Honey Bee Viruses: An Ongoing History of Discovery

INTRODUCTION

Honey bees (Apis mellifera) are indispensable to the global agricultural ecosystem since their pollination affects the yield of numerous crops (Gallai et al., 2009). Moreover, honey bees produce honey, pollen, royal jelly, wax, and other products that significantly contribute to the agricultural economy (Popovska Stojanov et al., 2021; Zacepins et al., 2021). Winter mortality, which is higher than summer mortality, is one of the key challenges (Steinhauer et al., 2014). In summer, honey bee activity is so high that the exchange of various pathogens among honey bees occurs outside, increasing the load of pathogens (Runckel et al., 2011), but the nutrients that honey bees can take are abundant, which does not appreciably affect the health of honey bees (Di Pasquale et al., 2013). In winter, nutrients are limited, and the Varroa mite, a vector of pathogens, increases (Traynor et al., 2016). As a result of the lengthy lifespan and the dense structure (winter cluster) inside the hive, and pathogens continuously infect the honey bees in winter that cause more harmful than in summer (Jung and Bae, 2022).

The physiological ecology of honey bees can be divided into summer honey bees, which have a short lifespan of 15 to 45 days, and winter honey bees, which have a lifespan of approximately 150 days or more (Doeke et al., 2015). Honey bees are known to prepare for the winter season around the autumnal equinox (Jung and Bae, 2022). The strength of a honey bee colony influences the ability of honey bee to survive during overwintering (Jung and Bae, 2022). In Korea, winter honey bees are born beginning mid-October, and if they fail to develop into adults during this period, they overwinter with weakened colonies or continue to make winter honey bees until December (Jung and Bae, 2022). Throughout the winter, honey bee colonies remain overcrowded to form winter clusters for temperature management; as a result, winter honey bees have more antibiotic activity than summer honey bees, but they are more vulnerable to infectious diseases (Jung and Bae, 2022). Winter clusters begin to form when the external temperature drops to 10 to 14℃ for more than three days (Stabentheiner et al., 2010). The inside of a winter cluster must be at least 13℃, and typically needs to be maintained between 20 to 25℃ for honey bees to be able to carry out colony maintenance activities (Southwick and Mugaas, 1971). According to Steinhauer et al. (2014), honey bee mortality in overwintering colonies in the US, was caused by weak forces, a lack of food, unproductive queen honey bees, honey bee mites, and pesticides. Between 2011 and 2013, the average overwintering success rate in Korea was 82.6% (Jeong et al., 2016). Honey bee mites had the greatest influence on the mortality of winter colonies (Genersch et al., 2010; Guzman-Novoa et al., 2016). Winter honey bees infected with honey bee mites are reported to have a 20% higher overwinter mortality than healthy hives (Jung and Bae, 2022). If mite infection becomes severe during the winter honey bee breeding season, the risk of overwinter mortality increases due to losses of fat and vitellogenin, which are substances that enhance the resistance to cold in honey bees (Fries et al., 1994; Amdam et al., 2004). Viruses such as Deformed wing virus (DWV) and Israeli acute paralysis virus (IAPV) are closely associated with colony mortality, and the damage caused by these viruses can be exacerbated by honey bee mite infestations, leading to higher mortality rates in honey bee colonies (Gisder et al., 2009; Chen et al., 2014).

Worker honey bees are reduced by 10 to 20% in the average overwintering colony. In Korea, a drop of more than 30% is considered abnormal mass loss phenomenon (Kim, 2022). Colony collapse disorder (CCD), which first occurred in Pennsylvania in the US in 2006 (Cox-Foster et al., 2007; vanEngelsdorp et al., 2007), is a phenomenon similar to abnormal winter mortality in Korea. CCD is a phenomenon in which worker honey bees disappear with little evidence of mass mortality near the hive, leaving only the queen and some young honey bees in the colony despite having sufficient food in the colony (Johnson, 2010). In this review, we describe the viruses that have been reported thus far, as well as synergy between viruses and other factors and virome analysis.

