Skip to main content
PMC home page
Genome Announcements logoLink to Genome Announcements
. 2016 Jul 28;4(4):e00729-16. doi: 10.1128/genomeA.00729-16

Complete Genome Sequence of an Avian Paramyxovirus Representative of Putative New Serotype 13

Iryna Goraichuk a,b, Poonam Sharma b, Borys Stegniy a, Denys Muzyka a, Mary J Pantin-Jackwood a, Anton Gerilovych a, Olexii Solodiankin a, Vitaliy Bolotin a, Patti J Miller b, Kiril M Dimitrov b, Claudio L Afonso b,✉
PMCID: PMC4966462  PMID: 27469958

Abstract

Here, we report the complete genome sequence of a virus of a putative new serotype of avian paramyxovirus (APMV). The virus was isolated from a white-fronted goose in Ukraine in 2011 and designated white-fronted goose/Ukraine/Askania-Nova/48-15-02/2011. The genomic characterization of the isolate suggests that it represents the novel avian paramyxovirus group APMV 13.

GENOME ANNOUNCEMENT

Avian paramyxoviruses (APMVs) belong to the genus Avulavirus of the family Paramyxoviridae, order Mononegavirales (1). There are 12 confirmed (APMV-1 to -12) serotypes in the genus (2, 3). Virulent strains of APMV-1 cause Newcastle disease (ND), one of the most devastating diseases in poultry. The rest of the serotypes have been associated with mild infections in poultry, wild and domestic waterfowl, passerines, psittacines, and columbids, among other species (4–11). Three of the recently accepted serotypes (APMV-10 to -12) were isolated from Rockhopper penguin, Common snipe, and Eurasian wigeon, respectively (12–14). Viruses from the genus Avulavirus have a genome size of approximately 15 kb, consisting of a negative-sense single-stranded RNA, with six genes encoding up to eight different proteins.

In 2011, active surveillance of wild birds for avian influenza (AI) virus and APMV was conducted in the Azov-Black Sea region of Ukraine. A hemagglutinating agent that did not cross-react with AI virus antisera was isolated from fecal samples collected from a white-fronted goose (Anser albifrons) in the Kherson region. The isolate weakly cross-reacted with antisera against APMV-1 and APMV-7 but did not show any cross-reactivity with the other APMV serotypes. The intracerebral pathogenicity index (ICPI) test (15) resulted in a value of 0.34, which is indicative of a virus of low virulence for chickens.

Complete genome sequencing of the virus was conducted at the Southeast Poultry Research Laboratory, Athens, GA. Viral RNA was isolated from allantoic fluid using the QIAamp RNA viral minikit (Qiagen, USA). The complete genome sequence was obtained using next-generation sequencing employing the Nextera XT DNA library preparation kit (Illumina, San Diego, CA). The distribution size and concentration of the prepared libraries were checked on a Bioanalyzer 2100, using the Agilent high-sensitivity DNA kit (Agilent Technologies, Germany), and Qubit, using the double-stranded DNA (dsDNA) HS assay kit (Life Technologies, USA). Paired-end sequencing was performed on an Illumina MiSeq instrument using the 500-cycle MiSeq reagent kit version 2 (Illumina). Sequence data were assembled using MIRA version 3.4.0 (16) within a customized workflow on the Galaxy platform (17).

Sequence analysis revealed that the complete genome length of the isolated strain designated white-fronted goose/Ukraine/Askania-Nova/48-15-02/2011 is 16,146 nucleotides (nt) (in accordance with the “rule of six”). The viral genome contained six transcriptional units (3′-NP-P-M-F-HN-L-5′) of 1,482 nt, 1,194 nt, 1,101 nt, 1,638 nt, 1,740 nt, and 6,600 nt in length, respectively. The genome sequence showed 97% nucleotide identity to that of goose/Kazakhstan/5751/2013 (accession no. KU646513) that was recently deposited in GenBank and designated APMV-13 (18). However, the genome of white-fronted goose/Ukraine/Askania-Nova/48-15-02/2011 is 150 nt longer than the one of the virus isolated in Kazakhstan. The 5ˊ and 3ˊ ends of the genome reported here were confirmed as described previously (19). The fusion protein gene of the white-fronted goose/Ukraine/Askania-Nova/48-15-02/2011 isolate had 98% nucleotide identity to APMV/goose/Shimane/67/2000, isolated in Japan from goose fecal samples and also reported previously as APMV-13 (20). Phylogenetic evaluation of the predicted amino acid sequences of the viral proteins revealed that among the rest of the serotypes, APMV-12 is most closely related to the newly characterized virus (63.7 to 75.1% amino acid identity).

