Identification and complete genome sequencing of paramyxoviruses in mallard ducks (Anas platyrhynchos) using random access amplification and next generation sequencing technologies

Virology Journal

Steven Van Borm¹  Thierry van den Berg¹  Frank Vandenbussche¹  Bénédicte Lambrecht¹  Toon Rosseel¹ 

[1] Operational Directorate of Virology, Veterinary and Agrochemical Research Center, Ukkel, Belgium

关键词: SISPA;    random amplification;    next generation sequencing;    mallard;    avian paramyxovirus;    APMV6;    APMV4;   

Others  :  1155947
DOI  :  10.1186/1743-422X-8-463

 received in 2011-08-30, accepted in 2011-10-06,  发布年份 2011

【 摘 要 】

Background

During a wildlife screening program for avian influenza A viruses (AIV) and avian paramyxoviruses (APMV) in Belgium, we isolated two hemagglutinating agents from pools of cloacal swabs of wild mallards (Anas platyrhynchos) caught in a single sampling site at two different times. AIV and APMV1 were excluded using hemagglutination inhibition (HI) testing and specific real-time RT-PCR tests.

Methods

To refine the virological identification of APMV2-10 realized by HI subtyping tests and in lack of validated molecular tests for APMV2-10, random access amplification was used in combination with next generation sequencing for the sequence independent identification of the viruses and the determination of their genomes.

Results

Three different APMVs were identified. From one pooled sample, the complete genome sequence (15054 nucleotides) of an APMV4 was assembled from the random sequences. From the second pooled sample, the nearly complete genome sequence of an APMV6 (genome size of 16236 nucleotides) was determined, as well as a partial sequence for an APMV4. This APMV4 was closely related but not identical to the APMV4 isolated from the first sample. Although a cross-reactivity with other APMV subtypes did not allow formal identification, the HI subtyping revealed APMV4 and APMV6 in the respective pooled samples but failed to identify the co-infecting APMV4 in the APMV6 infected pool.

Conclusions

These data further contribute to the knowledge about the genetic diversity within the serotypes APMV4 and 6, and confirm the limited sensitivity of the HI subtyping test. Moreover, this study demonstrates the value of a random access nucleic acid amplification method in combination with massive parallel sequencing. Using only a moderate and economical sequencing effort, the characterization and full genome sequencing of APMVs can be obtained, including the identification of viruses in mixed infections.

