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Predominance of Fourth Panzootic Newcastle Disease Virus Subgenotype VII.1.1 in Iran and Its Relation to the Genotypes Circulating in the Region

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Abstract

Following recent Newcastle disease virus (NDV) outbreaks in Iranian poultry farms which were mostly associated with lesions of the avian gastrointestinal tract, it was speculated that the scale of the outbreaks could be attributed in part to co-circulating infectious agents or a new NDV genotype/subgenotype. This speculation was due to the isolation of a few 5th panzootic subgenotype VII.2 viruses from Iranian poultry farms in 2017. Samples from different species of commercial and domestic birds were collected from different provinces of Iran, 19 of which were selected for the current study. Phylogenetic analyses showed that the recent outbreaks have been caused by only one agent, i.e. the distinctive NDV subgenotype VII.1.1 (previously known VIIl) viruses that seem to be circulating predominantly in Iran, but have also been sporadically reported from Iraq among neighbouring countries. At most, 96.3–96.7% BLAST identity to non-Iranian VII.1.1 isolates was observed. Genetic distance values of <1% were indicative of high similarity between the isolates, but the values were approaximately 2% when the current isolates were compared to the earliest recorded Iranian VII.1.1 viruses isolated in 2010. Using Bayesian analysis, annual mutation rates of 1.7156E-3 (strict) and 1.9902E-3 (relaxed) over 11 years were obtained. In addition, we report that our laboratories have not detected any genotype XIII strains since 2011. Following up on previous reports, we concluded that currently, and except in Columbiforms, subgenotype VII.1.1 may likely be the predominant subgenotype in many bird species in Iran despite the subgenotype VII.2 being predominant in neighbouring countries.

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Funding

The research was funded by Razi Vaccine and Serum Research Institute for the project numbered 13-18-1851-070-97020-971049.

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Authors and Affiliations

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

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

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

    Esameel Allahyari

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

    Arash Ghalyanchilangeroudi

  4. Wageningen Bioveterinary Research, Wageningen University and Research, Lelystad, the Netherlands

    Marc Engelsma

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

    Swee Hua Erin Lim

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  1. Aidin Molouki
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  2. Mohammad Sotani
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Contributions

AM: designed the study, performed the experiments, carried out the computer analyses and wrote the manuscript. MS: conceived the project, provided samples, performed some experiments and revised the manuscript. MHFM: conceived and supervised the project and also provided the funding. AS: provided samples and supervised AA: assisted in the experiments and provided samples. MMA: performed all the inoculations and pathogenicity assays. SAP: provided resources. SHEL: reviewed and revised the manuscript. AGL: conceived the study and provided resources. EA: provided samples, performed experiments, carried out computer analyses. MA: performed the pathogenicity assays including ICPI. ME: performed the Bayesian analysis and revised the manuscript.

Corresponding authors

Correspondence to Aidin Molouki or Mohammad Hossein Fallah Mehrabadi.

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Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

The Institutional Animal Care and Use Committee (IACUC) of Razi Vaccine and Serum Research Institute approved all animal experiments (permit code: RVSRI.REC.99.002).

Informed Consent

The present study did not involve any human subject.

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 (Permit Code: RVSRI.REC.99.002).

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Supplementary Information

Below is the link to the electronic supplementary material.

284_2021_2572_MOESM1_ESM.docx

Supplementary file 1 A list of NDV isolates sequenced in our laboratory as well as all the local (144 isolates) and several regional (70 isolates) sequences derived from GenBank, ViPR database and publications. The list includes all the Iranian submissions to date (as of September 2020), however, all the pigeon-derived sequences and most vaccinal strains were omitted. Only the longest GenBank submission was used if multiple submissions for one isolate had been made. This included submission for different genes of one isolate since the aim of study was identifying genotypes. The F sequences were used to make phylogenetic tree and conduct Bayesian analysis. Some sequences did not include the complete CDS, yet they were studied to find the closest genotypes. Genotypes for each of the isolates were carefully determined by phylogenetic anaysis in the current study. The list is primarily sorted by country and then arranged based on the year of collection. (DOCX 174 kb)

