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). By intensity-based label-free quantitation, 1,433 proteins were differentially expressed across developmental stages, including two distinct viral polyproteins. 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 (169 of which were differentially expressed) supported by 1,464 peptides which were previously unannotated. Since this is a recurring trend with annotating genomes of non-model species, we analyzed their amino acid and nucleotide composition as well as their orthology to other species to suggest reasons why they may have been missed initially. Overall, this work provides a first-of-its-kind interrogation of the patterns of gene expression that govern the Varroa life cycle and the tools we have developed will support further research on this threatening honey bee pest.