【 授权许可】

   
2011 Rosseel et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Lamb RA, Parks G: Paramyxoviridae: the viruses and their replication. 5th edition. Philadelphia: Lippincott Williams and Wilkins; 2007.
• [2]Lamb RA, Collins PL, Kolakofsky D, Melero JA, Nagai Y, Oldstone MBA, Pringle CR, Rima BK: Family paramyxoviridae. In Virus Taxonomy: The classification and nomenclature of viruses. The eighth report of the international committee in taxonomy of viruses Edited by Fauquet CM. 2005.
• [3]Alexander DJ, Hinshaw VS, Collins MS, Yamane N: Characterization of viruses which represent further distinct serotypes (PMV-8 and PMV-9) of avian paramyxoviruses. Arch Virol 1983, 78:29-36.
• [4]Alexander DJ: Newcastle disease. In Disease of poultry. Edited by Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE. Ames IA: Iowa State Press; 2003:64-87.
• [5]Miller PJ, Afonso CL, Spackman E, Scott MA, Pedersen JC, Senne DA, Brown JD, Fuller CM, Uhart MM, Karesh WB, et al.: Evidence for a New Avian Paramyxovirus Serotype-10 Detected in Rockhopper Penguins from the Falkland Islands. J Virol 2010, 84:11496-11504.
• [6]OIE: Terrestrial animal health code. World organisation for animal health 2010.
• [7]Alexander DJ, Collins MS: Pathogenicity of PMV-3/parakeet/Netherlands/449/75 for chickens. Avian Pathol 1982, 11:179-85.
• [8]Warke A, Stallknecht D, Williams SM, Pritchard N, Mundt E: Comparative study on the pathogenicity and immunogenicity of wild bird isolates of avian paramyxovirus 2, 4, and 6 in chickens. Avian Pathol 2008, 37:429-34.
• [9]Saif YM, Mohan R, Ward L, Senne DA, Panigrahy B, Dearth RN: Natural and experimental infection of turkeys with avian paramyxovirus-7. Avian Dis 1997, 41:326-9.
• [10]Tumova B, Stumpa A, Janout V, Uvizl M, Chmela J: A further member of the Yucaipa group isolated from the common wren (Troglodytes troglodytes). Acta Virol 1979, 23:504-7.
• [11]Bankowski RA, Almquist J, Dombrucki J: Effect of paramyxovirus yucaipa on fertility, hatchability, and poult yield of turkeys. Avian Dis 1981, 25:517-20.
• [12]Redmann T, Zeydanli MM, Herbst W, Kaleta EF: [Isolation of a paramyxovirus-3 from turkeys with respiratory tract disease in Germany]. Dtsch Tierarztl Wochenschr 1991, 98:138-41.
• [13]Zhang GZ, Zhao JX, Wang HW, Yang AM, Bu CY, Wang M: Isolation, identification, and comparison of four isolates of avian paramyxovirus serotype 2 in China. Avian Dis 2006, 50:386-90.
• [14]Alexander DJ: Newcastle disease and other avian paramyxoviridae infections. In Diseases of poultry. Edited by Calnek BW. Ames: Iowa State University Press; 1997:541-569.
• [15]Jung A, Grund C, Muller I, Rautenschlein S: Avian paramyxovirus serotype 3 infection in Neopsephotus, Cyanoramphus, and Neophema species. J Avian Med Surg 2009, 23:205-8.
• [16]Nerome K, Nakayama M, Ishida M, Fukumi H: Isolation of a new avian paramyxovirus from budgerigar (Melopsittacus undulatus). J Gen Virol 1978, 38:293-301.
• [17]Gough RE, Alexander DJ: Avian paramyxovirus type 4 isolated from a ringed teal (Calonetta leucophrys). Vet Rec 1984, 115:653.
• [18]Stallknecht DE, Senne DA, Zwank PJ, Shane SM, Kearney MT: Avian paramyxoviruses from migrating and resident ducks in coastal Louisiana. J Wildl Dis 1991, 27:123-8.
• [19]Maldonado A, Arenas A, Tarradas MC, Luque I, Astorga R, Perea JA, Miranda A: Serological survey for avian paramyxoviruses from wildfowl in aquatic habitats in Andalusia. J Wildl Dis 1995, 31:66-9.
• [20]Capua I, De Nardi R, Beato MS, Terregino C, Scremin M, Guberti V: Isolation of an avian paramyxovirus type 9 from migratory waterfowl in Italy. Vet Rec 2004, 155:156.
• [21]Alexander DJ: The classification, host range and distribution of avian paramyxoviruses. In Acute virus infections of poultry. Edited by McFerran JB, MCNulty MS. The Netherlands: Martinus Nijhoff Publishers; 1986:52-66.
• [22]Stanislawek WL, Wilks CR, Meers J, Horner GW, Alexander DJ, Manvell RJ, Kattenbelt JA, Gould AR: Avian paramyxoviruses and influenza viruses isolated from mallard ducks (Anas platyrhynchos) in New Zealand. Arch Virol 2002, 147:1287-302.