284_2021_2572_MOESM2_ESM.fas

Supplementary file 2 A FASTA file containing all the Iranian and regional NDV F gene sequences (except those isolated from Columbiformes) is available for download (341 isolates). The dataset will be regularly updated at our online repository. See text for URL. The sequences were added to the latest pilot NDV dataset of the international NDV consortium. The other datasets of the study can be obtained by unselecting the sequences that are not required for a particular analysis. For example, the first dataset is made of the consortium pilot file and the isolates mentioned in Table 1. All the short sequences that may have contributed to error during genetic and mino acid distance analysis were removed from the file. (FAS 573 kb)

284_2021_2572_MOESM3_ESM.pdf

Supplementary file 3 A philogenetic tree made using the first dataset of this study. The dataset itself was made by adding the F gene sequence of the 19 isolates of this study (marked with ●) to the pilot file of the international NDV consortium (125+19=144 sequences). All the isolates belonged to the subgenotype VII.1.1. The evolutionary history was inferred by using the Maximum Likelihood method and General Time Reversible model [46]. The bootstrap consensus tree was inferred from 1000 replicates [47]. A discrete Gamma distribution was used to model evolutionary rate differences among sites (4 categories (+G, parameter = 0.7347)). There were a total of 1662 positions in the final dataset. Evolutionary analyses were conducted in MEGA X [24]. (PDF 133 kb)

284_2021_2572_MOESM4_ESM.tif

Supplementary file 4 A tree made using the second dataset of the current study (Supplementary File 2). The dataset was made by adding all the F gene sequences of the isolates of Supplementary File 1 to the pilot file of the international NDV consortium (total of 341 isolates). The Iranian NDV genotype VII.1.1 (formerly VIIl) formed a distinct cluster that has been consistent over a decade. Two Iraqi NDV isolated in 2012 also clustered within the Iranian group. Some Saudi Arabian VII.1.1 isolates were closely related to the Iranian VII.1.1 isolates, yet they formed a different cluster of their own (see Supplementary File 5 for genetic distances). The only VIId isolated from Iran was also shown in a different branch next to the VIId isolate included in the pilot dataset. The tree also shows the location of Iranian and regional subgenotype VII.2 NDV compared with the VII.2 isolates included in the pilot dataset of the international NDV consortium. The Iranian VII.2 isolates sided with the newly reported Belgian, Baghdadi and Israeli isolates closer than those from other countries (see Supplementary File 5 for distances). Some Iraqi VII.2 isolates from 2012 formed a different cluster. The evolutionary history was inferred using the Maximum Likelihood method and General Time Reversible model [46]. The bootstrap consensus tree was inferred from 1000 replicates [47]. A discrete Gamma distribution was used to model evolutionary rate differences among sites (4 categories (+G, parameter = 0.4727)). There were a total of 1662 positions in the final dataset. Evolutionary analyses were conducted in MEGA X [24]. All isolates used in the current study are marked: ● Iran, ■ Iraq, ▼ Turkey, ▲ Saudi Arabia, ∆ UAE, ∇ Israel, □ Belgium, ♦ Pakistan, ◊ Indonesia. (TIF 2720 kb)

284_2021_2572_MOESM5_ESM.xlsx

Supplementary file 5 Estimates of evolutionary divergence between Iranian, regional and international NDV F gene sequences. Analyses were conducted using the Maximum Composite Likelihood model [48](500 bootstrap replications). The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 340 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All ambiguous positions were removed for each sequence pair (pairwise deletion option). There were a total of 1662 positions in the final dataset. Evolutionary analyses were conducted in MEGA 7 [49]. (XLSX 691 kb)

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Molouki, A., Sotani, M., Fallah Mehrabadi, M.H. et al. Predominance of Fourth Panzootic Newcastle Disease Virus Subgenotype VII.1.1 in Iran and Its Relation to the Genotypes Circulating in the Region. Curr Microbiol 78, 3068–3078 (2021). https://doi.org/10.1007/s00284-021-02572-z

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