Iridovirus and microsporidian linked to honey bee colony decline

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Bromenshenk, Jerry J ^a,f   Henderson, Colin B ^a,f   Wick, Charles H ^b   Stanford, Michael F ^b   Zulich, Alan W ^b   Jabbour, Rabih E ^c   Deshpande, Samir V ^d,j   McCubbin, Patrick E ^e   Seccomb, Robert A ^f   Welch, Phillip M ^f   Williams, Trevor ^g   Firth, David R ^a   Skowronski, Evan ^b   Lehmann, Margaret M ^h   Bilimoria, Shan L ⁱ   Gress, Joanna ^h   Wanner, Kevin W ^h   Cramer Jr , Robert A ^h  

^a UNIVERSITY OF MONTANA   (United States)

^b EDGEWOOD CHEMICAL BIOLOGICAL CENTER   (United States)

^c SAIC FREDERICK INC   (United States)

^d Science Technology Corporation   (United States)

^e OptiMetrics Inc   (United States)

^f Bee Alert Technology Inc   (United States)

^g INSTITUTO DE ECOLOGÍA   (Mexico)

^h MONTANA STATE UNIVERSITY   (United States)

ⁱ TEXAS TECH UNIVERSITY   (United States)

^j TOWSON UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUSTRALIA; COLONY COLLAPSE; CONTROLLED STUDY; HONEYBEE; IRIDOVIRUS; KAKUGO VIRUS; MASS SPECTROMETRY; MICROSPORIDIA; MIXED INFECTION; NONHUMAN; NOSEMA APIS; NOSEMA CERANAE; PREVALENCE; PROTEIN ANALYSIS; PROTEOMICS; RNA VIRUS; UNITED STATES; VARROA DESTRUCTOR 1 VIRUS; ANIMAL; BEE; PATHOGENICITY; VIROLOGY;

ACARI; APIS MELLIFERA; APOIDEA; INVERTEBRATA; IRIDOVIRIDAE; IRIDOVIRUS; KAKUGO VIRUS; MICROSPORIDIA; NOSEMA; NOSEMA APIS; NOSEMA CERANAE; RNA VIRUSES; VARROA DESTRUCTOR;

ANIMALS; BEES; COLONY COLLAPSE; IRIDOVIRUS; MASS SPECTROMETRY; MICROSPORIDIA; UNITED STATES;

EID: 78049248014     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013181     Document Type: Article

References (55)

