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Multiple combinations of RDL subunits diversify the repertoire of GABA receptors in the honey bee parasite Varroa destructor.

ABSTRACT: In insects, ?-aminobutyric acid (GABA) is the major inhibitory neurotransmitter, and GABA-gated ion channels are the target of different classes of insecticides, including fipronil. We report here the cloning of six subunits (four RDL, one LCCH3, and one GRD) that constitute the repertoire of the GABA-gated ion channel family of the Varroa mite (Varroa destructor), a honey bee ectoparasite. We also isolated a truncated GRD subunit with a premature stop codon. We found that when expressed in Xenopus laevis oocytes, three of the four RDL subunits (VdesRDL1, VdesRDL2, and VdesRDL3) formed functional, homomultimeric anionic receptors, whereas GRD and LCCH3 produced heteromultimeric cationic receptors. These receptors displayed specific sensitivities toward GABA and fipronil, and VdesRDL1 was the most resistant to the insecticide. We identified specific residues in the VdesRDL1 pore-lining region that explain its high resistance to fipronil. VdesRDL4 did not form a functional receptor when expressed alone, but it assembled with VdesRDL1 to form a heteromultimeric receptor with properties distinct from those of the VdesRDL1 homomultimeric receptor. Moreover, VdesRDL1 physically interacted with VdesRDL3, generating a heteromultimeric receptor combining properties of both subunits. On the other hand, we did not detect any functional interaction between VdesLCCH3 and the VdesRDL subunits, an observation that differed from what was previously reported for Drosophila melanogaster In conclusion, this study provides insights relevant to improve our understanding of the precise role of GABAergic signaling in insects and new tools for the development of Varroa mite-specific insecticidal agents that do not harm honey bees.

SUBMITTER: Menard C

PROVIDER: S-EPMC6295728 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Multiple combinations of RDL subunits diversify the repertoire of GABA receptors in the honey bee parasite Varroa destructor.

Ménard Claudine C Folacci Mathilde M Brunello Lorène L Charreton Mercedes M Collet Claude C Mary Rosanna R Rousset Matthieu M Thibaud Jean-Baptiste JB Vignes Michel M Charnet Pierre P Cens Thierry T

The Journal of biological chemistry 20181017 49

In insects, γ-aminobutyric acid (GABA) is the major inhibitory neurotransmitter, and GABA-gated ion channels are the target of different classes of insecticides, including fipronil. We report here the cloning of six subunits (four RDL, one LCCH3, and one GRD) that constitute the repertoire of the GABA-gated ion channel family of the Varroa mite (Varroa destructor), a honey bee ectoparasite. We also isolated a truncated GRD subunit with a premature stop codon. We found that when exp ...[more]

PMID: 30333227

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Project description:BACKGROUND: Recent elevated winter loss of honey bee colonies is a major concern. The presence of the mite Varroa destructor in colonies places an important pressure on bee health. V. destructor shortens the lifespan of individual bees, while long lifespan during winter is a primary requirement to survive until the next spring. We investigated in two subsequent years the effects of different levels of V. destructor infestation during the transition from short-lived summer bees to long-lived winter bees on the lifespan of individual bees and the survival of bee colonies during winter. Colonies treated earlier in the season to reduce V. destructor infestation during the development of winter bees were expected to have longer bee lifespan and higher colony survival after winter. METHODOLOGY/PRINCIPAL FINDINGS: Mite infestation was reduced using acaricide treatments during different months (July, August, September, or not treated). We found that the number of capped brood cells decreased drastically between August and November, while at the same time, the lifespan of the bees (marked cohorts) increased indicating the transition to winter bees. Low V. destructor infestation levels before and during the transition to winter bees resulted in an increase in lifespan of bees and higher colony survival compared to colonies that were not treated and that had higher infestation levels. A variety of stress-related factors could have contributed to the variation in longevity and winter survival that we found between years. CONCLUSIONS/SIGNIFICANCE: This study contributes to theory about the multiple causes for the recent elevated colony losses in honey bees. Our study shows the correlation between long lifespan of winter bees and colony loss in spring. Moreover, we show that colonies treated earlier in the season had reduced V. destructor infestation during the development of winter bees resulting in longer bee lifespan and higher colony survival after winter.

