Updated unified phylogenetic classification system and revised nomenclature for Newcastle disease virus

Abstract

Several Avian paramyxoviruses 1 (synonymous with Newcastle disease virus or NDV, used hereafter) classification systems have been proposed for strain identification and differentiation. These systems pioneered classification efforts; however, they were based on different approaches and lacked objective criteria for the differentiation of isolates. These differences have created discrepancies among systems, rendering discussions and comparisons across studies difficult. Although a system that used objective classification criteria was proposed by Diel and co-workers in 2012, the ample worldwide circulation and constant evolution of NDV, and utilization of only some of the criteria, led to identical naming and/or incorrect assigning of new sub/genotypes. To address these issues, an international consortium of experts was convened to undertake in-depth analyses of NDV genetic diversity. This consortium generated curated, up-to-date, complete fusion gene class I and class II datasets of all known NDV for public use, performed comprehensive phylogenetic neighbor-Joining, maximum-likelihood, Bayesian and nucleotide distance analyses, and compared these inference methods. An updated NDV classification and nomenclature system that incorporates phylogenetic topology, genetic distances, branch support, and epidemiological independence was developed. This new consensus system maintains two NDV classes and existing genotypes, identifies three new class II genotypes, and reduces the number of sub-genotypes. In order to track the ancestry of viruses, a dichotomous naming system for designating sub-genotypes was introduced. In addition, a pilot dataset and sub-trees rooting guidelines for rapid preliminary genotype identification of new isolates are provided. Guidelines for sequence dataset curation and phylogenetic inference, and a detailed comparison between the updated and previous systems are included. To increase the speed of phylogenetic inference and ensure consistency between laboratories, detailed guidelines for the use of a supercomputer are also provided. The proposed unified classification system will facilitate future studies of NDV evolution and epidemiology, and comparison of results obtained across the world.

Keywords: Avian paramyxovirus 1 (APMV-1); Classification; Genotype; Newcastle disease virus (NDV); Nomenclature; Phylogenetic analysis.

Fig. 1

Maximum likelihood phylogenetic trees of class I (A) and class II (B). Phylogenetic analyses are based on the full-length nucleotide sequence of the fusion gene of isolates representing Newcastle disease virus class I (A, n = 284) and class II (B, n = 1672). The evolutionary history was inferred by using RaxML (Stamatakis, 2014) and utilizing the Maximum Likelihood method based on the General Time Reversible model with 1000 bootstrap replicates. The trees with the highest log likelihood (class I = −18,683.27, class II = −106,684.34) are shown. A discrete gamma distribution was used to model evolutionary rate differences among sites and the rate variation model allowed for some sites to be evolutionarily invariable. For imaging purposes, the taxa tips are not displayed and colors are randomly assigned to indicate the different sub/genotypes. Three new class II genotypes assigned in the current study are highlighted in red font. The trees are drawn to scale, with branch lengths measured in the number of substitutions per site. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Class II “pilot” tree. Phylogenetic analysis is based on the full-length nucleotide sequence of the fusion gene of selected isolates representing all class II Newcastle disease virus sub/genotypes (n = 125). The evolutionary history was inferred by using RaxML (Stamatakis, 2014) and utilizing the Maximum Likelihood method based on the General Time Reversible model with 1000 bootstrap replicates. The tree with the highest log likelihood (−28,785.59) is shown. A discrete gamma distribution was used to model evolutionary rate differences among sites and the rate variation model allowed for some sites to be evolutionarily invariable. The Roman numerals presented in the taxa names in the phylogenetic tree represent the respective genotype for each isolate. The new (decimal naming) and the old names (alpha-numerical) are provided for easier comparison. The taxa names also include the GenBank identification number, host name, country of isolation, strain designation, and year of isolation. Three new genotypes assigned in the current study are highlighted in red font. The trees are drawn to scale, with branch lengths measured in the number of substitutions per site. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)