Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States

Honey bee samples collected between 1995 and 2007 from 12 states were examined for the presence of Nosema infections. Our results showed that Nosema ceranae is a wide-spread infection of the European honey bee, Apis mellifera in the United States. The discovery of N. ceranae in bees collected a decade ago indicates that N. ceranae was transferred from its original host, Apis cerana to A. mellifera earlier than previously recognized. The spread of N. ceranae infection in A. mellifera warrants further epidemiological studies to identify conditions that resulted in such a widespread infection.     

Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera)

Nosema ceranae, a microsporidian parasite originally described in the Asian honey bee Apis cerana, has recently been found to be cross-infective and to also parasitize the European honey bee Apis mellifera. Since this discovery, many studies have attempted to characterize the impact of this parasite in A. mellifera honey bees. Nosema species can infect all colony members, workers, drones and queens, but the pathological effects of this microsporidium has been mainly investigated in workers, despite the prime importance of the queen, who monopolizes the reproduction and regulates the cohesion of the society via pheromones. We therefore analyzed the impact of N. ceranae on queen physiology. We found that infection by N. ceranae did not affect the fat body content (an indicator of energy stores) but did alter the vitellogenin titer (an indicator of fertility and longevity), the total antioxidant capacity and the queen mandibular pheromones, which surprisingly were all significantly increased in Nosema-infected queens. Thus, such physiological changes may impact queen health, leading to changes in pheromone production, that could explain Nosema-induced supersedure (queen replacement).     

Correlation of proteome-wide changes with social immunity behaviors provides insight into resistance to the parasitic mite, Varroa destructor, in the honey bee (Apis mellifera)

Background

Disease is a major factor driving the evolution of many organisms. In honey bees, selection for social behavioral responses is the primary adaptive process facilitating disease resistance. One such process, hygienic behavior, enables bees to resist multiple diseases, including the damaging parasitic mite Varroa destructor. The genetic elements and biochemical factors that drive the expression of these adaptations are currently unknown. Proteomics provides a tool to identify proteins that control behavioral processes, and these proteins can be used as biomarkers to aid identification of disease tolerant colonies.

Results

We sampled a large cohort of commercial queen lineages, recording overall mite infestation, hygiene, and the specific hygienic response to V. destructor. We performed proteome-wide correlation analyses in larval integument and adult antennae, identifying several proteins highly predictive of behavior and reduced hive infestation. In the larva, response to wounding was identified as a key adaptive process leading to reduced infestation, and chitin biosynthesis and immune responses appear to represent important disease resistant adaptations. The speed of hygienic behavior may be underpinned by changes in the antenna proteome, and chemosensory and neurological processes could also provide specificity for detection of V. destructor in antennae.

Conclusions

Our results provide, for the first time, some insight into how complex behavioural adaptations manifest in the proteome of honey bees. The most important biochemical correlations provide clues as to the underlying molecular mechanisms of social and innate immunity of honey bees. Such changes are indicative of potential divergence in processes controlling the hive-worker maturation.     

Uncovering the novel characteristics of Asian honey bee,Apis cerana,by whole genome sequencing

Background

The honey bee is an important model system for increasing understanding of molecular and neural mechanisms underlying social behaviors relevant to the agricultural industry and basic science. The western honey bee, Apis mellifera, has served as a model species, and its genome sequence has been published. In contrast, the genome of the Asian honey bee, Apis cerana, has not yet been sequenced. A. cerana has been raised in Asian countries for thousands of years and has brought considerable economic benefits to the apicultural industry. A cerana has divergent biological traits compared to A. mellifera and it has played a key role in maintaining biodiversity in eastern and southern Asia. Here we report the first whole genome sequence of A. cerana.

Results

Using de novo assembly methods, we produced a 238 Mbp draft of the A. cerana genome and generated 10,651 genes. A.cerana-specific genes were analyzed to better understand the novel characteristics of this honey bee species. Seventy-two percent of the A. cerana-specific genes had more than one GO term, and 1,696 enzymes were categorized into 125 pathways. Genes involved in chemoreception and immunity were carefully identified and compared to those from other sequenced insect models. These included 10 gustatory receptors, 119 odorant receptors, 10 ionotropic receptors, and 160 immune-related genes.