Nucleotide sequence accession number.

The complete genome sequence of APMV/white-fronted goose/Askania-Nova/48-15-02/11 has been deposited in GenBank under the accession no. KX119151.

ACKNOWLEDGMENTS

We acknowledge Dawn Williams-Coplin and Tim Olivier for their technical assistance in characterizing the virus.

The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. The USDA is an equal opportunity provider and employer.

This work was partially funded by Project Agreement P-568 funded by the Department of the State.

Footnotes

Citation Goraichuk I, Sharma P, Stegniy B, Muzyka D, Pantin-Jackwood MJ, Gerilovych A, Solodiankin O, Bolotin V, Miller PJ, Dimitrov KM, Afonso CL. 2016. Complete genome sequence of an avian paramyxovirus representative of putative new serotype 13. Genome Announc 4(4):e00729-16. doi:10.1128/genomeA.00729-16.

REFERENCES

  • 1.Mayo MA. 2002. A summary of taxonomic changes recently approved by ICTV. Arch Virol 147:1655–1656. doi: 10.1007/s007050200039. [DOI] [PubMed] [Google Scholar]
  • 2.Afonso CL, Amarasinghe GK, Banyai K, Bao Y, Basler CF, Bavari S, Bejerman N, Blasdell KR, Briand FX, Briese T, Bukreyev A, Calisher CH, Chandran K, Cheng J, Clawson AN, Collins PL, Dietzgen RG, Dolnik O, Domier LL, Durrwald R, Dye JM, Easton AJ, Ebihara H, Farkas SL, Freitas-Astua J, Formenty P, Fouchier RA, Fu Y, Ghedin E, Goodin MM, Hewson R, Horie M, Hyndman TH, Jiang D, Kitajima EW, Kobinger GP, Kondo H, Kurath G, Lamb RA, Lenardon S, Leroy EM, Li CX, Lin XD, Liu L, Longdon B, Marton S, Maisner A, Muhlberger E, Netesov SV, Nowotny N, et al.. 23 May 2016. Taxonomy of the order Mononegavirales: update 2016. Arch Virol [Epub ahead of print.] doi: 10.1007/s00705-016-2880-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Dimitrov KM, Ramey AM, Qiu X, Bahl J, Afonso CL. 2016. Temporal, geographic, and host distribution of avian paramyxovirus 1 (Newcastle disease virus). Infect Genet Evol 39:22–34. doi: 10.1016/j.meegid.2016.01.008. [DOI] [PubMed] [Google Scholar]
  • 4.Lamb R, Parks G. 2013. Paramyxoviridae, p 957–995. In Knipe DM, Howley PM (ed), Fields virology, vol 1, 6th ed. Lippincott Williams & Wilkins, Philadelphia, PA. [Google Scholar]
  • 5.Alexander DJ. 1988. Newcastle disease virus—an avian paramyxovirus, p 11–22. In Alexander DJ (ed), Newcastle disease. Kluwer Academic Publishers, Boston, MA. [Google Scholar]
  • 6.Maldonado A, Arenas A, Tarradas MC, Luque I, Astorga R, Perea JA, Miranda A. 1995. Serological survey for avian paramyxoviruses from wildfowl in aquatic habitats in Andalusia. J Wildl Dis 31:66–69. doi: 10.7589/0090-3558-31.1.66. [DOI] [PubMed] [Google Scholar]
  • 7.Goodman BB, Hanson RP. 1988. Isolation of avian paramyxovirus-2 from domestic and wild birds in Costa Rica. Avian Dis 32:713–717. doi: 10.2307/1590989. [DOI] [PubMed] [Google Scholar]
  • 8.Lipkind M, Alexander D, Shihmanter E, Weisman Y, Collins M. 1995. Antigenic heterogeneity of avian paramyxoviruses of serotype 2 (“Yucaipa-like”) isolated from domestic and wild birds in Israel. Comp Immunol Microbiol Infect Dis 18:189–207. doi: 10.1016/0147-9571(95)00003-Q. [DOI] [PubMed] [Google Scholar]
