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CYP9Q-Mediated Detoxification of Acaricides in the Honey

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CYP9Q-Mediated Detoxification of Acaricides in the Honey CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera) Wenfu Maoa, Mary A. Schulerb, and May R. Berenbauma,1 aDepartment of Entomology and bDepartment of Cell and Developmental Biology, University of Illinois, Urbana, IL 61801 Contributed by May R. Berenbaum, June 27, 2011 (sent for review March 22, 2011) Although Apis mellifera, the western honey bee, has long encoun- is not uniquely vulnerable to pesticides (10), its capacity to me- tered pesticides when foraging in agricultural fields, for two dec- tabolize multiple toxins simultaneously may be limited. Syner- ades it has encountered pesticides in-hive in the form of acaricides gistic interactions, for example, have been documented in honey to control Varroa destructor, a devastating parasitic mite. The py- bees between insecticides and fungicides (11, 12), between pyr- rethroid tau-fluvalinate and the organophosphate coumaphos ethroids and chlordimeform (13), and between the organo- have been used for Varroa control, with little knowledge of honey phosphate and pyrethroid acaricides approved for use against bee detoxification mechanisms. Cytochrome P450-mediated de- Varroa (14). Such synergism of co-occurring pesticides may be of toxification contributes to pyrethroid tolerance in many insects, particular importance in view of the extensive contamination of but specific P450s responsible for pesticide detoxification in honey bees, bee products, and wax foundation with in-hive and agri- bees (indeed, in any hymenopteran pollinator) have not been de- cultural pesticides documented in the wake of colony collapse fined. We expressed and assayed CYP3 clan midgut P450s and disorder, a phenomenon associated with extensive honey bee demonstrated that CYP9Q1, CYP9Q2, and CYP9Q3 metabolize colony losses that have been reported annually since 2006 (7, 15). tau-fluvalinate to a form suitable for further cleavage by the car- Understanding how A. mellifera metabolizes pesticides is, there- boxylesterases that also contribute to tau-fluvalinate tolerance. fore, important for maintaining a viable apiculture industry in These in vitro assays indicated that all of the three CYP9Q enzymes the United States; identifying the specific mechanisms contrib- also detoxify coumaphos. Molecular models demonstrate that cou- uting to acaricide metabolism is critical for assessing the limits of fl fi SCIENCES maphos and tau- uvalinate t into the same catalytic pocket, pro- pesticide tolerance and evaluating the probability of synergistic AGRICULTURAL viding a possible explanation for the synergism observed between and antagonistic interactions in this species, as well as for de- these two compounds. Induction of CYP9Q2 and CYP9Q3 tran- signing less-toxic alternatives for use against pesticide-resistance scripts by honey extracts suggested that diet-derived phytochem- mites and for monitoring exposures to pesticides in agricultural fields. icals may be natural substrates and heterologous expression of fi fl The multifunctional activities of cytochrome P450 mono- CYP9Q3 con rmed activity against quercetin, a avonoid ubiqui- oxgenases (P450s) contribute to the metabolism of natural and tous in honey. Up-regulation by honey constituents suggests that synthetic toxins in most aerobic organisms (16–18). P450-medi- diet may influence the ability of honey bees to detoxify pesticides. ated detoxification is central to tolerance and evolved resistance Quantitative RT-PCR assays demonstrated that tau-fluvalinate to pesticides in many pest insects (19, 20), including tolerance of enhances CYP9Q3 transcripts, whereas the pyrethroid bifenthrin pyrethroid insecticides in honey bees (11, 21, 22). Specific P450s enhances CYP9Q1 and CYP9Q2 transcripts and represses CYP9Q3 responsible for pesticide detoxification in honey bees have not transcripts. The independent regulation of these P450s can be use- been previously defined but, with the availability of the honey ful for monitoring and differentiating between pesticide expo- sures in-hive and in agricultural fields. bee genome sequence, identifying them is greatly facilitated by the reduced inventory of P450 loci in this species (23). The Apidae | miticide | transcriptional regulation complement of 46 full-length P450 genes in this genome is about half the number of P450 genes found in the dipteran Drosophila melanogaster genome (24) and the hymenopteran Nasonia vitri- s a pollinator, the western honey bee Apis mellifera con- pennis genome (25). Of these P450 genes, 28 belong to the CYP3 Asumes nectar and pollen (albeit in processed form as honey clan, a large P450 lineage including many CYP6 and CYP9 and beebread), and in doing so generally encounters dietary family