCR (rt-PCR) 53 1.9.2.3 Microarrays 54 1.9.2.4 Sanger sequencing 55 1.9.2.5 Pyrosequencing 55 1.10 Aims of this research 56 2 General materials and methods 58 2.1 Virus propagation in white-eyed pupae 58 2.2 Total RNA extraction using GITC, paramagnetic beads and a 59 Kingfisher ML® Total Nucleic Acid (TNA) extraction machine 2.3 Agarose gel electrophoresis 60 2.4 Gel extraction / purification of PCR products 60 2.5 Concentration of PCR products 60 2.6 Virus purification in sucrose gradients 61 2.7 Transmission electron microscopy (TEM) 62 2.8 Honey bees sampling plan 62 2.8.1 Sampling Protocol 63 2.8.2 Sample size calculation 67 3 A viral RNA extraction method to detect low prevalence 69 viruses Introduction 69 Material and methods 70 3.1 Comparison of FERA total nucleic acid extraction method with 70 new RNA extraction method 3.2 Serial RNA extractions using Kingfisher ML TNA extraction 72 machine Results 72 3.3 PepMV T.E.M and Real Time rt-PCR 72 3.4 Comparison between GITC method and virus precipitation 73 method 3.5 Serial RNA extractions using Kingfisher ML TNA extraction 73 machine Discussion 74 4 Distribution and prevalence of honeybee viruses in UK 80 Introduction 80 Materials and methods 80 4.1 Primer design 80 4.2 Real Time rt-PCR analysis 81 4.3 Analysis of the results 82 Results 88 4.4 Prevalence of honey bee virus in England and Wales 88 4.5 Distribution of honey bee viruses in England and Wales 89 4.6R4LY form and symptoms reported by bee inspectors 89 Discussion 94 5 Detection, sequencing and characterization of honeybee 99 viruses Introduction 100 Materials and methods 100 5.1 rt-PCR primers design 100 5.2 Samples analysed 103 5,3 Reaction details 103 5.4 Software used and parameters applied 107 Results 108 5.5 characterisation of samples found positive for DWV/VDV- 108 1/KBV and BQCV using the classical rt-PCR 5.5.1 Assay validation 108 5.5.2 DWV/VDV-1 /KV it PCR characterisation 108 5.5.3 BQCV rt-PCR characterisation 109 5.6 Bio-informatic analysis of the DWV/VDV-1 /KBV and BQCV 114 sequences found using the classical rt-PCR 5.6.1 DWV/VDV-1 /KV sequence analysis 114 5.6.1.1 RdRp nucleotide sequences analysis 114 5.6.1.2 capsid nucleotide sequence analysis 117 5.6.2 BQCV sequence analysis 121 5.6.2.1 RdRp nucleotide sequence analysis 121 5.6.2.2 Capsid nucleotide sequence analysis 121 Discussion 127 5.7 Assay validation and DWV/VDV-1 /KV characterisation 127 5.8 Assay validation and BQCV characterisation 128 5.9 Analysis of the negative samples from Real Time rt-PCR 128 5.10 DWV/VDV-1 /KV and BQCV sequences analysis and 129 distribution maps 5.10.1 D WV/VDV-1 /KV sequence ^alysis and distribution 130 maps 5.10.2 BQCV sequence analysis and distribution maps 134 6 Overall discussion and future perspectives 136 6.1 Design an extensive sampling plan that could give a statistically 136 representative snapshot of the prevalence and distribution of honey bee viruses in England and Wales 6.2 Set up a viral RNA extraction method that could lead to the 140 isolation of RNA of rare viruses (e.g. KBV or SBPV) 6.3 Analyse all the samples for each virus by Real Time rt-PCR and 142 calculate the prevalence and the distribution of the viruses found using Geographical Information System (GIS) tools 6.4 Characterise some of the samples using classic rt-PCR followed by 144 sequencing or pyrosequencing 6.5 Future perspective ......................................................... 1.45 References 148 Appendix I 162 Appendix 11 166 Publications 172 Abstract Honey bees play a fundamental role in agriculture producing wealth in terms of hive products (honey, royal jelly, pollen, wax, and propolis) and by increasing the productivity of important plant species through pollination. Moreover, the pollination of natural plants, at the base of the food chain for many wild animals, guarantee their survival . So for the role that honey bees have in nature and for their economical import^ce in agriculture, their diseases are of paramount importance. Unfortunately, in the last few years a large-scale colony loss called Colony Collapse Disorder syndrome reduced the overall number of hives in different countries. However, the cause of this is still not clear and for this reason the Department for Environment, Food and Rural affairs . (DEFRA) funded this research in order to gain a better knowledge of honey bee virus epidemiology and taxonomy in England and Wales. A National level sampling plan w ^ designed to be statistically representative of the honey bee population present in England and Wales. In order to detect viruses at low prevalence level, a new viral RNA extraction method based on virus precipitation was developed and the viral RNAs obtained were screened for eight honey bee viruses using Real Time rt-PCR. Once information about thé prevalence and the distribution of the eight honey bee viruses was obtained, à further characterisation of Deformed wing virus DWV and Black queen cell virus BQCV was performed using classic rt-PCR coupled with Sanger sequencing, and phylogenetic trees were obtained using bioinformatic tools. The viruses, grouped according to their nucleotide siniilarity, were reported on a geographically referenced map in order to highlight the distribution of the yari^ts found in England and Wales. The results obtained in this thesis have resulted in a better knowledge of the epidemiology and taxonomy of honey bee viruses, determination of the full sequence of Slow paralysis virus SBPV for the first time, and a new virus RNA extraction method that can be exploited in other research fields. Acknowledgements In first instance I would like to thank my supervisors Giles Budge and Lisa Roberts because they have been very helpful and always present when I needed their precious help. Giles has been a real guide, particularly during my induction at FERA, teaching me many of the laboratory techniques that I used in this research. I remember with pleasure our daily scientific discussions that, being based on our different backgrounds, turned to be a point of strength to shape the research into a multidisciplinary approach. I thank Lisa because she accepted the challenge to have me as her student when my previous supervisor Mike Carter left the university. I have appreciated the effort she made supervising me, as I know that she already had many students to supervise. She is an excellent supervisor, giving me useful suggestions and correcting scrupulously my thesis. In the first year of my PhD Mike Carter gave me advice and training in virology that helped me to define the aims of this research.
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