Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination

Maori, Eyal; Lavi, Shai; Mozes-Koch, Rita; Gantman, Yulia; Peretz, Yuval; Edelbaum, Orit; Tanne, Edna; Sela, Ilan

doi:10.1099/vir.0.83284-0

Cited by 216 publications

(202 citation statements)

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“…This virus was first diagnosed in Israel, where it reportedly caused large scale honeybee mortality and symptoms included trembling wings and paralysis (Maori et al, 2007;Palacios et al, 2008). The detection of IAPV in Varroa mites sampled during this study is therefore of concern, especially since it was recently confirmed that Varroa mites are capable of transmitting IAPV to honeybees (Di Prisco et al, 2011).…”

Section: Discussionmentioning

confidence: 79%

Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

Strauss

Human

Gauthier

et al. 2013

Journal of Invertebrate Pathology

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Section: Discussionmentioning

confidence: 79%

Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

Strauss

Human

Gauthier

et al. 2013

Journal of Invertebrate Pathology

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“…Aside from the above mortality and sub-lethal effects, the symptoms associated with IAPV have not been well characterized and thus hinder our ability to observe the progression of IAPV infection in these important pollinators, especially when considering that virus-induced paralysis symptoms are normally the signal of overt infection and death. Besides, the initial observation of IAPV symptoms are from honeybees; symptom analysis in bumblebees would enhance our knowledge of this virus (de Miranda et al, 2010;DeGrandi-Hoffman & Chen, 2015;Maori et al, 2007Maori et al, , 2009Piot et al, 2015). Therefore, in this study, we report progressive viral symptoms in workers of B. terrestris, which is one of the most numerous bumblebee species in Europe (Velthuis & van Doorn, 2006).…”

Section: Introductionmentioning

confidence: 95%

“…IAPV is positive single-stranded RNA virus in the family Dicistroviridae with a global distribution range (de Miranda et al, 2010;Maori et al, 2007;Palacios et al, 2008). The nomenclature of this virus is largely based on its symptoms that are similar to ABPV.…”

Section: Introductionmentioning

confidence: 99%

“…DWV caused crippled wings in bumblebee (Bombus terrestris and Bombus pascuorum) workers even without Varroa (Fürst et al, 2014;Genersch et al, 2006). Interestingly, viral tissue tropism was different between DWV-infected (asymptomatic) and clinically diseased (symptomatic) honeybees and bumblebees, indicating that overt infection may also be associated with virus tissue spreading (Genersch et al, 2006).IAPV is positive single-stranded RNA virus in the family Dicistroviridae with a global distribution range (de Miranda et al, 2010;Maori et al, 2007;Palacios et al, 2008). The nomenclature of this virus is largely based on its symptoms that are similar to ABPV.…”

mentioning

confidence: 99%

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Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Wang

Meeus

Smagghe

2016

Journal of General Virology

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Although it is known that Israeli acute paralysis virus (IAPV) can cause bee mortality, the symptoms of paralysis and the distribution of the virus in different body tissues and their potential to respond with an increase of the siRNA antiviral immune system have not been studied. In this project we worked with Bombus terrestris, which is one of the most numerous bumblebee species in Europe and an important pollinator for wild flowers and many crops in agriculture. Besides the classic symptoms of paralysis and trembling prior to death, we report a new IAPVrelated symptom, crippled/immobilized forelegs. Reverse-transcriptase quantitative PCR showed that IAPV accumulates in different body tissues (midgut, fat body, brain and ovary). The highest levels of IAPV were observed in the fat body. With fluorescence in situ hybridization (FISH) we detected IAPV in the Kenyon cells of mushroom bodies and neuropils from both antennal and optic lobes of the brain in IAPV-infected workers. Finally, we observed an induction of Dicer-2, a core gene of the RNAi antiviral immune response, in the IAPV-infected tissues of B. terrestris workers. According to our results, tissue tropism and the induction strength of Dicer-2 could not be correlated with virus-related paralysis symptoms. INTRODUCTIONHoneybees and bumblebees are the two most important bee species used in modern apiculture and agriculture. They host many viruses. When looking at the honeybee, there have been around 23 viruses reported and many of these viruses only persist as covert and asymptomatic infections which show no detectable impact at both the individual and colony level (McMenamin & Genersch, 2015). However, under certain conditions, for example the presence of the ectoparasitic honeybee mite Varroa destructor, the covert infections of some viruses turn into overt ones with observable symptoms (Martin et al., 2012;McMahon et al., 2015;Singh et al., 2010). The symptoms of overt infections vary from virus to virus, including deformed wings, discoloration, hair losses, bloated abdomen, paralysis, decreased locomotion, impaired cognition and both brood and adult mortality (Lanzi et al., 2006;McMenamin & Genersch, 2015;Singh et al., 2010). Some symptoms can be easily recognized by the behaviour and appearance of the infected bees, while others can only be confirmed through meticulous and continuous observations or by molecular techniques.In bumblebees (Bombus spp.) a subset of honeybee-infecting viruses has been reported, such as deformed wing virus (DWV), Israeli acute paralysis virus (IAPV), acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), slow bee paralysis virus (SBPV), sacbrood virus (SBV), black queen cell virus (BQCV) and Lake Sinai virus (LSV) (Genersch et al., 2006;Levitt et al., 2013;Parmentier et al., 2016;Peng et al., 2011). However, only DWV, KBV and IAPV have been reported to cause clinical symptoms (Genersch et al., 2006;Meeus et al., 2014). DWV caused crippled wings in bumblebee (Bombus terrestris and Bombus pascuorum) workers even without ...