1. Bromenshenk JJ (2010) Colony collapse disorder (CCD) is alive and well. Bee Culture 138: 51.
2. Debnam S, Westervelt D, Bromenshenk J, Oliver R (2008) Colony collapse disorder: symptoms change with seasons and are different with various locations. Bee Culture 137: 30-32.
3. CCD Working Group (2006) Colony Collapse Disorder (CCD). Available: http://maarec.cas.psu.edu/pressReleases/FallDwindleUpdate0107.pdf. Accessed 2010 Jan 15.
4. Cox-Foster DL, Conlan S, Holmes EC, Palacious G, Evans JD, et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287.
5. Chen YP, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apismellifera) in the United States. J Invertebr Pathol 92: 152-159.
6. Joan (2008) Scientists Discover New Virus Invading US Honeybees, U.S. Army Edgewood Chemical Biological Center, Public Affairs Office. News Release. Available: http://www.ecbc.army.mil/pr/download/VDV-1_Discvery.pdf. Accessed 2010 April 20.
7. Edgewood Chemical Biological Center (2007) Scientists Identify Pathogens That May Be Causing Global Honey-Bee Deaths. Science Daily. Available: http://www.sciencedaily.com/releases/2007/04/070426100117.htm. Accessed 2010 August 9.
8. Maori E, Paldi N, Shafir S, Kalev H, Tsur E, et al. (2009) IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18: 55-60.
9. van Engelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, et al. (2009) Colony Collapse Disorder: A Descriptive Study. PLoS ONE 4(8): e6481.
10. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, et al. (2007) Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honey bees in Israel: evidence for diversity due to intra- and inter-species recombination. J Gen Virol 88: 3428-3438.
11. Johnson RM, Evans JD, Robinson GE, Berenbaum MR (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apismellifera). Proc Nat Acad Sci USA 106: 14790-14795.
12. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE 5: e9754.
13. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, et al. (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96: 1-10.
14. Higes M, Martin-Hernandez R, Garrido-Bailon E, Gonzalez-Porto AV, Garcìa- Palencia P, et al. (2009) Honey bee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Reports 1: 110-113.
15. Neumann P, Carreck NL (2010) Honey bee colony losses. J Apicult Res 49: 1-6.
16. Dworzanski JP, Deshpande SV, Chen R, Jabbour RE, Snyder AP, et al. (2006) Mass Spectrometry-based proteomics combined with informatics tools for bacterial classification. J Proteome Res 5: 76-87.
17. Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 13: 198-207.
18. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-92.
19. Jabbour RE, Deshpande SV, Wade MM, Stanford MF, Wick CH, et al. (2010) Double-blind characterization of non-genome-sequenced bacteria by mass spectrometry-based proteomics. Appl Environ Microbiol 76: 3637-3644.
20. Wick CH, Stanford MF, Zulich AW, Skowronski E, Bromenshenk JJ, et al. (2010) Iridescent virus and Nosema ceranae linked to honey bee Colony Collapse Disorder (CCD). Edgewood Chemical Biological Center Technical Report: TR-814, July 2010.
21. Ongus JR, Roode EC, Pleij CWA, Vlak JM, van Oers MM (2006) The 59 nontranslated region of Varroa destructor virus 1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. J Gen Virol 87: 3397-3407.
22. Fujiyuki T, Ohka S, Takeuchi H, Ono M, Nomoto A, et al. (2006) Prevalence and phylogeny of Kakugo virus, a novel insect picorna-like virus that infects the honey bee (Apis mellifera L.), under various colony conditions. J Virol 80: 11528-11538.
23. Terio V, Martella V, Camero M, Decaro N, Testini G, et al. (2008) Detection of a honey bee iflavirus with intermediate characteristics between KaKugo Virus and Deformed Wing Virus. New Microbiol 31: 439-444.
24. Bailey L, Ball BV, Woods RD (1976) An iridovirus from bees. J Gen Virol 31: 459-461.
25. Verma S, Phogat KPS (1982) Seasonal incidence of Apis iridescent virus in Apis cerana indica. Fab. in Uttar Pradesh, India. Indian Bee J 44: 36-37.
26. Bailey L, Ball BV (1978) Apis iridescent virus and ''clustering disease'' of Apiscerana. J Invertebr Pathol 31: 368-371.
27. Baker AC, Schroeder C (2008) The use of RNA-dependent RNA polymerase for the taxonomic assignment of picorna-like viruses (order Picornavirales) infecting Apis mellifera L. populations. Virol J 5: 10.
