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Advances in Honey Bee Virus Research

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Insect Viruses".

Deadline for manuscript submissions: closed (31 March 2020) | Viewed by 68152

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Prof. Nor Chejanovsky

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Guest Editor

Entomology Department, Institute of Plant Protection, Agricultural Research Organization, The Volcani Center, Israel
Interests: honey bee viruses; insect viruses; insect virus host-range

Special Issue Information

Dear Colleagues,

The sudden collapse of honey bee colonies in California in 2005 and alarming reports about significant colony losses in the U.S. and Europe have attracted the renewed attention of researchers and the general public to the role played by honey bee viruses in this process. Thus, research focused on the elucidation of the genomic sequences of previously identified and new honey bee-associated viruses, their pathogenicity at the individual and colony levels, their structure, their interactions with other pathogens, and their relationship with the host, many times emerging from covert-asymptomatic to overt-symptomatic infections following stress challenges, has recently been conducted. These efforts have resulted in new and substantial knowledge.

In this Special Issue of Viruses, our aim is to highlight recent significant advances in this area of virology to provide an updated integrated picture of honey bee-associated viruses in order to improve, facilitate, and encourage further innovative research in this fascinating field, as well as to highlight select, recent advances that could contribute to broaden our understanding of this topic. Researchers who would like to contribute their views and/or original research on the above themes, including molecular, structural, genomic, and biological virus–host aspects and the emergence/involvement of new virus strains, as well as new viruses, are welcome to do so.

Prof. Nor Chejanovsky
Guest Editor

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Keywords

Honey bee virus
virus strain
virus structure
metagenomics analysis
virus tolerance/resistance
pathogen/insecticide–virus synergism/antagonism
virus host-range

Published Papers (13 papers)

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Editorial

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2 pages, 161 KiB

Open AccessEditorial

Advances in Honey Bee Virus Research

by Nor Chejanovsky

Viruses 2020, 12(10), 1149; https://0-doi-org.brum.beds.ac.uk/10.3390/v12101149 - 10 Oct 2020

Viewed by 1680

Abstract

The sudden collapse of honey bee colonies in California in 2005 and alarming reports about significant colony losses in the U [...] Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

Research

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11 pages, 3858 KiB

Open AccessArticle

Infection of a Lepidopteran Cell Line with Deformed Wing Virus

by Tal Erez and Nor Chejanovsky

Viruses 2020, 12(7), 739; https://0-doi-org.brum.beds.ac.uk/10.3390/v12070739 - 09 Jul 2020

Cited by 7 | Viewed by 2738

Abstract

Many attempts to develop a reliable cell cultured-based system to study honey bee virus infections have encountered substantial difficulties. We investigated the ability of a cell line from a heterologous insect to sustain infection by a honey bee virus. For this purpose, we infected the Lepidopteran hemocytic cell line (P1) with Deformed wing virus (DWV). The genomic copies of DWV increased upon infection, as monitored by quantitative RT-PCR. Moreover, a tagged-primer-based RT-PCR analysis showed the presence of DWV negative-sense RNA in the cells, indicating virus replication. However, the DWV from infected cells was mildly infectious to P1 cells. Similar results were obtained when the virus was injected into Apis mellifera pupae. Thus, though the virus yields from the infected cells appeared to be very low, we show for the first time that DWV can replicate in a heterologous cell line. Given the availability of many other insect cell lines, our study paves the way for future exploration in this direction. In the absence of adequate A. mellifera cell lines, exploring the ability of alternative cell lines to enable honey bee virus infections could provide the means to study and understand the viral infectious cycle at the cellular level and facilitate obtaining purified isolates of these viruses. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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8 pages, 894 KiB

Open AccessCommunication

Detection and Replication of Moku Virus in Honey Bees and Social Wasps

by Andrea Highfield, Jessica Kevill, Gideon Mordecai, Jade Hunt, Summer Henderson, Daniel Sauvard, John Feltwell, Stephen J. Martin, Seirian Sumner and Declan C. Schroeder

Viruses 2020, 12(6), 607; https://0-doi-org.brum.beds.ac.uk/10.3390/v12060607 - 02 Jun 2020

