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Black Queen Cell Virus in the Bumble Bee, Bombus Huntii Wenjun Peng, Jilian Li, Humberto Boncristiani, James Strange, Michele Hamilton, Yanping Chen

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Black Queen Cell Virus in the Bumble Bee, Bombus Huntii Wenjun Peng, Jilian Li, Humberto Boncristiani, James Strange, Michele Hamilton, Yanping Chen Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii Wenjun Peng, Jilian Li, Humberto Boncristiani, James Strange, Michele Hamilton, Yanping Chen To cite this version: Wenjun Peng, Jilian Li, Humberto Boncristiani, James Strange, Michele Hamilton, et al.. Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii. Apidologie, Springer Verlag, 2011, 42 (5), pp.650-658. 10.1007/s13592-011-0061-5. hal-01003597 HAL Id: hal-01003597 https://hal.archives-ouvertes.fr/hal-01003597 Submitted on 1 Jan 2011 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2011) 42:650–658 Original article * INRA, DIB-AGIB and Springer Science+Business Media B.V., 2011 DOI: 10.1007/s13592-011-0061-5 Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii 1 1 2 3 Wenjun PENG , Jilian LI , Humberto BONCRISTIANI , James P. STRANGE , 2 2 Michele HAMILTON , Yanping CHEN 1Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Xiangshan, Beijing, China 2USDA-ARS Bee Research Lab, BARC-East Bldg, 476,, Beltsville, MD 20705, USA 3USDA-ARS Pollinating Insects, Biology, Management and Systematics Laboratory, Utah State University, BNR 255, Logan, UT 84322-5310, USA Received 27 September 2010 – Revised 18 January 2011 – Accepted 30 January 2011 Abstract – Here we provide the first evidence that Black Queen Cell Virus (BQCV), one of the most prevalent honey bee viruses, can cause an infection in bumble bees, Bombus huntii, and that the BQCV infection could spread to different tissues of bumble bees. The detection of negative strand RNA of BQCV, an indicator of active virus replication, in the gut of B. huntii suggests that virus particles replicate within the gut and then cross the gut lining to other tissues through hemolymph circulation. The observation of active replication of the BQCVin the gut, together with the fact that BQCV was more widespread in the body of field-collected bees than that of lab-reared bees, implies a possible association between the foraging activities of bumble bees and virus transmission. The fact that bumble bees and honey bees are able to share nectar and pollen resources in the same field suggests that geographical proximity of two host species could play a role in host range breadth of BQCV. host range / bumble bee / Bombus huntii / Black queen cell virus 1. INTRODUCTION (Heinrich 2004). The interactions by sharing the same nectar and pollen resources in the field Bumble bees (Order: Hymenoptera, Family: have been documented for two bee species Apidae, Genus: Bombus) have long been rec- (Reader et al. 2005; Evans and Spivak 2006; ognized as important pollinators of crops, Dohzond and Yokoyama 2010). Compared to particularly in temperate zone plants (Proctor honey bees, bumble bees have longer tongues et al. 1996; Velthuis and van Doorn 2006). Like (glossa) which allow them to forage more honey bees (Apis mellifera L.), bumble bees efficiently from flowers with long and narrow forage for nectar and pollen from a wide range corollas. The specialized behavior, termed of plants as food for the entire colony and act as “buzz pollination,” and the branched hair that pollinators transferring pollen between plants covers the entire bodies of bumble bees facilitate efficient collection and transfer of pollen from flower to flower. Under certain Corresponding author: Y. Chen, [email protected] circumstances, bumble bees are considered Wenjun Peng and Jilian Li contributed equally in this superior in pollinating to honey bees because work. bumble bees can pollinate plants on rainy, Manuscript editor: Peter Rosenkranz cool days, when honey bees stay inactive Host range expansion of honey bee Black Queen Cell Virus 651 within the hive (Whitman 2007). Due primar- 2. MATERIALS AND METHODS ily to their efficiency in pollinating solana- ceous crops, some species of bumble bees have 2.1. Insects been commercially reared for the pollination of the crops, especially greenhouse tomatoes, Three groups of bumble bees, B. huntii,were peppers, and eggplants. Bombus huntii,a used in the study: (1) male B. huntii reared in the bumble bee species native to western North lab, (2) worker B. huntii reared in the lab, and (3) America, is a prominent pollinator in agro- male B. huntii collected from the field. Bumble ecosystems (Hobbs 1967) and is easily reared bees were collected from the USDA-ARS Pollinat- in the laboratory (Strange 2011). ing Insect Research Unit, Logan, UT. Lab-reared From a health perspective, host range breadth males and workers