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“…2c). Like other positive-stranded RNA viruses, the replication of IAPV (Maori et al, 2007) proceeds via the production of negative-stranded intermediates. Therefore, the presence of negative-strand RNA of IAPV in Varroa mite appears to be evidence of virus replication and suggests that the (Fig.…”

mentioning

confidence: 99%

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

Prisco

Pennacchio

Caprio

et al. 2010

Journal of General Virology

214

147

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The Israeli acute paralysis virus (IAPV) is a significant marker of honeybee colony collapse disorder (CCD). In the present work, we provide the first evidence that Varroa destructor is IAPV replication-competent and capable of vectoring IAPV in honeybees. The honeybees became infected with IAPV after exposure to Varroa mites that carried the virus. The copy number of IAPV in bees was positively correlated with the density of Varroa mites and time period of exposure to Varroa mites. Further, we showed that the mite-virus association could possibly reduce host immunity and therefore promote elevated levels of virus replication. This study defines an active role of Varroa mites in IAPV transmission and sheds light on the epidemiology of IAPV infection in honeybees.Varroatosis is one of the most serious honeybee diseases caused by a parasitic mite, Varroa destructor. Varroa mites use their piercing mouthparts to suck out haemolymph from honeybees. The repeated feeding results in a decline of colony vigour, shortened life span of the honeybees and eventual perishing of colonies (Rosenkranz et al., 2010). Further, the feeding of Varroa mites gives mites the potential to act as vectors of bee diseases, presenting additional threats to bee health. The role of Varroa mite as a vector in the transmission of bee viruses has been well documented (Bowen-Walker et al., 1999;Chen et al., 2004;Shen et al., 2005). However, it has not yet been demonstrated if this mite could act as a vector of Israeli acute paralysis virus (IAPV), a virus that was tightly correlated with honeybee colony collapse disorder (CCD), a malady that has decimated honeybee colonies across the USA (Cox-Foster et al., 2007;vanEngelsdorp et al., 2007) and around the world (Neumann & Carreck, 2010). The present study was undertaken to determine the possible role of Varroa mites in the transmission of IAPV and in the promotion of its replication in honeybees. Moreover, the expression of immune-related gene transcripts, apidaecin and eater that are involved in honeybee humoral and cellular immunity (Ertürk-Hasdemir & Silverman, 2005;Evans et al., 2006;Kocks et al., 2005;Simone et al., 2009) was measured in Varroa-challenged bees. Apidaecin is a proline-rich peptide and one of the most prominent components of the honeybee humoral defence against microbial invasion (Evans et al. 2006). Eater is a member of epidermal growth factor-family protein involved cellular immunity, as it plays an important role in phagocytosis (Ertürk-Hasdemir & Silverman, 2005;Kocks et al., 2005). Two strong bee colonies (i.e. with at least seven frames filled with capped brood and food, and covered with adult bees) and two weak colonies (i.e. with a low-adult bee population and fewer than four frames with a small patch of capped brood) that were determined to be free of IAPV infection by RT-PCR assay were selected for transmission studies. Further, the expression levels of vitellogenin, an indicator of the general health of the colonies (Amdam et al., 2005;Simone et al., 2009), were det...

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Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination

Cited by 216 publications

References 35 publications

Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

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