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Horizontal and Vertical Transmission of Viruses in the Honey Bee, Apis Mellifera ଝ

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Horizontal and Vertical Transmission of Viruses in the Honey Bee, Apis Mellifera ଝ Journal of Invertebrate Pathology 92 (2006) 152–159 www.elsevier.com/locate/yjipa Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera ଝ Yanping Chen ¤, Jay Evans, Mark Feldlaufer USDA-ARS, Bee Research Laboratory, Beltsville, MD 20705, USA Received 22 February 2006; accepted 12 March 2006 Abstract The most crucial stage in the dynamics of virus infections is the mode of virus transmission. In general, transmission of viruses can occur through two pathways: horizontal and vertical transmission. In horizontal transmission, viruses are transmitted among individuals of the same generation, while vertical transmission occurs from mothers to their oVspring. Because of its highly organized social structure and crowded population density, the honey bee colony represents a risky environment for the spread of disease infection. Like other plant and animal viruses, bee viruses use diVerent survival strategies, including utilization of both horizontal and vertical routes, to transmit and main- tain levels in a host population. In this review, we explore the current knowledge about the honey bee viruses and transmission routes of bee viruses. In addition, diVerent transmission strategies on the persistence and dynamics of host–pathogen interactions are also discussed. Published by Elsevier Inc. Keywords: Apis mellifera; Viruses; Varroa mite; Horizontal transmission; Vertical transmission 1. Introduction and the persistence of pathogens in a population. Knowl- edge of how the virus infection spreads is fundamental to Viruses are a group of obligate, intracellular parasites that design an appropriate disease control program. In general, are found in virtually all life forms. Viruses lack a system for transmission of a virus can occur horizontally or vertically, their own metabolism and must live and develop inside living or both. In horizontal transmission, viruses are transmitted host cells. Within host cells, viruses take over the metabolism among individuals of the same generation. Horizontal of the host and utilize the host cell’s machinery and compo- transmission can be further classiWed as direct or indirect. nents to make whatever is needed to produce their own prog- Horizontal transmission by a direct route includes air- enies, virions. This process harms the host, resulting in the borne infection, food-borne infection, and venereal (sexual) disease infection or even death of the host. Because of their infection, whereas transmission by an indirect route profound impact on host health, viruses represent a major involves an intermediate biological host, like a mosquito challenge to public health and agriculture societies. vector, which acquires and transmits virus from one host to A very crucial aspect of the dynamics of virus infections another. In vertical transmission, viruses are passed verti- and evolution of host–pathogen interactions is the mode of cally from mother to oVspring via egg, either on the surface transmission. Transmission processes determine the spread of the egg (transovum transmission) or within the egg (transovarian transmission). It has been suggested that ଝ Disclaimer: Mention of trade names or commercial products in this ar- these diVerent transmission modes play a crucial role in W ticle is solely for the purpose of providing speci c information and does determining the virulence of a pathogen (Clayton and not imply recommendation or endorsement by the U.S. Department of Agriculture. Tompkins, 1994; Ewald, 1994). Typically, horizontal trans- * Corresponding author. Fax: +1 301 504 8736. mission favors overt expression of the disease and increases E-mail address: [email protected] (Y. Chen). infection prevalence under certain conditions, such as high 0022-2011/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.jip.2006.03.010 Y. Chen et al. / Journal of Invertebrate Pathology 92 (2006) 152–159 153 host population density and high pathogen replication rate. elucidation of bee virus transmission modes represents a In contrast, vertical transmission is a mechanism for long- rapidly developing research area, and our understanding of term virus persistence and favors evolution of benign virus transmission and epidemiology in honey bees has infection. The outcome of any virus infection can reXect the grown considerably over the last decade. In this review, we balance between the two transmission processes. provide a brief overview of the current knowledge regard- The honey bee (Apis mellifera L.) is the most important ing honey bee viruses and transmission routes of honey bee pollinating insect species and plays a vital role in US agricul- viruses, and discuss the