Cited by 18 | Viewed by 3504

Abstract

Transmission of honey bee viruses to other insects, and vice versa, has previously been reported and the true ecological importance of this phenomenon is still being realized. Members of the family Vespidae interact with honey bees via predation or through the robbing of brood or honey from colonies, and these activities could result in virus transfer. In this study we screened Vespa velutina and Vespa crabro collected from Europe and China and also honey bees and Vespula vulgaris from the UK for Moku virus (MV), an Iflavirus first discovered in the predatory social wasp Vespula pensylvanica in Hawaii. MV was found in 71% of Vespula vulgaris screened and was also detected in UK Vespa crabro. Only seven percent of Vespa velutina individuals screened were MV-positive and these were exclusively samples from Jersey. Of 69 honey bee colonies screened, 43% tested positive for MV. MV replication was confirmed in Apis mellifera and Vespidae species, being most frequently detected in Vespula vulgaris. MV sequences from the UK were most similar to MV from Vespula pensylvanica compared to MV from Vespa velutina in Belgium. The implications of the transfer of viruses between the Vespidae and honey bees are discussed. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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12 pages, 374 KiB

Open AccessArticle

Tolerance of Honey Bees to Varroa Mite in the Absence of Deformed Wing Virus

by John M. K. Roberts, Nelson Simbiken, Chris Dale, Joel Armstrong and Denis L. Anderson

Viruses 2020, 12(5), 575; https://0-doi-org.brum.beds.ac.uk/10.3390/v12050575 - 23 May 2020

Cited by 27 | Viewed by 7094

Abstract

The global spread of the parasitic mite Varroa destructor has emphasized the significance of viruses as pathogens of honey bee (Apis mellifera) populations. In particular, the association of deformed wing virus (DWV) with V. destructor and its devastating effect on honey bee colonies has led to that virus now becoming one of the most well-studied insect viruses. However, there has been no opportunity to examine the effects of Varroa mites without the influence of DWV. In Papua New Guinea (PNG), the sister species, V. jacobsoni, has emerged through a host-shift to reproduce on the local A. mellifera population. After initial colony losses, beekeepers have maintained colonies without chemicals for more than a decade, suggesting that this bee population has an unknown mite tolerance mechanism. Using high throughput sequencing (HTS) and target PCR detection, we investigated whether the viral landscape of the PNG honey bee population is the underlying factor responsible for mite tolerance. We found A. mellifera and A. cerana from PNG and nearby Solomon Islands were predominantly infected by sacbrood virus (SBV), black queen cell virus (BQCV) and Lake Sinai viruses (LSV), with no evidence for any DWV strains. V. jacobsoni was infected by several viral homologs to recently discovered V. destructor viruses, but Varroa jacobsoni rhabdovirus-1 (ARV-1 homolog) was the only virus detected in both mites and honey bees. We conclude from these findings that A. mellifera in PNG may tolerate V. jacobsoni because the damage from parasitism is significantly reduced without DWV. This study also provides further evidence that DWV does not exist as a covert infection in all honey bee populations, and remaining free of this serious viral pathogen can have important implications for bee health outcomes in the face of Varroa. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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12 pages, 827 KiB

Open AccessCommunication

Mode of Transmission Determines the Virulence of Black Queen Cell Virus in Adult Honey Bees, Posing a Future Threat to Bees and Apiculture

by Yahya Al Naggar and Robert J. Paxton

Viruses 2020, 12(5), 535; https://0-doi-org.brum.beds.ac.uk/10.3390/v12050535 - 14 May 2020

Cited by 23 | Viewed by 5068

Abstract

Honey bees (Apis mellifera) can be infected by many viruses, some of which pose a major threat to their health and well-being. A critical step in the dynamics of a viral infection is its mode of transmission. Here, we compared for the first time the effect of mode of horizontal transmission of Black queen cell virus (BQCV), a ubiquitous and highly prevalent virus of A. mellifera, on viral virulence in individual adult honey bees. Hosts were exposed to BQCV either by feeding (representing direct transmission) or by injection into hemolymph (analogous to indirect or vector-mediated transmission) through a controlled laboratory experimental design. Mortality, viral titer and expression of three key innate immune-related genes were then quantified. Injecting BQCV directly into hemolymph in the hemocoel resulted in far higher mortality as well as increased viral titer and significant change in the expression of key components of the RNAi pathway compared to feeding honey bees BQCV. Our results support the hypothesis that mode of horizontal transmission determines BQCV virulence in honey bees. BQCV is currently considered a benign viral pathogen of adult honey bees, possibly because its mode of horizontal transmission is primarily direct, per os. We anticipate adverse health effects on honey bees if BQCV transmission becomes vector-mediated. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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17 pages, 4070 KiB