Conclusions

This first report of the whole genome sequence of A. cerana provides resources for comparative sociogenomics, especially in the field of social insect communication. These important tools will contribute to a better understanding of the complex behaviors and natural biology of the Asian honey bee and to anticipate its future evolutionary trajectory.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-16-1) contains supplementary material, which is available to authorized users.     

Performance evaluation of indigenous and exotic honey bee (Apis mellifera L.) races in Assir region,southwestern Saudi Arabia

This study was conducted in the Assir region of southwestern Saudi Arabia to compare the activities of honeybee colonies of indigenous Apis mellifera jemenitica (AMJ) and imported Apis mellifera carnica (AMC) during the late summer and autumn of 2009 and 2010. The results showed that the workers of the two races exhibited relatively similar forage timings throughout the period of study (August–November). The highest numbers of foraged workers were recorded at 6:00 am, 10:00 am and 6:00 pm, while the lowest numbers were recorded at 8:00 am, 12:00 pm and 4:00 pm. Although foraging activity was negatively affected by decreased temperature, AMJ was more resistant to cold than AMC. In the first season, the smallest amount of worker brood rearing was recorded in August, and the highest amount of rearing occurred in November in both races. In the second season, the smallest amount of brood was observed in October, and the largest amount of brood was observed in November. Brood rearing and pollen collecting was significantly (P < 0.05) higher in AMJ compared with AMC, while AMC stored significantly (P < 0.05) more honey than AMJ during the tested periods. In AMJ colonies, a positive significant correlation was observed between the area of the sealed worker brood and stored pollen, while a negative but nonsignificant correlation was observed between the area of the sealed worker brood and surplus honey. In the AMC colonies, a positive significant correlation was observed between the area of the sealed brood and the stored pollen and surplus honey.     

Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera

Background

Long non-coding RNAs (lncRNAs) are a class of RNAs that do not encode proteins. Recently, lncRNAs have gained special attention for their roles in various biological process and diseases.

Results

In an attempt to identify long intergenic non-coding RNAs (lincRNAs) and their possible involvement in honey bee development and diseases, we analyzed RNA-seq datasets generated from Asian honey bee (Apis cerana) and western honey bee (Apis mellifera). We identified 2470 lincRNAs with an average length of 1011 bp from A. cerana and 1514 lincRNAs with an average length of 790 bp in A. mellifera. Comparative analysis revealed that 5 % of the total lincRNAs derived from both species are unique in each species. Our comparative digital gene expression analysis revealed a high degree of tissue-specific expression among the seven major tissues of honey bee, different from mRNA expression patterns. A total of 863 (57 %) and 464 (18 %) lincRNAs showed tissue-dependent expression in A. mellifera and A. cerana, respectively, most preferentially in ovary and fat body tissues. Importantly, we identified 11 lincRNAs that are specifically regulated upon viral infection in honey bees, and 10 of them appear to play roles during infection with various viruses.

Conclusions

This study provides the first comprehensive set of lincRNAs for honey bees and opens the door to discover lincRNAs associated with biological and hormone signaling pathways as well as various diseases of honey bee.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1868-7) contains supplementary material, which is available to authorized users.     

Effects of soybean trypsin inhibitor on hypopharyngeal gland protein content, total midgut protease activity and survival of the honey bee (Apis mellifera L.)

Insecticidal properties of protease inhibitors have been established in transgenic plants. In the wake of continuous research and rapid development of protease inhibitors it is important to assess possible effects on beneficial insects like the honey bee (Apis mellifera L.). In this study, newly emerged caged bees were fed pollen diets containing three different concentrations (0.1%, 0.5% and 1% w:w) of soybean trypsin inhibitor (SBTI). Hypopharyngeal gland protein content, total midgut proteolytic enzyme activity of these bees, and survival were measured. Bees fed 1% SBTI had significantly reduced hypopharyngeal gland protein content and midgut proteolytic enzyme activity. There were no significant differences between control, 0.1% and 0.5% SBTI treatments. Bees fed a diet containing 1% SBTI had the lowest survival, followed by 0.5% and 0.1%, over a 30-day period. We concluded that nurse bees fed a pollen diet containing at least 1% SBTI would be poor producers of larval food, potentially threatening colony growth and maintenance.     