HONEY BEE VIRUSES

Viruses are classified as DNA or RNA viruses depending on the nucleic acid genome, and can be single and double-stranded depending on the structure of the genome (Villarreal, 2004). In addition, RNA viruses are divided into positive-sense and negative-sense (Payne, 2017). Positive-sense viral RNA genomes can be translated in the same manner as mRNA, so they can be expressed immediately after the viral genome enters the cell, but negative-sense RNA viruses can only be expressed in cells after a transcription process to positive-sense RNA virus occurs (Nguyen and Haenni, 2003).

Viruses are highly mutable, but RNA viruses have a higher mutation rate than DNA viruses (Sanjuán et al., 2010). Positive-sense single-stranded RNA viruses are the most common viruses identified in honey bees (Brutscher et al., 2016). Recently, many DNA viruses have been discovered in honey bees (Kraberger et al., 2019). However, little is known about the impacts of DNA viruses other than Apis mellifera filamentous virus (Gauthier et al., 2015).

Thus far, 128 viruses found in honey bees have been reported in the NCBI GenBank database (Table 1). Viruses are mainly found in worker honey bees but are sometimes found in drones, queen honey bees, bumblebees, wasps, and honey bee mites. The pathways, symptoms, and risks of most viruses have not yet been uncovered. Acute bee paralysis virus (ABPV), Black queen cell virus (BQCV), Chronic bee paralysis virus (CBPV), DWV, IAPV, Kashmir bee virus (KBV), Sacbrood virus (SBV), Apis rhabdovirus (ARV) group, and Lake Sinai virus (LSV) group have been the focus of global research.

Table 1.

List of viruses found in honey bees (Apis mellifera) reported in the NCBI GenBank database

MAJOR TAXA OF HONEY BEE VIRUSES

The viruses discovered in honey bees reported to NCBI are divided into nine orders, 11 families, and six genera, with several unclassified viruses (Table 1). The major honey bee viruses are mainly found in Nodamuvirales and Picornavirales.

Nodamuvirales was named after the Nodamura virus found in Noda-mura, Tokyo, Japan (Scherer and Hurlbut, 1967). It includes two families, and the virion form has a non-enveloped icosahedral symmetric structure with a size of 25-33 nm and a genome of 4.5-6 kb. In the case of the family Nodaviridae, it consists of two molecules of positive-sense single-stranded RNA1 and RNA2 (Thiéry et al., 2022). However, viruses in the family Sinhaliviridae have one positive-sense single-stranded RNA genome (Runckel et al., 2011). Among the two families, the viruses found in honey bees belong to the family Sinhaliviridae. Sinhaliviridae was named after two phylogenetically similar virus groups, the virus found in the sweat bee (Halictus scabiosae, Adlikon virus (Bigot et al., 2017)) and the LSV found in honey bees.

Picornavirus is a combination of the words “pico”, which means “small” in Spanish, and RNA virus. Several phylogenetically similar “picornavirus-like” viruses have been identified since the first identification of Picornavirus in 1963 and the identification of the entire genome sequence in 1980, and the family Picornaviridae are used to bind them (Le Gall et al., 2008). It has now been reported in ICTV as the order Picornavirales, which is a higher group (Sanfaçon et al., 2022). Picornaviruses are classified into five families, among which the bee viruses are found in family Dicistroviridae and Iflaviridae.

The Dicistroviridae family has a positive-sense single-stranded RNA genome of 8-10 kb, and the virion type has an icosahedral structure with a size of 30 nm without an envelope (Valles et al., 2017). It also has a characteristic dicistronic genome, from which it was named, which includes the genera Aparavirus, Triatovirus, and Cripavirus. Aparavirus is derived from the Acute bee paralysis virus, Triatovirus is derived from the Triatoma virus, and Cripavirus is derived from the Cricket paralysis virus (ICTV, 2022). Major honey bee viruses belonging to this order include ABPV, KBV, and IAPV belonging to the genus Aparavirus, and BQCV belonging to the Triatovirus, and several viruses belonging to the genus Cripavirus have also been found (Table 1).

Iflaviridae has an RNA genome of 9-11 kb, and the virion form is 22-30 nm in size, without an envelope, and has an icosahedral symmetrical structure. Derived from the Infectious flacherie virus, both family and genus were named, and one genus was included (Chen et al., 2022). The major honey bee viruses are DWV, SBV, and Varroa destructor virus (Table 1).

CHARACTERISTICS OF HONEY BEE VIRUSES

4. Deformed wing virus (DWV)

DWV is a positive-sense single-stranded RNA virus belonging to the family Iflaviridae and genus Iflavirus. In honey bees, DWV infection causes immature development, wing deformity, and sometimes death (Bailey, 1968a). Bailey et al. (1979) named it the Egypt bee virus (EBV) after its first discovery during their research. In 1982, a virus similar to the EBV was discovered in malformed adults collected in Japan; the EBV was subsequently renamed DWV because of its similar symptoms (Ribière et al., 2008). Currently, there are three different types of DWV: DWV-A, DWV-B, and DWV-C. DWV-A corresponds to the known DWV. DWV-A is 97% identical to Kakugo virus (KV), which is only found in the brains of nurse honey bees and foragers, and its infection symptoms are more aggressive than those of DWV (Fujiyuki et al., 2004). It has also been demonstrated experimentally that KV can infect tissues other than the brains of honey bees (Lanzi et al., 2006). DWV-B, also known as the Varroa destructor virus-1 (VDV-1), was first detected in the Varroa mite, and it is 84% identical to DWV-A (Ongus et al., 2004). VDV-1 can be replicated in honey bees (Yue and Genersch, 2005). In temperate regions, DWV-B is a larger problem than other types of DWV (Natsopoulou et al., 2017). Recombination between type A and type B has also been reported (Moore et al., 2011). Overall, DWV-C shared 79% identity with type A and 78.9% identity with type B (Mordecai et al., 2016). In Korea, after a partial viral genome sequence (EU836051) was reported in 2008, a complete viral genome sequence was reported in 2012 (Reddy et al., 2013c). The documented hosts included A. mellifera, A. cerana (MH607198), Varroa destructor (MZ821838), Bumbus sp. (HQ655506 and MW222481), Vespa sp. (MN565036), and other insects (KF978606, KF314877, ON448657, KF314878, MF13482, and ON448672). DWV diagnostic manuals that include ultra-rapid PCR, ultra-rapid real time PCR, real time PCR, and LAMP methods have been developed (Lim, 2013; Lim and Yoon, 2013; Kim et al., 2014a; Kim et al., 2019b).

Fig. 1.

Symptoms caused by the Deformed wing virus, such as deformed wing and shortened abdomen.