opportunities that lie ahead in the ture by assisting in the pollination of a wide variety of crops study of bee virus transmission and epidemiology. and by producing honey and other hive products, with an annual market value exceeding 15 billion dollars (Morse and 2. Honey bee viruses Calderone, 2000). However, like all living organisms, honey bees are exposed to a diverse array of pathogens including 2.1. Morphology, genome structures, and classiWcation of bee viruses, which are signiWcant threats to their health and well- viruses being. So far, at least 18 viruses have been reported to attack honey bees worldwide and dramatically aVect honey bee Except for Wlamentous bee virus, all honey bee viruses health under certain conditions (Ball and Allen, 1988; Martin, reported so far are spherical to oval shaped 20–30 nm in 2001). Honey bees are social insects and live in colonies con- diameter, isometrically symetrical, non-occluded, and pos- sisting of two generations: one mother queen and her succes- sess a buoyant density in CsCl ranging from 1.33 to 1.42 g/ sors, 20,000–60,000 workers and several hundreds of drones. ml, and a 100–190S sedimentation coeYcient (Bailey, 1976). Individual bees in the colony work together in a highly struc- Because of their similar characteristics, honey bee viruses tured social order and engage in numerous coordinating are diYcult to distinguish morphologically under the elec- activities including defending invaders, building combs, forag- tron microscope (Fig. 1). ing for food, clearing brood cells, rearing oVspring, and Honey bee viruses are positive-sense single-stranded attending the queen. Because of densely crowded populations RNA viruses belonging to the picorna-like virus superfam- and a high contact rate between colony members related to ily and have the following common features. The viral feeding and chemical communication, honey bee colonies pro- genome is composed of a single-stranded RNA molecule vide great opportunities for disease transmission. coated with capsid proteins. The RNA genome is cova- Although there are many gaps in the knowledge of the lently attached by a genome-linked virion protein (VPg) at key processes underlying virus transmission dynamics, the 5Ј and a polyA tail at 3Ј ends. At the 5Ј end, there is a (A) (B) Band containing virus particles Fig. 1. (A) Virus band after CsCl density gradient centrifugation. Supernatant containing viruses mixed with CsCl solution to an initial density of 1.37 g/ml and centrifuged at 40,000 rpm for 18 h at 10 °C. The virus-containing band was collected for subsequent electron micrograph analysis. (B) Electron micro- graph of honey bee virus particles. Bee viruses are spherical to slightly oval particles about 29 nm in diameter as determined from EM. The virus prepara- tion used for this electron micrograph was determined by RT-PCR to contain four diVerent viruses, BQCV, DWV, KBV, and SBV. No signiWcant diVerence in the virion size and morphology could be observed among the four diVerent virus particles. Bar marker represents 0.1 M. 154 Y. Chen et al. / Journal of Invertebrate Pathology 92 (2006) 152–159 long untranslated region (UTR) containing a ‘cloveleaf’ eYcient translation as the internal ribosomal entry site secondary structure. The replication of viruses occurs in the (IRES). However, there is no evidence of that translation of cytoplasm of the host cell. The virus particle attaches to protein is mediated by IRES for monopartite monocistronic surface of the host cell and interacts with a receptor on the genome. Based on their genomic organization, BQCV, KBV, host cell membrane and injects its RNA genome into the and ABPV are assigned to a new virus family, Dicistroviridae, host cell. Once inside the host cell, the RNA genome is whereas SBV and DWV are assigned to the genus IXavirus, translated into a single polyprotein that is subsequently which is a “Xoating genus” that has not yet been assigned to cleaved into structural proteins and functional proteins for a family (Mayo, 2002). RNA replication. With the help of RNA-dependent RNA polymerase, the positive-stranded RNA genome is copied 2.2. Honey bee virus infections to a negative-stranded intermediate, which serves as a tem- plate for replication of new genomic strands that are assem- Viruses infect all developmental stages of the bee includ- bled into progeny viral particles. ing eggs, brood, and adults. Under Weld conditions, most To date, the complete genome sequences of Wve honey bee bee viruses usually persist as latent infections and cause no viruses, acute bee paralysis virus (ABPV) (Govan et al., 2000, overt signs of disease. Moreover, bee colonies can be GenBank Accession No. AF150629), black queen cell virus attacked by more than one virus simultaneously and multi- (BQCV) (Leat et al., 2000, GenBank Accession No. ple viral infections have
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