came from a colony originating of pathogens may have important consequences from a queen bee collected foraging in the spring. for the increase of pathogen virulence, the The colony was reared according to Strange (2011) emergence of new diseases, and the reduction until workers and males were present. Briefly, the of biodiversity. Studying the occurrence of colony was fed syrup of 25% sugars (sucrose, multiple host infection of pathogens could have glucose, and fructose) and pollen, removed and an important implication for understanding collected from pollen traps affixed to honey bee pathogen population structure and diversity, colonies, until the colony reached a size exceeding host–pathogen interactions, and evolutionary 100 individuals. Individual worker bees were then dynamics of diseases (Schmid-Hempel 2001; removed from the lab-reared colony before the bees Brown et al. 2003). Like their relatives, the were permitted to forage freely. Field-collected honey bees, bumble bees face threats from males were captured with an entomological aerial numerous pathogens, including bacteria, fungi, net while foraging on raspberry (Rubus sp.). No protozoa, and viruses and some species have female B. huntii were observed during the field been experiencing population declines collection, likely due to the seasonality of worker (Cameron et al. 2011). Previous studies have production in bumble bees. Each group of captured shown that both honey bees and bumble bees bees was transferred into a cage which was can share the same pathogens (Colla et al. provisioned with sugar syrup and mailed alive to 2006). For instance, Deformed Wing Virus, one the USDA Bee Research Laboratory, Beltsville, MD of the most common and prevalent viruses for the molecular analysis. found in honey bees (reviewed in Chen and Siede 2007), was demonstrated to cause wing 2.2. Tissue dissection deformities in bumble bees (Genersch et al. 2006). Other honey bee viruses, including Acute Bee Different groups of B. huntii were used for tissue Paralysis Virus and Kashmir Bee Virus were dissection. Ten bees were dissected for each group. found to be equally capable of infecting different Each live bumble bee was individually fixed on the species of bumble bees (Bailey and Gibbs 1964; wax top of a dissecting dish with insect pins. Anderson 1991). In order to gain further insight Hemolymph was collected with a micropipette tip into the movement of pathogens between honey by making a small hole on the roof of the bee’s bees and bumble bees, the infection of another thorax with a needle to make it bleed. About 20 μl one of the most prevalent honey bee virus, Black of hemolymph was collected from each bee. Fol- Queen Cell Virus (BQCV), a RNA virus classi- lowing hemolymph collection, the legs, wings, fied within the family Dicistroviridae genus antennae, and eyes were cut off and then the main Cripavirus (Mayo 2002) and was found to cause body of the bee was opened with scissors. Tissues of a significant disease in developing queen larvae the brain, fat bodies, salivary glands, gut, nervous and pupae (Bailey and Woods 1977; Anderson systems, trachea, and food glands were separated 1993), was investigated in bumble bees in the and pulled out of the body with forceps under a present study. dissecting microscope. To prevent possible contam- 652 W. Peng et al. ination with hemolymph, all tissues were rinsed with 2.5. Strand-specific RT-PCR 1× phosphate-buffered saline three times and twice with nuclease-free water and the washing solution In order to determine whether the bumble bee was was changed every time for each tissue. Individual a biological host to support replication of BQCV, tissues were subjected to subsequent RNA extrac- strand-specific RT-PCR was conducted for the pres- tion immediately. ence of negative-stranded RNA of BQCV in bumble bees. The cDNA which is complementary to the 2.3. RNA extraction negative strand RNA of BQCV was synthesized from total RNA extracted from different tissues of bumble Total RNA samples were individually extracted bees with Tag-BQCV-sense primer (position 8132– from 12 different tissues of the bumble bees using 8151) (5′-agcctgcgcacgtggTCAGGTCGGAA- Trizol reagent according to the manufacturer’s spec- TAATCTCGA-3′) using SuperScript III Reverse ifications (RNA extraction kit; Invitrogen, Carlsbad, Transcriptase (Invitrogen, Carlsbad, CA). The se- CA). The resultant RNA pellets were re-suspended in quence of Tag is shown in lowercase and was UltraPure DNase/RNase-Free Distilled Water (Invi- published by Yue and Genersch (2005). The synthe- trogen) in the presence of Ribonuclease Inhibitor sized cDNAs were then purified twice using MinE- (Invitrogen). RNA samples were stored at −80°C lute PCR purification kit and MinElute Reaction prior to molecular detection for BQCV.
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