Project description:BACKGROUND: The parasitic mite, Varroa destructor, is the most serious pest of the western honey bee, Apis mellifera, and has caused the death of millions of colonies worldwide. This mite reproduces in brood cells and parasitizes immature and adult bees. We investigated whether Varroa infestation induces changes in Apis mellifera gene expression, and whether there are genotypic differences that affect gene expression relevant to the bee's tolerance, as first steps toward unravelling mechanisms of host response and differences in susceptibility to Varroa parasitism. RESULTS: We explored the transcriptional response to mite parasitism in two genetic stocks of A. mellifera which differ in susceptibility to Varroa, comparing parasitized and non-parasitized full-sister pupae from both stocks. Bee expression profiles were analyzed using microarrays derived from honey bee ESTs whose annotation has recently been enhanced by results from the honey bee genome sequence. We measured differences in gene expression in two colonies of Varroa-susceptible and two colonies of Varroa-tolerant bees. We identified a set of 148 genes with significantly different patterns of expression: 32 varied with the presence of Varroa, 116 varied with bee genotype, and 2 with both. Varroa parasitism caused changes in the expression of genes related to embryonic development, cell metabolism and immunity. Bees tolerant to Varroa were mainly characterized by differences in the expression of genes regulating neuronal development, neuronal sensitivity and olfaction. Differences in olfaction and sensitivity to stimuli are two parameters that could, at least in part, account for bee tolerance to Varroa; differences in olfaction may be related to increased grooming and hygienic behavior, important behaviors known to be involved in Varroa tolerance. CONCLUSION: These results suggest that differences in behavior, rather than in the immune system, underlie Varroa tolerance in honey bees, and give an indication of the specific physiological changes found in parasitized bees. They provide a first step toward better understanding molecular pathways involved in this important host-parasite relationship.

Project description:Honey bees play important roles in pollination for many crops and wild plants, but have been facing great threats posed by various pathogens and parasites. Among them, Varroa destructor, an obligate ectoparasite of honey bees, is considered the most damaging. Within the last century, V. destructor shifted from the original host, the Asian honey bee Apis cerana to the new host, the European honey bee A. mellifera. However, the reproduction of Varroa mites, especially of different haplotypes in the two hosts, is still largely unknown. In this study, we first investigated the existing Varroa haplotypes in local colonies in southern China, and then compared the reproduction of different haplotypes on the worker brood of both the original and new hosts by artificial inoculation. We confirmed that there are two haplotypes of V. destructor in southern China, one is the Korea haplotype and the other is the China haplotype, and the two types parasitized different honey bee species. Although Varroa females from A. mellifera (Korea haplotype) are able to reproduce on the worker brood of both honey bee species, they showed better reproductive performance in the new host A. mellifera with significantly higher fecundity (number of offspring per mother mite) and reproductive rate (number of adult daughters per mother mite), suggesting that this parasite gains higher fitness after host shift. The data further showed that a short stay of Varroa females inside the A. cerana worker cells decreased their fecundity and especially the reproductive rate in a time-dependent manner, suggesting that the A. cerana worker cells may inhibit Varroa reproduction. In contrast, Varroa mites derived from A. cerana colonies (China haplotype) were entirely sterile in A. mellifera worker cells during two sequential inoculations, while the control mites from A. mellifera colonies (Korea haplotype) reproduced normally. In addition, all the infertile mites were found to defecate on the abdomen of bee pupae. We have revealed that two haplotypes of V. destructor exhibit differential reproduction on the worker brood of the original and new host honey bees, providing novel insights into the diversity and complexity of the reproduction of V. destructor.

Dataset Information

Multiple combinations of RDL subunits diversify the repertoire of GABA receptors in the honey bee parasite Varroa destructor.

Publications

Multiple combinations of RDL subunits diversify the repertoire of GABA receptors in the honey bee parasite <i>Varroa destructor</i>.

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