  • 9.Parthiban M, Kaliyaperumal M, Xiao S, Nayak B, Paldurai A, Kim S-H, Ladman BS, Preskenis LA, Gelb J, Collins PL, Samal SK. 2013. Complete genome sequence of an avian paramyxovirus type 4 from North America reveals a shorter genome and new genotype. Genome Announc 1(1):e00075-12. doi: 10.1128/genomeA.00075-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Kelleher CJ, Halvorson DA, Newman JA, Senne DA. 1985. Isolation of avian paramyxovirus from sentinel ducks and turkeys in Minnesota. Avian Dis 29:400–407. doi: 10.2307/1590501. [DOI] [PubMed] [Google Scholar]
  • 11.Mundt E. 2013. Newcastle disease, p 107–138. In Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair V (ed), Diseases of poultry, 13th ed. Wiley-Blackwell, Hoboken, NJ. [Google Scholar]
  • 12.Miller PJ, Afonso CL, Spackman E, Scott MA, Pedersen JC, Senne DA, Brown JD, Fuller CM, Uhart MM, Karesh WB, Brown IH, Alexander DJ, Swayne DE. 2010. Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. J Virol 84:11496–11504. doi: 10.1128/JVI.00822-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Briand F-X, Henry A, Massin P, Jestin V. 2012. Complete genome sequence of a novel avian paramyxovirus. J Virol 86:7710. doi: 10.1128/JVI.00946-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Terregino C, Aldous EW, Heidari A, Fuller CM, De Nardi R, Manvell RJ, Beato MS, Shell WM, Monne I, Brown I, Alexander DJ, Capua I. 2013. Antigenic and genetic analyses of isolate APMV/wigeon/Italy/3920-1/2005 indicate that it represents a new avian paramyxovirus (APMV-12). Arch Virol 158:2233–2243. doi: 10.1007/s00705-013-1735-2. [DOI] [PubMed] [Google Scholar]
  • 15.World Organisation for Animal Health (OIE) 2012. Newcastle disease. Manual of diagnostic tests and vaccines for terrestrial animals (mammals, birds and bees), vol 1. Biological Standards Commission, World Organisation for Animal Health, Paris, France: http://www.oie.int/doc/ged/D7710.pdf. [Google Scholar]
  • 16.Chevreux B, Wetter T, Suhai S. 1999. Genome sequence assembly using trace signals and additional sequence information, p 45–56. In Computer science and biology. Proceedings of the German Conference on Bioinformatics, GCB ’99. GCB, Hannover, Germany. [Google Scholar]
  • 17.Goecks J, Nekrutenko A, Taylor J, Galaxy Team . 2010. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86. doi: 10.1186/gb-2010-11-8-r86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Karamendin K, Kydyrmanov A, Seidalina A, Asanova S, Sayatov M, Kasymbekov E, Khan E, Daulbayeva K, Harrison SM, Carr IM, Goodman SJ, Zhumatov K. 2016. Complete genome sequence of a novel avian paramyxovirus (APMV-13) isolated from a wild bird in Kazakhstan. Genome Announc 4(3):e00167-16. doi: 10.1128/genomeA.00167-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Brown PA, Briand F-X, Guionie O, Lemaitre E, Courtillon C, Henry A, Jestin V, Eterradossi N. 2013. An alternative method to determine the 5′ extremities of non-segmented, negative sense RNA viral genomes using positive replication intermediate 3′ tailing: application to two members of the Paramyxoviridae family. J Virol Methods 193:121–127. doi: 10.1016/j.jviromet.2013.05.007. [DOI] [PubMed] [Google Scholar]
  • 20.Yamamoto E, Ito H, Tomioka Y, Ito T. 2015. Characterization of novel avian paramyxovirus strain APMV/Shimane67 isolated from migratory wild geese in Japan. J Vet Med Sci 77:1079–1085. doi: 10.1292/jvms.14-0529. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genome Announcements are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES