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Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses

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Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses Fredrik Granberg1,2*., Marina Vicente-Rubiano3., Consuelo Rubio-Guerri3, Oskar E. Karlsson1,2,4, Deborah Kukielka3,Sa´ndor Bela´k1,2,5, Jose´ Manuel Sa´nchez-Vizcaı´no3 1 Department of Biomedical Sciences and Veterinary Public Health (BVF), Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden, 2 The OIE Collaborating Centre for the Biotechnology-based Diagnosis of Infectious Diseases in Veterinary Medicine, Uppsala, Sweden, 3 Animal Health Department, Faculty of Veterinary, Complutense University of Madrid, Madrid, Spain, 4 SLU Global Bioinformatics Center, Department of Animal Breeding and Genetics (HGEN), SLU, Uppsala, Sweden, 5 Department of Virology, Immunobiology and Parasitology, VIP, National Veterinary Institute (SVA), Uppsala, Sweden Abstract The situation in Europe concerning honeybees has in recent years become increasingly aggravated with steady decline in populations and/or catastrophic winter losses. This has largely been attributed to the occurrence of a variety of known and ‘‘unknown’’, emerging novel diseases. Previous studies have demonstrated that colonies often can harbour more than one pathogen, making identification of etiological agents with classical methods difficult. By employing an unbiased metagenomic approach, which allows the detection of both unexpected and previously unknown infectious agents, the detection of three viruses, Aphid Lethal Paralysis Virus (ALPV), Israel Acute Paralysis Virus (IAPV), and Lake Sinai Virus (LSV), in honeybees from Spain is reported in this article. The existence of a subgroup of ALPV with the ability to infect bees was only recently reported and this is the first identification of such a strain in Europe. Similarly, LSV appear to be a still unclassified group of viruses with unclear impact on colony health and these viruses have not previously been identified outside of the United States. Furthermore, our study also reveals that these bees carried a plant virus, Turnip Ringspot Virus (TuRSV), potentially serving as important vector organisms. Taken together, these results demonstrate the new possibilities opened up by high-throughput sequencing and metagenomic analysis to study emerging new diseases in domestic and wild animal populations, including honeybees. Citation: Granberg F, Vicente-Rubiano M, Rubio-Guerri C, Karlsson OE, Kukielka D, et al. (2013) Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses. PLoS ONE 8(2): e57459. doi:10.1371/journal.pone.0057459 Editor: Amit Kapoor, Columbia University, United States of America Received May 28, 2012; Accepted January 24, 2013; Published February 27, 2013 Copyright: ß 2013 Granberg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was mainly supported by the Award of Excellence (Excellensbidrag), provided to SB by the Swedish University of Agricultural Sciences (SLU), and an FPU grant from the Ministry of Education, Culture and Sports of Spain, which supported MVR and CRG. Special recognition is given to the Ministry of Education of Spain for the FPU grant of Consuelo Rubio-Guerri and Marina Vicente-Rubiano. The work was also partly supported by/executed in the framework of the EU-project AniBioThreat (Grant Agreement: Home/2009/ISEC/AG/191) with the financial support from the Prevention of and Fight against Crime Programme of the European Union, European Commission - Directorate General Home Affairs. This publication reflects the views only of the authors, and the European Commission cannot be held responsible for any use, which may be made of the information contained therein. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] . These authors contributed equally to this work. Introduction honeybee decline, which is the most efficient pollinator of most crops [2], the global value of insect pollination has been estimated In recent years, the world’s population of honeybee (Apis at US$ 212 billion (J153 billion), which represents about 9.5% of mellifera), the main insect pollinator in the USA and Europe, has the total value of agricultural production. Specifically, the value of been decreasing. This loss of bee population has been called insect pollination to agriculture for EU25 is US$ 19.8 billon Colony Collapse Disorder (CCD), defined as the disappearance of (J14.2 billion) [3]. As a result, the CCD phenomenon has become bees from the beehives without any dead bees around the affected a growing concern for governments and international organiza- hives, presence of abundant breeding cells, pollen, and honey tions, which have led to increased investments in terms of research despite a small population of adult bees and without any on its origin. characteristic symptom of disease [1]. The importance of this The manifestations of increased honeybee mortality and decline phenomenon stems not only from the large direct losses of honey- of managed hives due to unclear diseases, such as CCD, have to producing countries, of which Spain has the largest honey a great extent been associated with viral infections [4,5]. At least production in the European Union (EU) and EU ranks third in 18 different viruses with the ability to infect honeybees have so far the world honey production CCD may also cause indirect losses been identified [6,7], and an additional four were recently for a lack of crop pollination, some of them very important in suggested [8]. Several of them have been demonstrated to have Spain such as citrus crop. To illustrate the serious effects of a global spread [9,10] and colonies frequently suffer from multiple PLOS ONE | www.plosone.org 1 February 2013 | Volume 8 | Issue 2 | e57459 Detection of Viral Pathogens in Spanish Honeybees viral co-infections [11–14]. In addition, since most of the honeybee Given the unclear diagnosis of many honeybee viral diseases, viruses tend to persist as covert infections with no obvious the frequent covert infection of these viruses and the high symptoms, requiring stress to be activated [15] even seemingly prevalence of multiple viral co-infections, we hypothesize that healthy colonies can harbour a variety of potentially harmful viral a metagenomic approach should be particularly useful to find infections [16,17]. Among the natural activation factors, especially various potentially causative agents in the bee colonies. This has mite infestations have been correlated with outbreak of disease. also been demonstrated by previous studies aimed at character- The parasitism is believed to induce virus proliferation by causing izing the microflora, or microbiome, of the honeybee in search of a general decline in immune capacity of the hosts and mites have microbial agents involved in CCD [4,8]. In this study, honeybees also been shown to act as vectors of honeybee viruses [18–20]. from Spain were investigated using a high-throughput sequencing Regarding the above listed serious problems and losses, there is approach to identify all potential etiological agents. a high need to investigate the occurrence, emergence and effects of various pathogens in the European honeybee populations, with Materials and Methods special regard to known and ‘‘unknown’’, emerging new viruses and to the combination of various agents in complex infections. Specimens For the time being, the direct diagnosis of the various disease forms The sample of honeybees (Apis mellifera) was collected with the is based on two main approaches: a) traditional diagnostic owners’ permission from one colony belonging to one apiary of 25 methods, such as virus isolation and electron microscopy; b) commercial hives located in Los Arcos, Navarre, North of Spain. molecular diagnostic methods, such as PCR and microarrays, The colony was sampled by the veterinary services due to lack of among others. vitality of adult worker honeybees and unusual depopulation, The traditional paradigm of detecting and identifying pathogens especially in the brood frames. Furthermore, symptoms compat- relies upon diagnostic tests available for the detection of known ible with CCD such as drastically reduced adult population in agents. This makes it difficult, or impossible, to identify un- presence of abundant food and breeding were observed. There expected or novel pathogens by using conventional methods. were no specific symptoms compatible with viral diseases. The Virus isolation has a very powerful diagnostic capacity, sample consisted of approximately 50 adult worker bees from considering that this method is able to detect a very wide range inside and outside the hives to ensure the presence of young and of viruses directly, in a single system. However, even this excellent adult bees. The bees were collected in sterile containers and frozen method has many weaker sides, e.g., the inability of many viruses, until delivered to the Department of Animal Health at the including honeybee viruses, to replicate in the used cell cultures Complutense University of Madrid for routine testing with
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