Open AccessArticle

Green Bees: Reverse Genetic Analysis of Deformed Wing Virus Transmission, Replication, and Tropism

by Olesya N. Gusachenko, Luke Woodford, Katharin Balbirnie-Cumming, Ewan M. Campbell, Craig R. Christie, Alan S. Bowman and David J. Evans

Viruses 2020, 12(5), 532; https://0-doi-org.brum.beds.ac.uk/10.3390/v12050532 - 12 May 2020

Cited by 32 | Viewed by 5799

Abstract

Environmental and agricultural pollination services by honey bees, Apis mellifera, and honey production are compromised by high levels of annual colony losses globally. The majority are associated with disease caused by deformed wing virus (DWV), a positive-strand RNA virus, exacerbated by the ectoparasitic mite Varroa destructor. To improve honey bee health, a better understanding of virus transmission and pathogenesis is needed which requires the development of tools to study virus replication, transmission, and localisation. We report the use of reverse genetic (RG) systems for the predominant genetically distinct variants of DWV to address these questions. All RG-recovered viruses replicate within 24 h post-inoculation of pupae and could recapitulate the characteristic symptoms of DWV disease upon eclosion. Larvae were significantly less susceptible but could be infected orally and subsequently developed disease. Using genetically tagged RG DWV and an in vitro Varroa feeding system, we demonstrate virus replication in the mite by accumulation of tagged negative-strand viral replication intermediates. We additionally apply a modified DWV genome expressing a fluorescent reporter protein for direct in vivo observation of virus distribution in injected pupae or fed larvae. Using this, we demonstrate extensive sites of virus replication in a range of pupal tissues and organs and in the nascent wing buds in larvae fed high levels of virus, indicative of a direct association between virus replication and pathogenesis. These studies provide insights into virus replication kinetics, tropism, transmission, and pathogenesis, and produce new tools to help develop the understanding needed to control DWV-mediated colony losses. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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16 pages, 2850 KiB

Open AccessArticle

Development of a Honey Bee RNA Virus Vector Based on the Genome of a Deformed Wing Virus

by Eugene V. Ryabov, Krisztina Christmon, Matthew C. Heerman, Francisco Posada-Florez, Robert L. Harrison, Yanping Chen and Jay D. Evans

Viruses 2020, 12(4), 374; https://0-doi-org.brum.beds.ac.uk/10.3390/v12040374 - 28 Mar 2020

Cited by 20 | Viewed by 7239

Abstract

We developed a honey bee RNA-virus vector based on the genome of a picorna-like Deformed wing virus (DWV), the main viral pathogen of the honey bee (Apis mellifera). To test the potential of DWV to be utilized as a vector, the 717 nt sequence coding for the enhanced green fluorescent protein (eGFP), flanked by the peptides targeted by viral protease, was inserted into an infectious cDNA clone of DWV in-frame between the leader protein and the virus structural protein VP2 genes. The in vitro RNA transcripts from egfp-tagged DWV cDNA clones were infectious when injected into honey bee pupae. Stable DWV particles containing genomic RNA of the recovered DWV with egfp inserts were produced, as evidenced by cesium chloride density gradient centrifugation. These particles were infectious to honey bee pupae when injected intra-abdominally. Fluorescent microscopy showed GFP expression in the infected cells and Western blot analysis demonstrated accumulation of free eGFP rather than its fusions with DWV leader protein (LP) and/or viral protein (VP) 2. Analysis of the progeny egfp-tagged DWV showed gradual accumulation of genome deletions for egfp, providing estimates for the rate of loss of a non-essential gene an insect RNA virus genome during natural infection. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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21 pages, 4779 KiB

Open AccessArticle

The Heat Shock Response in the Western Honey Bee (Apis mellifera) is Antiviral

by Alexander J. McMenamin, Katie F. Daughenbaugh and Michelle L. Flenniken

Viruses 2020, 12(2), 245; https://0-doi-org.brum.beds.ac.uk/10.3390/v12020245 - 22 Feb 2020