28. Anderson D, East IJ (2008) The latest buzz about colony collapse disorder. Science 319: 724-725.
29. Williams T (1998) Invertebrate iridescent viruses. In: The Insect Viruses Miller LK, Ball LA, eds. New York: Springer. pp 31-68.
30. Anonymous (2000 Dec 13) Analysis Informativo (Laboratory analysis of bees from Guadalajara, Spain, December 13, 2000). Available: Servicio de Investigacion Agraria, Bee Pathology Laboratory, Central Apicola Regional, Marchamalo, Spain. Provided by M. Higes.
31. Bilimoria SL (2001) Use of viral proteins for controlling the boll weevil and other insect pests. (U.S. Patent 6,200,561, Bl 2001).
32. Marina CF, Fernandez-Salas I, Ibarra JE, Arrendondo-Jimenez JI, Valle J, et al. (2005) Transmission dynamics of an iridescent virus in an experimental mosquito population: the role of host density. Ecol Entomol 30: 376-382.
33. Becnel JJ, White SE (2007) Mosquito pathogenic viruses-the last 20 years. J Am Mosq Control Assoc 23: 36-49.
34. Williams T (2008) Natural invertebrate hosts of iridoviruses (Iridoviridae). Neotrop Entomol 37: 615-632.
35. Jakob NJ, Müller K, Bahr U, Darai G (2001) Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus. Virology 286: 182-196.
36. Delhon G, Tulman ER, Afonso CL, Becnel JJ, Moser BA, et al. (2006) Genome of Invertebrate iridescent virus type 3 (Mosquito iridescent virus). J Virol 80: 8439-8449.
37. Tinsley TW, Kelly DC (1970) An interim nomenclature system for the iridescent group of viruses. J Invertebr Pathol 16: 470-472.
38. Williams T, Cory JS (1994) Proposals for a new classification of iridescent virus. J Gen Virol 75: 1291-1301.
39. Cole A, Morris TJ (1980) A new iridovirus of two species of terrestrial isopods, Armadillidium vulgare and Porcellio scaber. Intervirol 137: 14:21-30.
40. Webby R, Kalmakoff J (1998) Sequence comparison of the major capsid protein gene from 18 diverse iridoviruses. Arch Virol 143: 1940-1966.
41. Marina CF, Ibarra JE, Arredondo-Jimenez JI, Fernandez-Salas I, Liedo P, et al. (2003) Adverse effects of covert iridovirus infection on the life history and demographic parameters of Aedes aegypti. Entomol Exp Appl 106: 53-61.
42. Marina CF, Arredondo-Jimenez J, Castillo A, Williams T (1999) Sublethal effects of iridovirus disease in a mosquito. Oecologia 119: 383-388.
43. Paul ER, Chitnis NS, Henderson CW, Kaul RJ, D'Costa SM, et al. (2007) Induction of apoptosis by iridovirus protein extract. Arch Virol 152: 1353-1364.
44. Chitnis NS, D'Costa SM, Paul ER, Bilimoria SL (2008) Modulation of iridovirus-induced apoptosis by endocytosis, early expression, JNK, and apical caspase. Virology 370: 333-342.
45. Lopez M, Rojas JC, Vandame R, Williams T (2002) Parasitoid-mediated transmission of an iridescent virus. J Invertebr Pathol 80: 160-170.
46. Tonka T, Weiser J (2000) Iridovirus infection in mayfly larvae. J Invertebr Pathol 76: 229-231.
47. Hukuhara T (1964) Induction of epidermal tumor in Bombyx mori (Linnaeus) with Tipula iridescent virus. J Insect Pathol 6: 246-248.
48. Camazine S, Liu TP (1998) A putative iridovirus from the honey bee mite, Varroa jacobsoni Oudemans. J Invertebr Pathol 71: 177-178.
49. Fries I, Feng F, Da Silva A, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32: 356-365.
50. de Miranda JR, Drebot M, Tyler S, Shen M, Cameron CE, et al. (2004) Complete nucleotide sequence of Kashmir bee virus and comparison with Acute bee paralysis virus. J Gen Virol 85: 2263-2270.
51. Bruce WA, Anderson DL, Calderone NW, Shimanuki H (1995) A survey for Kashmir bee virus in honey bee colonies in United States. Am Bee J 135: 352-355.
52. Wilson WT, Menapace DM (1979) Disappearing disease of honey bees: A survey of the United States. Am Bee J. pp 184-186, 217.
53. Suter GW II (2007) Ecological Risk Assessment, 2nd edition. Boca Raton: CRC Press, Taylor and Francis Group. 643 p.
54. D'Costa SM, Yao HJ, Bilimoria SL (2004) Transcriptional mapping in Chilo iridescent virus infections. Arch Virol 149: 723-742.
55. Henderson CW, Johnson CL, Lodhi SA, Bilimoria SL (2001) Replication of Chilo iridescent virus in the cotton boll weevil, Anthonomus grandis, and development of an infectivity assay. Arch Virol 146: 767-775.