Updated Unified Phylogenetic Classification System and Revised Nomenclature for Newcastle 2 Disease Virus

1 Updated unified phylogenetic classification system and revised nomenclature for Newcastle 2 disease virus 3 Kiril M. Dimitrova*, Celia Abolnikb, Claudio L. Afonsoa*, Emmanuel Albinac,d, Justin Bahle, 4 Mikael Bergf, Francois-Xavier Briandg, Ian H. Brownh, Kang-Seuk Choii, Ilya Chvalaj, Diego G. 5 Dielk, Peter A. Durrl, Helena L. Ferreiraa,m, Alice Fusaron, Patricia Gild,o, Gabriela V. 6 Goujgoulovap, Christian Grundq, Joseph T. Hickse, Tony M. Joannisr, Mia Kim Torchettis, Sergey 7 Kolosovj, Bénédicte Lambrechtt, Nicola S. Lewish,u, Haijin Liuv, Sam McCulloughl, Patti J. 8 Millerw, Isabella Monnen, Claude P. Mullerx, Muhammad Muniry, Dilmara Reischakz, Mahmoud 9 Sabraaa, Siba K. Samalab, Renata Servan de Almeidad,o, Ismaila Shittur, Chantal J. Snoeckx, David 10 L. Suareza, Steven Van Bormt, Zhiliang Wangac, Frank Y. K. Wongl 11 12 aExotic and Emerging Avian Viral Disease Research Unit, Southeast Poultry Research Laboratory, 13 US National Poultry Research Center, ARS, USDA, 934 College Station Road, Athens, GA 30605, 14 USA 15 bDepartment of Production Studies, Faculty of Veterinary Science, University of Pretoria, Old 16 Soutpan Road, Onderstepoort, Pretoria, 0110, South Africa 17 cCIRAD, UMR ASTRE, F-97170 Petit-Bourg, Guadeloupe, France 18 dASTRE CIRAD, INRA, Univ Montpellier, Montpellier, France 19 eCenter for Ecology of Infectious Disease, Department of Infectious Diseases, Department of 20 Epidemiology and Biostatistics, Institute of Bioinformatics, University of Georgia, Athens, 21 Georgia, 30602, USA 22 fDepartment of Biomedical Sciences and Veterinary Public Health, Swedish University of 23 Agricultural Sciences, Box 7028, 750 07 Uppsala, Sweden 24 gANSES, Avian and Rabbit Virology Immunology and Parasitology Unit, National reference 25 laboratory for avian Influenza and Newcastle disease, BP 53 - 22440 Ploufragan, France 26 hOIE/FAO International Reference Laboratory for Newcastle Disease, Animal and Plant Health 27 Agency (APHA –Weybridge), Addlestone, KT15 3NB, UK 28 iAnimal and Plant Quarantine Agency, Ministry of Agriculture, Food and Rural Affairs (MAFRA), 29 177 Hyeoksin 8-ro, Gimcheon-si, Gyeongsangbuk-do, 39660, Republic of Korea 30 jFederal Governmental Budgetary Institution, Federal Centre for Animal Health, FGI ARRIAH, 31 Vladimir 600901, Russia 32 kDepartment of Veterinary and Biomedical Sciences, Animal Disease, Research and Diagnostic 33 Laboratory, South Dakota State University, Brookings, SD, USA 34 lCSIRO Australian Animal Health Laboratory, Portarlington Road, East Geelong, Victoria 3219, 35 Australia 36 mUniversity of Sao Paulo, ZMV- FZEA, Pirassununga, 13635900, Brazil 37 nIstituto Zooprofilattico Sperimentale delle Venezie (IZSVe), Viale dell’Università 10, Legnaro 38 35020, Italy 39 oCIRAD, UMR ASTRE, F-34398 Montpellier, France 40 pNational Diagnostic and Research Veterinary Medical Institute, 15 Pencho Slaveikov blvd., Sofia 41 1606, Bulgaria 42 qFriedrich-Loeffler-Institut, 17493 Greifswald, Insel Riems, Germany 43 rRegional Laboratory for Animal Influenzas and Transboundary Animal Diseases, National 44 Veterinary Research Institute, Vom, Nigeria 1 45 sNational Veterinary Services Laboratories, Diagnostics and Biologics, Veterinary Services, 46 Animal and Plant Health Inspection Service, U.S. Department of Agriculture, 1920 Dayton Ave, 47 Ames, IA 50010, USA 48 tInfectious Diseases in Animals, SCIENSANO, Groeselenberg 99, 1180 Ukkel, Brussels, Belgium 49 uRoyal Veterinary College, University of London, 4 Royal College Street, London NW1 0TU, UK 50 vCollege of Veterinary Medicine, Northwest A & F University, Yangling, Shaanxi, 712100, 51 People’s Republic of China 52 wDepartment of Population Health, College of Veterinary Medicine, University of Georgia, 953 53 College Station Road, Athens, GA 30602, USA 54 xInfectious Diseases Research Unit, Department of Infection and Immunity, Luxembourg Institute 55 of Health, 29, rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg 56 yDivision of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, 57 Lancaster, United Kingdom. 