A Varroa destructor protein atlas reveals molecular underpinnings of developmental transitions and sexual differentiation

Abstract

Varroa destructor is the most economically damaging honey bee pest, weakening colonies by simultaneously parasitizing bees and transmitting harmful viruses. Despite these impacts on honey bee health, surprisingly little is known about its fundamental molecular biology. Here, we present a Varroa protein atlas crossing all major developmental stages (egg, protonymph, deutonymph, and adult) for both male and female mites as a web-based interactive tool (http://foster.nce.ubc.ca/varroa/index.html). We used intensity-based label-free quantitation to find 1,433 differentially expressed proteins across developmental stages. Enzymes for processing carbohydrates and amino acids were among many of these differences as well as proteins involved in cuticle formation. Lipid transport involving vitellogenin was the most significantly enriched biological process in the foundress (reproductive female) and young mites. In addition, we found that 101 proteins were sexually regulated and functional enrichment analysis suggests that chromatin remodeling may be a key feature of sex determination. In a proteogenomic effort, we identified 519 protein-coding regions, 301 of which were supported by two or more peptides and 169 of which were differentially expressed. Overall, this work provides a first-of-its-kind interrogation of the patterns of protein expression that govern the Varroa life cycle and the tools we have developed will support further research on this threatening honey bee pest.

2D-DIGE proteomic analysis reveals changes in haemolymph proteome of 1-day-old honey bee (Apis mellifera) workers in response to infection with Varroa destructor mites

“…Lipid transport involving vitellogenin (Vg) is the most significantly enriched biological process in the foundress (reproductive female) and in young mites (McAfee et al 2017), suggesting that honey bee Vg may be altered by Varroa infestation. However, in our study, no alteration of Vg was found in 1-day-old honey bee haemolymph after Varroa infestation.…”

“…Recently, proteomics analysis has been used in studies of Varroa destructor mites (Erban et al 2015;McAfee et al 2017;Iovinella et al 2018). Several groups of proteins were identified in Varroa females, as follows: (i) proteins of virions such as Varroa destructor Macula-like virus, DWV and acute bee paralysis virus (Erban et al 2015); (ii) a variety of honey bee haemolymph proteins, including apolipophorin, hexamerins and various major royal jelly proteins (Erban et al 2015); and (iii) key proteins that may act as semiochemical carriers, such as odorant-binding proteins and Niemann-Pick family, type C2 proteins (Iovinella et al 2018).…”

Transcriptome profiling of the honeybee parasite Varroa destructor provides new biological insights into the mite adult life cycle

“…For instance, transcriptomic analysis were performed on Varroa destructor synganglion [ 15 ] and foreleg (olfactory organ) [ 16 ]. A proteomic analysis was also performed on V. destructor , with a focus on the different developmental stages of the mite [ 17 ]. In addition, differential gene expression was investigated in V. jacobsoni with respect to the host on which they reproduce [ 18 ].…”

Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera)

“…We performed all further proteomics sample preparation steps exactly as previously described. 58 Briefly, we used urea digestion buffer to solubilize the protein, then reduced (dithiothreitol), alkylated (iodoacetamide), diluted with four volumes of 50 mM ammonium bicarbonate, digested (Lys-C for 3 h, then trypsin overnight), and desalted peptides using C18 STAGE tips made in-house. We suspended the desalted, dried peptides in Buffer A, then estimated peptide concentration by the absorbance at 280 nanometers (Nanodrop).…”