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Circulation of at Least Six Distinct Groups of Pigeon-Derived Newcastle Disease Virus in Iran Between 1996 and 2019

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Abstract

According to the latest Newcastle disease virus (NDV) classification system, Iranian PPMV-1 isolates were classified as either XXI.1.1 or XXI.2 subgenotypes only. However, a few recent studies have suggested the possible existence of other Iranian PPMV-1 genotypes/subgenotypes. Recently, we isolated a PPMV-1 closely related to the African origin subgenotype VI.2.1.2 from an ill captive pigeon in a park aviary in central Tehran (Pg/IR/AMMM160/2019). This subgenotype had never been reported from Iran or neighboring countries. We also isolated a subgenotype VII.1.1 NDV (Pg/IR/AMMM117/2018), usually reported from non-pigeon birds in Iran. The nucleotide distance of AMMM117 was 1.0–2.5% compared to other Iranian subgenotypes VII.1.1 isolates. However, usually the same year VII.1.1 viruses that we isolate from Iranian poultry farms show negligible distances (0.0–0.5%). More isolates are required to study if this difference is due to subgenotype VII.1.1 being circulated and mutated in pigeons. Here, we also characterized two other isolates, namely Pg/IR/AMMM168/2019 and Pg/IR/MAM39/2017. The latter is the first Iranian subgenotype XXI.1.1 to be featured in the NDV datasets of the international NDV consortium. We also investigated the phylogenetic relation of all the published Iranian pigeon-derived NDV to date and updated the grouping according to the latest classification system. We have concluded that at least six different groups of pigeon-derived NDV have been circulating in Iran since 1996, four of which have been reported from just one city over the last seven years. This study suggests that the Iranian pigeon-origin NDV have been more diverse than the Iranian poultry-derived NDV in recent years.

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Abbreviations

Pigeon paramyxovirus serotype-1:

PPMV-1

Newcastle disease virus:

NDV

specific pathogen-free:

SPF

hemagglutination assay:

HA

hemagglutination inhibition assay:

HI

Fusion:

F

Basic Local Alignment Search Tool:

BLAST

mean death time:

MDT

intracerebral pathogenicity index:

ICBI

coding sequence:

CDS

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Acknowledgements

This work was supported by Razi Institute under the grant number 1-18-18-062-97020.

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Authors and Affiliations

  1. Department of Avian Diseases Research and Diagnostics, Agricultural Research, Education and Extension Organization (AREEO), Razi Vaccine and Serum Research Institute, Karaj, Iran

    Aidin Molouki, Mohammad Soltani, Mohsen Mahmoudzadeh Akhijahani, Mohammad Hossein Fallah Merhabadi, Alireza Abtin, Abdelhamid Shoushtari, Mohammad Abdoshah & Seyed Ali Pourbakhsh

  2. Department of Microbiology and Immunology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

    Arash Ghalyanchi Langeroudi

  3. Health Sciences Division, Abu Dhabi Women’s College, Higher Colleges of Technology, 41012, Abu Dhabi, United Arab Emirates

    Swee Hua Erin Lim

  4. Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

    Esmaeel Allahyari

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  1. Aidin Molouki
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Contributions

AM and MS designed and performed the experiments. MS and MHFM provided samples. EA and AM performed computer analysis. MMA and AA performed inoculation, HA and HI. MA performed MDT and ICPI. AM wrote the first draft of the manuscript. MS, SHEL, AG edited the manuscript. SAP and AS were involved in executing the study and providing laboratory space.

Corresponding author

Correspondence to Mohammad Soltani.

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Conflict of interest

The authors declare they have no conflict of interest.

Research involving human participants and/or animals

The present study did not involve any human subject. Animal handling procedures were performed in line with the national animal welfare regulations. The Institutional Animal Care and Use Committee (IACUC) of Razi Vaccine and Serum Research Institute approved all animal experiments.

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The present study did not involve any human subject.

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Supplementary Information

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Supplementary File 1

. The phylogenetic tree for all the Iranian pigeon-derived NDV made using the large dataset of the international NDV consortium. Six distinct groups were observed based on the sequence of the F gene. The evolutionary history was inferred by using the Maximum Likelihood method (bootstrap 1000) and General Time Reversible model [26]. A discrete Gamma distribution was used to model evolutionary rate differences among sites (5 categories (+G, parameter = 1.1762)). This analysis involved 1789 nucleotide sequences. Evolutionary analyses were conducted in MEGA X [18]. All the isolates of this study are marked with ●. The file must be opened in MEGA X. Supplementary file 1 (MTSX 1395 KB)

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Supplementary File 2

. Estimates of evolutionary divergence between the F gene sequences of Iranian pigeon-derived isolates and all the sequences available in the large dataset of the NDV consortium. Analyses were conducted using the Maximum Composite Likelihood model [26] and a bootstrap 1000. The rate variation among sites was modeled with a gamma distribution (shape parameter=1). The analysis involved 1789 nucleotide sequences. The file must be viewed with text editor in MEGA X. Supplementary file 2 (ZIP 5830 KB)

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Supplementary File 3

. A phylogenetic tree for the seven complete F gene CDS of the Iranian pigeon-derived NDV. The tree was constructed using the pilot dataset of the NDV consortium. The evolutionary history was inferred by using the Maximum Likelihood method (bootstrap 500) and General Time Reversible model [26]. All the isolates of this study are marked with ●. Evolutionary analyses were conducted in MEGA X [18]. Supplementary file 3 (TIF 12889 KB)

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Supplementary File 4

. Estimates of evolutionary divergence between the seven Iranian pigeon-derived NDV and the isolates in the large dataset of the NDV consortium based on the complete F gene CDS. Analyses were conducted using the Maximum Composite Likelihood model [26] and a bootstrap 500. The file must be viewed using the text editor in MEGA X. Supplementary file 4 (ZIP 7844 KB)

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Supplementary File 5

. A FASTA file prepared using all the partial/complete F gene sequences of Iranian PPMV-1 and the pilot file of the NDV consortium. The genotype/subgenotype of all the isolates is shown in their title. An updated version of the file will be available in our Google Drive (see text for URL link). Supplementary file 5 (FAS 280 KB)

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Molouki, A., Soltani, M., Akhijahani, M.M. et al. Circulation of at Least Six Distinct Groups of Pigeon-Derived Newcastle Disease Virus in Iran Between 1996 and 2019. Curr Microbiol 78, 2672–2681 (2021). https://doi.org/10.1007/s00284-021-02505-w

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