Cited by 31 | Viewed by 6508

Abstract

Honey bees (Apis mellifera) are an agriculturally important pollinator species that live in easily managed social groups (i.e., colonies). Unfortunately, annual losses of honey bee colonies in many parts of the world have reached unsustainable levels. Multiple abiotic and biotic stressors, including viruses, are associated with individual honey bee and colony mortality. Honey bees have evolved several antiviral defense mechanisms including conserved immune pathways (e.g., Toll, Imd, JAK/STAT) and dsRNA-triggered responses including RNA interference and a non-sequence specific dsRNA-mediated response. In addition, transcriptome analyses of virus-infected honey bees implicate an antiviral role of stress response pathways, including the heat shock response. Herein, we demonstrate that the heat shock response is antiviral in honey bees. Specifically, heat-shocked honey bees (i.e., 42 °C for 4 h) had reduced levels of the model virus, Sindbis-GFP, compared with bees maintained at a constant temperature. Virus-infection and/or heat shock resulted in differential expression of six heat shock protein encoding genes and three immune genes, many of which are positively correlated. The heat shock protein encoding and immune gene transcriptional responses observed in virus-infected bees were not completely recapitulated by administration of double stranded RNA (dsRNA), a virus-associated molecular pattern, indicating that additional virus–host interactions are involved in triggering antiviral stress response pathways. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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12 pages, 1807 KiB

Open AccessArticle

Visualizing Sacbrood Virus of Honey Bees via Transformation and Coupling with Enhanced Green Fluorescent Protein

by Lang Jin, Shahid Mehmood, Giikailang Zhang, Yuwei Song, Songkun Su, Shaokang Huang, Heliang Huang, Yakun Zhang, Haiyang Geng and Wei-Fone Huang

Viruses 2020, 12(2), 224; https://0-doi-org.brum.beds.ac.uk/10.3390/v12020224 - 18 Feb 2020

Cited by 15 | Viewed by 4286

Abstract

Sacbrood virus (SBV) of honey bees is a picornavirus in the genus Iflavirus. Given its relatively small and simple genome structure, single positive-strand RNA with only one ORF, cloning the full genomic sequence is not difficult. However, adding nonsynonymous mutations to the bee iflavirus clone is difficult because of the lack of information about the viral protein processes. Furthermore, the addition of a reporter gene to the clones has never been accomplished. In preliminary trials, we found that the site between 3′ untranslated region (UTR) and poly(A) can retain added sequences. We added enhanced green fluorescent protein (EGFP) expression at this site, creating a SBV clone with an expression tag that does not affect virus genes. An intergenic region internal ribosome entry site (IRES) from Black queen cell virus (BQCV) was inserted to initiate EGFP expression. The SBV-IRES-EGFP clone successfully infected Apis cerana and Apis mellifera, and in A. cerana larvae, it was isolated and passaged using oral inoculation. The inoculated larvae had higher mortality and the dead larvae showed sacbrood symptoms. The added IRES-EGFP remained in the clone through multiple passages and expressed the expected EGFP in all infected bees. We demonstrated the ability to add gene sequences in the site between 3′-UTR and poly(A) in SBV and the potential to do so in other bee iflaviruses; however, further investigations of the mechanisms are needed. A clone with a desired protein expression reporter will be a valuable tool in bee virus studies. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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22 pages, 5653 KiB

Open AccessArticle

Viruses in the Invasive Hornet Vespa velutina

by Anne Dalmon, Philippe Gayral, Damien Decante, Christophe Klopp, Diane Bigot, Maxime Thomasson, Elisabeth A Herniou, Cédric Alaux and Yves Le Conte

Viruses 2019, 11(11), 1041; https://0-doi-org.brum.beds.ac.uk/10.3390/v11111041 - 08 Nov 2019

Cited by 37 | Viewed by 5470

Abstract

The Asian yellow-legged hornet Vespa velutina nigrithorax, a major predator of honeybees, is spreading in Europe in part due to a lack of efficient control methods. In this study, as a first step to identify biological control agents, we characterized viral RNA sequences present in asymptomatic or symptomatic hornets. Among 19 detected viruses, the honey bee virus Deformed wing virus-B was predominant in all the samples, particularly in muscles from the symptomatic hornet, suggesting a putative cause of the deformed wing symptom. Interestingly, two new viruses closely related to Acyrthosiphon pisum virus and Himetobi P virus and viruses typically associated with honey bees, Acute bee paralysis virus and Black queen cell virus, were detected in the brain and muscles, and may correspond to the circulation and possible replication forms of these viruses in the hornet. Aphid lethal paralysis virus, Bee Macula-like virus, and Moku virus, which are known to infect honey bees, were also identified in the gut virus metagenome of hornets. Therefore, our study underlined the urgent need to study the host range of these newly discovered viruses in hornets to determine whether they represent a new threat for honey bees or a hope for the biocontrol of V. velutina. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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Review