Dose-dependent inhibition of emergency queen rearing by synthetic 9-ODA in the honey bee,Apis mellifera carnica

In the honey bee colony queen rearing is usually suppressed by releaser effects of the queen's pheromone. This is part of the dominance hierarchy maintaining the monogynous homeostasis. Under queenless conditions, the queen's control over the construction of emergency queen cells by the workers can be substitued by exposure to only one component of the mandibular pheromone secretion of a queen, the main compound (E)-9-oxo-2-decenoic acid. A novel and simple synthesis of (E)-9-oxo-2-decenoic acid is described, and a bioassay was developed by which a dose-dependent effect of synthetic (E)-9-oxo-2-decenoic acid presented on a dummy bee was evaluated.Abbreviation 9-ODA (E)-9-oxo-2-decenoic acid In memoriam Viktor Schwartz (1907–1992), Professor of Zoology and Developmental Biology, University of Tübingen, who introduced smoothened bee stings into microsurgery     

The indigenous honey bees of Saudi Arabia (Hymenoptera, Apidae, Apis mellifera jemenitica Ruttner): Their natural history and role in beekeeping

Apis mellifera jemenitica Ruttner (= yemenitica auctorum: videEngel 1999) has been used in apiculture throughout the Arabian Peninsula since at least 2000 BC. Existing literature demonstrates that these populations are well adapted for the harsh extremes of the region. Populations of Apis mellifera jemenitica native to Saudi Arabia are far more heat tolerant than the standard races often imported from Europe. Central Saudi Arabia has the highest summer temperatures for the Arabian Peninsula, and it is in this region where only Apis mellifera jemenitica survives, while other subspecies fail to persist. The indigenous race of Saudi Arabia differs from other subspecies in the region in some morphological, biological, and behavioral characteristics. Further taxonomic investigation, as well as molecular studies, is needed in order to confirm whether the Saudi indigenous bee populations represent a race distinct from Apis mellifera jemenitica, or merely an ecotype of this subspecies.     

Ontogeny of rdh9 (Crad3) expression: Ablation causes changes in retinoid and steroid metabolizing enzymes,but RXR and androgen signaling seem normal

Crad3 (cis-retinol/androgen dehydrogenase 3), a short-chain dehydrogenase/reductase, converts 9-cis-retinol into 9-cis-retinal and 3α-androstanediol into dihydrotestosterone. Crad3 may serve in biosynthesis of 9-cis-retinoic acid, a putative RXR ligand, and/or regeneration of potent androgens. RT-PCR showed that expression of the gene that encodes Crad3, rdh9, begins in liver by e11.5, and in kidney, testis, brain and intestine during e15.5–e16.5. In situ hybridization showed rdh9 expression in embryonic liver, ganglia, small intestine, lung, skin and vertebral cartilage. In adult, in situ hybridization revealed rdh9 expression intensely in hepatocytes, weakly in kidney glomerulus, and intensely in collecting tubules. In intestine, undifferentiated epithelia had greater expression than differentiated epithelia at the distal villus end. Testes expressed rdh9 in spermatogonia, and weakly in Leydig cells. Adult brain expressed rdh9 in the dentate gyrus and CA regions of the hippocampus, the cerebellum Purkinje cells, and the glomerular and mitral cell layers of the olfactory bulb. Rdh9-null mice, backcrossed against C57BL/6J mice, were born in Mendelian frequency, were healthy and fertile, and had normal tissue retinoid and serum dihydrotestosterone levels. Expression of rdh1, a gene that encodes an efficient retinol dehydrogenase, decreased 3- to 8-fold in rdh9-null mice, depending on dietary vitamin A. Microarray analysis and quantitative PCR revealed 2- to 4-fold increases in mRNA of enzymes that catalyze xenobiotic and steroid metabolism, including Cyp2, Cyp3, 11β-hydroxysteroid dehydrogenase type 2, and 17β-hydroxsteroid dehydrogenases types 4 and 5. These data indicate widespread Crad3 function(s) in steroid and/or retinoid metabolism starting mid embryogenesis.