Population-genomic variation within RNA viruses of the Western honey bee, Apis mellifera, inferred from deep sequencing

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Cornman, Robert Scott ^a,e   Boncristiani, Humberto ^a,f   Dainat, Benjamin ^a,b   Chen, Yanping ^a   vanEngelsdorp, Dennis ^c   Weaver, Daniel ^d   Evans, Jay D ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b AGROSCOPE LIEBEFELD POSIEUX RESEARCH STATION ALP   (Switzerland)

^c Bldg 142   (United States)

^d Bee Power   (United States)

^e LEETOWN SCIENCE CENTER   (United States)

^f UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Apis mellifera; Deformed wing virus; Israel acute paralysis virus; Population genomics; Single nucleotide polymorphism

Indexed keywords

APIS MELLIFERA; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DEFORMED WING VIRUS; DICISTROVIRIDAE; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; RNA EXTRACTION; RNA VIRUS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; VARROA DESTRUCTOR; VIRUS GENOME; VIRUS STRAIN;

ANIMALS; BEES; CHROMOSOME MAPPING; CONSENSUS SEQUENCE; EVOLUTION, MOLECULAR; FEMALE; GENOMICS; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA VIRUSES; SELECTION, GENETIC; SEQUENCE ANALYSIS, RNA;

ACARI; ACUTE BEE PARALYSIS VIRUS; APIS MELLIFERA; DEFORMED WING VIRUS; RNA VIRUSES; VARROA DESTRUCTOR;

EID: 84874618682     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-154     Document Type: Article

References (40)

1. Oldroyd BP. What's killing American honey bees?. PLoS Biol 2007, 5(6):e168.
2. Van Engelsdorp D, Meixner MD. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 2010, 103:S80-95.
3. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 2011, 6:e20656.
4. Cornman RS, Tarpy DR, Chen YP, Jeffries L, Lopez D, Pettis J. vanEngelsdorp D 2012, Evans DJ: Pathogen webs in collapsing honey bee colonies. PLoS ONE.
5. Genersch E, Von der Ohe W, Kaatz H, Schroeder A, Otten C, Buchler R, Berg S, Ritter W, Muhlen W, Gisder S, et al. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010, 41:332-352.
6. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Dead or alive: Deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl Environ Microbiol 2012, 78:981-987.
7. Yang X, Cox-Foster D. Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 2007, 134:405-412.
8. Gisder S, Hedtke K, Mockel N, Frielitz MC, Linde A, Genersch E. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae?. Appl Environ Microbiol 2010, 76:3032-3038.
9. Jegouic S, Joffret ML, Blanchard C, Riquet FB, Perret C, Pelletier I, Colbere-Garapin F, Rakoto-Andrianarivelo M, Delpeyroux F. Recombination between polioviruses and co-circulating Coxsackie A viruses: role in the emergence of pathogenic vaccine-derived polioviruses. PLoS Pathog 2009, 5:e1000412.
10. Combelas N, Holmblat B, Joffret ML, Colbere-Garapin F, Delpeyroux F. Recombination between poliovirus and coxsackie A viruses of species C: a model of viral genetic plasticity and emergence. Viruses 2011, 3:1460-1484.
11. Fukuyama S, Kawaoka Y. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol 2011, 23:481-486.
12. Evans DM, Dunn G, Minor PD, Schild GC, Cann AJ, Stanway G, Almond JW, Currey K, Maizel JV. Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome. Nature 1985, 314:548-550.
13. de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol 2010, 103:S48-S61.
14. De Miranda JR, Cordoni G, Budge G. The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J Invertebr Pathol 2010, 103:S30-S47.
15. Bowen-Walker PL, Martin SJ, Gunn A. The transmission of Deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 1998, 73:101-106.
16. Gisder S, Aumeier P, Genersch E. Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 2009, 90(Pt 2):463-467.
17. Boncristiani HF, Di Prisco G, Pettis JS, Hamilton M, Chen YP. Molecular approaches to the analysis of deformed wing virus replication and pathogenesis in the honey bee. Apis mellifera. Virol J 2009, 6:221.
18. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination. J Gen Virol 2007, 88:3428-3438.
19. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007, 318:283-287.
20. Van Engelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, et al. Colony collapse disorder: a descriptive study. PLoS One 2009, 4:e6481.
21. Palacios G, Hui J, Quan PL, Kalkstein A, Honkavuori KS, Bussetti AV, Conlan S, Evans J, Chen YP, VanEngelsdorp D, et al. Genetic analysis of Israel acute paralysis virus: Distinct clusters are circulating in the United States. J Virol 2008, 82:6209-6217.
22. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powell M, Nikaido S, Schroeder DC. Global honey bee viral landscape altered by a parasitic mite. Science 2012, 336:1304-1306.
23. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
24. Day WH, McMorris FR. Consensus sequences based on plurality rule. Bull Math Biol 1992, 54:1057-1068.
25. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
26. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
27. Nei M. Molecular Evolutionary Genetics 1987, New York: Columbia University Press.
28. Kofler R, Pandey RV, Schlotterer C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 2011, 27:3435-3436.
29. Moore J, Jironkin A, Chandler D, Burroughs N, Evans DJ, Ryabov EV. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J Gen Virol 2011, 92(Pt 1):156-161.
30. Zioni N, Soroker V, Chejanovsky N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 2011, 417:106-112.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
32. Lunter G, Goodson M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 2011, 21:936-939.
33. Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
34. Ren Q, Wang QS, Firth AE, Chan MM, Gouw JW, Guarna MM, Foster LJ, Atkins JF, Jan E. Alternative reading frame selection mediated by a tRNA-like domain of an internal ribosome entry site. Proc Natl Acad Sci U S A 2012, 109:E630-639.
35. Witwer C, Rauscher S, Hofacker IL, Stadler PF. Conserved RNA secondary structures in Picornaviridae genomes. Nucleic Acids Res 2001, 29:5079-5089.
36. Weir BS. Genetic Data Analysis II 1996, Sunderland, Mass: Sinauer Associates.
37. Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF, Evans JD, Chen Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol 2011, 92(Pt 1):151-155.
38. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Vanengelsdorp D, Lipkin WI, Depamphilis CW, Toth AL, Cox-Foster DL. RNA viruses in hymenopteran pollinators: evidence of inter-Taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 2010, 5:e14357.
39. Racaniello VR. Picornaviridae: the viruses and their replication. Virology 2001, 685-722. Philadelphia: Lippincott, Williams, and Wilkins, Knipe DM, Howley PM, 4.
40. Liu Y, Wimmer E, Paul AV. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta 2009, 1789:495-517.