NOSEMA 

Nosema apis, a unicellular parasite belonging to Microsporidia, was first discovered in 1909 (Zander, 1909). Queen honey bees infected with N. apis have a reduced spawning potential owing to ovary degeneration, and queen honey bees located inside the bottom side of the hive during spring are predominantly infected with the N. apis (Fyg, 1945; Liu, 1992). In the case of worker bees, infections impair the hypopharyngeal glands, reducing the feeding capacity of spring nurse honey bees and making it impossible to properly raise larvae, thereby weakening the bee population (Lotmar, 1936). Moreover, RNA synthesis decreases in infected cells, and digestive enzymes release may cease, resulting in digestive disorders (Hartwig and Przelecka, 1971; Liu, 1984). When infected, worker honey bees develop into foraging honey bees faster than healthy bees, resulting in faster aging of infected honey bees (Hassanein, 1953; Wang and Mofller, 1970). The average life expectancy of infected honey bees is 17-31 days, 11-27 days shorter than honey bees that were not exposed to N. apis for seven years (Revell, 1960). As a result, it can reduce honey production (Moeller, 1962; L’Arrivee and Geiger, 1966; Cantwell and Shimanuki, 1969; Fries et al., 1984; Farrar, 2014). N. apis affects the wintering ability of the colony; winter loss is associated with the Nosema infection, and accumulation begins in the spring after surviving the winter (Farrar, 1942). In addition, when infected honey bees clean their honeycomb, the Nosema spores spread to the honeycomb itself and are then transmitted through the wax (Bailey and Ball, 2013). Honey bees infected with N. apis are suspected to have higher incidences of Malpighamoeba mellificae, however, more research is needed to confirm this (Bailey, 1968b). Recently, a TaqMan probe-based RT-qPCR diagnosis method for M. mellificae has been developed to study the effects of M. mellificae on honey bees (Schäfer et al., 2022). Several honey bee viruses are related to N. apis (Bailey, 1982). Considering that BQCV has a shorter lifespan in honey bees infected with both Nosema and BQCV than in single-infected honey bees, the simultaneous infection of BQCV and Nosema has been found to have a synergistic effect on the lifespan of honey bees (Gajda et al., 2021). In an experimental co-infection study, CBPV and Nosema had synergistic effects, as the co-infection resulted in faster honey bee mortality than individual infection (Toplak et al., 2013). Nosema infection did not significantly increase the DWV titer in the pollen supply process, however, compared to control, the DWV titer did increase significantly after the pollen supply was stopped, confirming that Nosema infection has a synergistic effect on the amplification of DWV when pollination is not properly performed (Zheng et al., 2015). In 1995, Nosema cerana was detected in A. cerana in China (Fries et al., 1996). N. cerana is known to have a greater impact on bumble bees than honey bees (Graystock et al., 2013). N. cerana was also found in pollen, which can cause infections, indicating that forager honey bees are more vulnerable to infection than queen honey bees and drones (Higes et al., 2008). N. cerana can be transmitted through N. apis, and can be infected by chewing contaminated wax when leaving the honeycomb (Malone and Gatehouse, 1998). Honey bees infected with N. cerana may have trouble returning to their hive due to stress (Wolf et al., 2016). This return ability has been demonstrated to reduce the level of trehalose involved in flight regardless of the degree of infection in infected honey bees (Kurze et al., 2016). Nosema-infected honey bees are also closely related to pesticides, with studies showing that honey bees exposed to high levels of pesticides are more susceptible to N. cerana infection than honey bees with low exposure levels (Pettis et al., 2013). After 8 days, honey bees infected with 1×10⁵ N. cerana spores showed a 100% mortality rate (Higes et al., 2007). As a result, it may have a synergistic effect on the CCD phenomenon, which is the biggest threat to honey bees, by inflicting various damage (Bromenshenk et al., 2010).

VARROA MITE

The Varroa mite is a honey bee pest known to cause considerable damage to honey bees (Fig. 2). To date, the Varroa mite comprises four species. Varroa jacobsoni Oudemans was discovered in 1904 in A. cerana, Java, Indonesia (Oudemans, 1904); V. underwoodi in A. cerana, Nepal (Delfinado-Baker and Aggarwal, 1987); and V. rindereri in A. koschevnikovi, Borneo, Malaysia (De Guzman and Delfinado-Baker, 1996). The fourth species, V. destructor, was recently separated as another species from being misclassified as V. jacobsoni (Anderson, 2000; Anderson and Trueman, 2000). Among these four Varroa mites, V. destructor is mostly distributed in mainland Asia, especially in the eastern part, and is the most destructive to honey bees (Rosenkranz et al., 2010). Several symptoms of Varroa infection in honey bees have been reported: first, some infected honey bees displayed shortened abdomens and a 6-25% weight loss compared to healthy honey bees, with the number of Varroa mites and the weight of the honey bees exhibiting a negative correlation (De Jong et al., 1982). Second, the life span of honey bees varied according to the number of Varroa mites. The average life span of honey bees was 18.1 days when infected by one Varroa mite and 8.9 days when infected by two or more mites, and the number of Varroa mites was correlated with the honey bee life-span (De Jong and De Jong, 1983). Third, infected worker honey bees were less efficient in major activities; when infected during the larval stage, the size of the hypopharyngeal glands decreased by up to 31% and the adult stage decreased by an average of 14% (Schneider and Drescher, 1987). This reduction in the hypopharyngeal gland size makes it difficult for the nurse honey bees to feed the larvae, which interferes with honey bee growth and weakens the colony. As a result, the Varroa mite directly injures bee larvae and adults, injures hemolymph and fat bodies, and harms them, affecting their life duration, weight, and endocrine organs (Ramsey et al., 2019). Fourth, the Varroa mite has a large effect on honey bee’s ability to fly. When infected by a Varroa mite in the larval stages, wing deformation can occur in some honey bees and the number of Varroa-infected honey bees that cannot return to the colony is twice that of healthy honey bees (Kralj and Fuchs, 2006). When a drone is infected by a Varroa mite, it has a great impact on the drone’s flight ability. There is no difference in flight abilities between a healthy drone and an infected drone through a single Varroa mite, but a drone infected by two or more Varroa mites showed a maximum flight time of up to 6 min compared to a healthy drone with an average flight time of 27 min (Duay et al., 2002). As such, Varroa mites, which cause substantial damage, also act as a mediator for transferring pathogens to honey bees (Fig. 3). Currently, there are 22 viruses registered in the GenBank that are associated with Varroa mites. Among them, ABPV (Ball and Allen, 1988), BQCV (Locke et al., 2012), CBPV (Celle et al., 2008), IAPV (Di Prisco et al., 2011), SBV (Shen et al., 2005), KBV (Chen et al., 2004), SBPV (Santillán-Galicia et al., 2010), DWV, and VDV1 (Ryabov et al., 2017) are known to infect honey bees. As a result, direct damage to bees can reduce their immune systems, resulting in synergistic effects in causing CCD, which is the primary cause of honey bee mortality in the world (Le Conte et al., 2010).