• [23]Shortridge KF, Alexander DJ: Newcastle disease virus surveillance in Hong Kong on local and imported poultry. Res Vet Sci 1978, 25:204-6.
• [24]Turek R, Gresikova M, Tumova B: Isolation of influenza A virus and paramyxoviruses from sentinel domestic ducks. Acta Virol 1984, 28:156-8.
• [25]Chang PC, Hsieh ML, Shien JH, Graham DA, Lee MS, Shieh HK: Complete nucleotide sequence of avian paramyxovirus type 6 isolated from ducks. J Gen Virol 2001, 82:2157-68.
• [26]Subbiah M, Xiao S, Collins PL, Samal SK: Complete sequence of the genome of avian paramyxovirus type 2 (strain Yucaipa) and comparison with other paramyxoviruses. Virus Res 2008, 137:40-8.
• [27]Kumar S, Nayak B, Samuel AS, Xiao S, Collins PL, Samal SK: Complete genome sequence of avian paramyxovirus-3 strain Wisconsin: evidence for the existence of subgroups within the serotype. Virus Res 2010, 149:78-85.
• [28]Kumar S, Nayak B, Collins PL, Samal SK: Complete genome sequence of avian paramyxovirus type 3 reveals an unusually long trailer region. Virus Res 2008, 137:189-97.
• [29]Nayak B, Kumar S, Collins PL, Samal SK: Molecular characterization and complete genome sequence of avian paramyxovirus type 4 prototype strain duck/Hong Kong/D3/75. Virol J 2008, 5:124. BioMed Central Full Text
• [30]Jeon WJ, Lee EK, Kwon JH, Choi KS: Full-length genome sequence of avain paramyxovirus type 4 isolated from a mallard duck. Virus Genes 2008, 37:342-50.
• [31]Samuel AS, Paldurai A, Kumar S, Collins PL, Samal SK: Complete genome sequence of avian paramyxovirus (APMV) serotype 5 completes the analysis of nine APMV serotypes and reveals the longest APMV genome. PLoS One 2010, 5:e9269.
• [32]Xiao S, Subbiah M, Kumar S, De Nardi R, Terregino C, Collins PL, Samal SK: Complete genome sequences of avian paramyxovirus serotype 6 prototype strain Hong Kong and a recent novel strain from Italy: evidence for the existence of subgroups within the serotype. Virus Res 2010, 150:61-72.
• [33]Xiao S, Paldurai A, Nayak B, Subbiah M, Collins PL, Samal SK: Complete genome sequence of avian paramyxovirus type 7 (strain Tennessee) and comparison with other paramyxoviruses. Virus Res 2009, 145:80-91.
• [34]Paldurai A, Subbiah M, Kumar S, Collins PL, Samal SK: Complete genome sequences of avian paramyxovirus type 8 strains goose/Delaware/1053/76 and pintail/Wakuya/20/78. Virus Res 2009, 142:144-53.
• [35]Samuel AS, Kumar S, Madhuri S, Collins PL, Samal SK: Complete sequence of the genome of avian paramyxovirus type 9 and comparison with other paramyxoviruses. Virus Res 2009, 142:10-8.
• [36]Djikeng A, Halpin R, Kuzmickas R, Depasse J, Feldblyum J, Sengamalay N, Afonso C, Zhang X, Anderson NG, Ghedin E, et al.: Viral genome sequencing by random priming methods. BMC Genomics 2008, 9:5. BioMed Central Full Text
• [37]Allander T, Emerson SU, Engle RE, Purcell RH, Bukh J: A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. Proc Natl Acad Sci USA 2001, 98:11609-14.
• [38]Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, et al.: Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-80.
• [39]Shihmanter E, Weisman Y, Manwell R, Alexander D, Lipkind M: Mixed paramyxovirus infection of wild and domestic birds in Israel. Vet Microbiol 1997, 58:73-8.
• [40]Kolakofsky D, Pelet T, Garcin D, Hausmann S, Curran J, Roux L: Paramyxovirus RNA synthesis and the requirement for hexamer genome length: the rule of six revisited. J Virol 1998, 72:891-9.
• [41]Morrison T, McQuain C, Sergel T, McGinnes L, Reitter J: The role of the amino terminus of F1 of the Newcastle disease virus fusion protein in cleavage and fusion. Virology 1993, 193:997-1000.
• [42]Reyes GR, Kim JP: Sequence-independent, single-primer amplification (SISPA) of complex DNA populations. Mol Cell Probes 1991, 5:473-81.
• [43]Metzker ML: Sequencing technologies - the next generation. Nat Rev Genet 2010, 11:31-46.
• [44]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-402.
• [45]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
• [46]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.