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19 pages, 1045 KiB

Open AccessReview

Pesticide–Virus Interactions in Honey Bees: Challenges and Opportunities for Understanding Drivers of Bee Declines

by Gyan P. Harwood and Adam G. Dolezal

Viruses 2020, 12(5), 566; https://0-doi-org.brum.beds.ac.uk/10.3390/v12050566 - 21 May 2020

Cited by 32 | Viewed by 6444

Abstract

Honey bees are key agricultural pollinators, but beekeepers continually suffer high annual colony losses owing to a number of environmental stressors, including inadequate nutrition, pressures from parasites and pathogens, and exposure to a wide variety of pesticides. In this review, we examine how two such stressors, pesticides and viruses, may interact in additive or synergistic ways to affect honey bee health. Despite what appears to be a straightforward comparison, there is a dearth of studies examining this issue likely owing to the complexity of such interactions. Such complexities include the wide array of pesticide chemical classes with different modes of actions, the coupling of many bee viruses with ectoparasitic Varroa mites, and the intricate social structure of honey bee colonies. Together, these issues pose a challenge to researchers examining the effects pesticide-virus interactions at both the individual and colony level. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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12 pages, 1529 KiB

Open AccessReview

Honey Bee Queens and Virus Infections

by Esmaeil Amiri, Micheline K. Strand, David R. Tarpy and Olav Rueppell

Viruses 2020, 12(3), 322; https://0-doi-org.brum.beds.ac.uk/10.3390/v12030322 - 17 Mar 2020

Cited by 17 | Viewed by 5370

Abstract

The honey bee queen is the central hub of a colony to produce eggs and release pheromones to maintain social cohesion. Among many environmental stresses, viruses are a major concern to compromise the queen’s health and reproductive vigor. Viruses have evolved numerous strategies to infect queens either via vertical transmission from the queens’ parents or horizontally through the worker and drones with which she is in contact during development, while mating, and in the reproductive period in the colony. Over 30 viruses have been discovered from honey bees but only few studies exist on the pathogenicity and direct impact of viruses on the queen’s phenotype. An apparent lack of virus symptoms and practical problems are partly to blame for the lack of studies, and we hope to stimulate new research and methodological approaches. To illustrate the problems, we describe a study on sublethal effects of Israeli Acute Paralysis Virus (IAPV) that led to inconclusive results. We conclude by discussing the most crucial methodological considerations and novel approaches for studying the interactions between honey bee viruses and their interactions with queen health. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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17 pages, 3113 KiB

Open AccessReview

Cell Lines for Honey Bee Virus Research

by Ya Guo, Cynthia L. Goodman, David W. Stanley and Bryony C. Bonning

Viruses 2020, 12(2), 236; https://0-doi-org.brum.beds.ac.uk/10.3390/v12020236 - 20 Feb 2020

Cited by 28 | Viewed by 5676

Abstract

With ongoing colony losses driven in part by the Varroa mite and the associated exacerbation of the virus load, there is an urgent need to protect honey bees (Apis mellifera) from fatal levels of virus infection and from the non-target effects of insecticides used in agricultural settings. A continuously replicating cell line derived from the honey bee would provide a valuable tool for the study of molecular mechanisms of virus–host interaction, for the screening of antiviral agents for potential use within the hive, and for the assessment of the risk of current and candidate insecticides to the honey bee. However, the establishment of a continuously replicating honey bee cell line has proved challenging. Here, we provide an overview of attempts to establish primary and continuously replicating hymenopteran cell lines, methods (including recent results) of establishing honey bee cell lines, challenges associated with the presence of latent viruses (especially Deformed wing virus) in established cell lines and methods to establish virus-free cell lines. We also describe the potential use of honey bee cell lines in conjunction with infectious clones of honey bee viruses for examination of fundamental virology. Full article

(This article belongs to the Special Issue Advances in Honey Bee Virus Research)

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