Fig. 2.

Varroa destructor, reddish-brown in color, (A) dorsal view, (B) ventral view.

Fig. 3.

Varroa mite infection pathway by honey bee life cycle, created by referring to de Miranda et al. (2011).

VIROME ANALYSIS USING HIGH-THROUGHPUT SEQUENCING (HTS)

Recent studies have focused not only on the diagnosis of individual viruses, but also on the analysis of all viral nucleic acids present in individuals, communities, and the environment, confirming the diversity within these groups. The virus or viral nucleic acid information of such a group is referred to as a “virome” (Zárate et al., 2017).

Virome analysis using HTS began in 2002 using seawater samples (Breitbart et al., 2002). HTS has demonstrated broad capabilities for the detection of known and novel viruses in a variety of different sample types, including environmental, clinical, and biological samples such as cell lines and biological products (Goodacre et al., 2018). HTS technologies have also provided new insights into intraspecific viral diversity, thereby facilitating the characterization of virus variants and improving the disentanglement of viral population genetics (Maclot et al., 2020).

HTS technology-based virome analysis has been widely used by several researchers to study honey bees (Remnant et al., 2017; Roberts et al., 2018; Kadlečková et al., 2022; Lester et al., 2022). Various novel viruses have been identified using virome analysis. As a result, the number of viruses detected in honey bees has increased from 18 in 2007 to 128 in 2022 (Chen and Siede, 2007; NCBI, 2022). Although Virome analysis has already been actively conducted by many researchers around the world, and a virome analysis was recently performed for the first time in honey bees in Korea (Kwon et al., 2023).

FUTURE DIRECTIONS

Since the CCD outbreak in 2006, many researchers around the world have been interested in honey bees’ health, with research on bees increasing annually. Several researchers in Korea have studied the effects of various factors on honey bee health, but research on viruses has not been conducted extensively. Countrywide, mass honey bee mortalities during the winter of 2021 were concluded to be caused by various factors (climate change, pesticides, and mites) without mentioning the influence of viruses (Lee and Choi, 2022). However, several studies have shown that viruses can have a significant impact on the health of bees, and further research is underway. Korea experienced severe damage from the SBV in Apis cerana during 2009-2010. Using past damage as a starting point, focusing on the risk of viruses in honey bees and accumulating data through various studies will lead to developments in Korean beekeeping.

Acknowledgments

This research was funded by the BSRP through the National Research Foundation of Korea (NRF), Ministry of Education (NRF-2018R1A6A1A03024862).

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