members that are known to mediate detoxificative func- phytochemicals in substantially lower concentrations than do tions in other insects (19). The unique expansion of genes in the insect herbivores that consume chemically well-defended foliage CYP6AS subfamily (relative to other hymenopteran genomes) (1). The polylectic foraging behavior of A. mellifera (2), however, suggests that these proteins play a role in the detoxification of exposes the honey bee to a potentially broad diversity of phy- xenobiotics present in the honey bee’s distinctive diet of honey tochemicals and its habit of concentrating nectar to make honey and beebread. In fact, Mao et al. demonstrated that CYP6AS3 is suggests that honey bees encounter phytochemicals at higher capable of contributing to the detoxification of quercetin, a fla- concentrations than do most nectar-feeding pollinators that do – vonol widely distributed in plant nectars (1). not process their food (3 6). In the late nineteenth century, the To identify the specific P450s contributing to pyrethroid me- chemical milieu of managed honey bees changed profoundly tabolism in the honey bee, we assayed a number of CYP3 clan with the introduction of agrochemicals, especially pesticides; P450s expressed in the honey bee midgut (the principal site of since that time, honey bees have regularly encountered a tre- xenobiotic metabolism) and demonstrated that those in the mendous diversity of synthetic toxins via pesticide drift or resi- CYP9Q subfamily hydroxylate tau-fluvalinate to a form poten- dues in treated crops (7). Since 1990, the chemical environment of the honey bee changed yet again, with the widespread de- liberate use of in-hive acaricides for control of Varroa, a devas- fl Author contributions: W.M., M.A.S., and M.R.B. designed research; W.M. performed re- tating parasitic mite af icting North American apiculture (8). search; M.A.S. contributed new reagents/analytic tools; W.M., M.A.S., and M.R.B. ana- In-hive acaricides, including the pyrethroid tau-fluvalinate and lyzed data; and W.M., M.A.S., and M.R.B. wrote the paper. the organophosphate coumaphos, have been used for Varroa The authors declare no conflict of interest. control with little knowledge of honey bee detoxification path- 1To whom correspondence should be addressed. E-mail: [email protected]. ways. An extensive literature review documenting pesticide This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. sensitivity in the honey bee (9) shows that, although this species 1073/pnas.1109535108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1109535108 PNAS | August 2, 2011 | vol. 108 | no. 31 | 12657–12662 Downloaded by guest on September 27, 2021 tially suitable for further cleavage by carboxylesterases (Fig. S1), P450s expressed in honey bee midguts metabolize λ-cyhalothrin shown by Johnson et al. to contribute to tau-fluvalinate tolerance (11), we set out to determine whether P450s metabolizing tau- (14). This study is thus unique in identifying specific genes fluvalinate are also located in this tissue. Intact midguts of 3-d-old contributing to pesticide metabolism within the order Hyme- worker bees were incubated with tau-fluvalinate in the presence noptera, which includes many of the world’s most important and absence of piperonyl butoxide (PBO), an inhibitor for most pollinator species, which also are facing pesticide exposures in bacterial and eukaryotic P450s. GC-MS data for the products agricultural landscapes. generated in these reactions indicated that P450s expressed in midgut tissue metabolize tau-fluvalinate (Fig. S2). Results Further identification of the P450s responsible for conversion Identification of Tau-Fluvalinate Metabolites in Frass. Although of tau-fluvalinate proceeded by cloning of 10 honey bee P450s Johnson et al. established that P450s are involved in pyrethroid (including CYP6AS3, CYP6AS10, CYP6AQ1, CYP6BD1, metabolism in honey bees, specific inhibitors of carboxylesterase CYP338A1, and all CYP9 family members) (Fig. S3) and coex- enzymes indicated that these enzymes might also be involved pressing them in Sf9 cells with house fly P450 reductase, as (22). As demonstrated for cypermethrin metabolism in Heli- described in Mao et al. (1). Carbon monoxide difference quan- coverpa (Heliothis) armigera, carboxylesterases metabolize not tification of their P450 levels (27) indicated that eight folded only pyrethroids but also the hydroxylated metabolites of pyr- correctly and two (CYP6AQ1 and CYP6BD1) folded incorrectly ethroids generated by P450s (26). Rather than use previously (generating P420 peaks). In vitro metabolism assays conducted described isotopic labeling procedures, we opted to characterize with 60 pmoles of the eight successfully expressed indicated that pyrethroid metabolites in honey bee midgut samples using GC- only CYP9Q1, CYP9Q2, and
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