58 zMinistério da Agricultura, Pecuária e Abastecimento, Laboratório Federal de Defesa 59 Agropecuário, Campinas, SP, 13100-105 Brazil 60 aaDepartment of Poultry Diseases, Faculty of Veterinary Medicine, South Valley University, Qena 61 83523, Egypt 62 abVirginia-Maryland Regional College of Veterinary Medicine, University of Maryland, College 63 Park, MD, USA 64 acNational Reference Laboratory for Newcastle Disease, China Animal Health and Epidemiology 65 Center (CAHEC), 369 Nanjing Road, Qingdao 266032, China 66 67 *Corresponding authors 68 Telephone: +1 706 546 6342 69 Fax: +1 706-546-3161 70 Email address: [email protected] 71 [email protected] 2 72 ABSTRACT 73 Several Avian paramyxoviruses 1 classification systems have been proposed for strain 74 identification and differentiation. These systems pioneered classification efforts; however, they 75 were based on different approaches and lacked objective criteria for the differentiation of isolates 76 (the term Newcastle disease viruses or NDV is used hereafter). These differences have created 77 discrepancies among systems, rendering discussions and comparisons across studies difficult. 78 Although a system that used objective classification criteria was proposed by Diel and co-workers 79 in 2012, the ample worldwide circulation and constant evolution of NDV, and utilization of only 80 some of the criteria led to identical naming and/or incorrect assigning of new sub/genotypes. To 81 address these issues, an international consortium of experts was convened to undertake in-depth 82 analyses of NDV genetic diversity. This consortium generated curated, up-to-date, complete fusion 83 gene class I and class II datasets of all known NDV for public use, performed comprehensive 84 phylogenetic Neighbor-Joining, maximum-likelihood, Bayesian and nucleotide distance analyses, 85 and compared these inference methods. An updated NDV classification and nomenclature system 86 that incorporates phylogenetic topology, genetic distances, branch support, and epidemiological 87 independence was developed. This new consensus system maintains two NDV classes and existing 88 genotypes, identifies three new genotypes, and reduces the number of sub-genotypes. In order to 89 track the ancestry of viruses, a dichotomous naming system for designating sub-genotypes was 90 introduced. In addition, a pilot dataset and sub-trees rooting guidelines for rapid preliminary 91 genotype identification of new isolates are provided. Guidelines for sequence dataset curation and 92 phylogenetic inference, and a detailed comparison between the updated and previous systems are 93 included. To increase the speed of phylogenetic inference and ensure consistency between 94 laboratories, detailed guidelines for the use of a supercomputer are also provided. The proposed 95 unified classification system will facilitate future studies of NDV evolution and epidemiology, and 96 comparison of results obtained across the world. 97 98 Keywords 99 Avian paramyxovirus 1 (APMV-1); Newcastle disease virus (NDV); classification; nomenclature; 100 genotype; phylogenetic analysis 101 3 102 1. Introduction 103 The International Committee on Taxonomy of Viruses has recently created three genera, 104 named Metaavulavirus, Orthoavulavirus, and Paraavulavirus, within a new subfamily 105 Avulavirinae of the family Paramyxoviridae (ICTV, 2019). Isolates of Avian orthoavulavirus 1 106 (AOAV-1), formerly designated as Avian avulavirus 1 (AAvV-1) or Avian paramyxovirus 1 107 (APMV-1), and commonly known as Newcastle disease viruses (NDV, used hereafter for the 108 purposes of this paper), cause infections in a wide range of domestic and wild birds worldwide 109 (Amarasinghe et al., 2018; ICTV, 2019; Miller and Koch, 2013). Newcastle disease (ND), caused 110 by virulent NDV, is highly contagious and can be devastating, particularly in naïve poultry 111 (Alexander et al., 2012). Virulent strains are defined by the World Organisation for Animal Helath 112 (OIE) as viruses that have an intracerebral pathogenicity index of 0.7 or higher (2.0 is maximum) 113 or a fusion cleavage site with multiple basic amino acids and phenylalanine at position 117 (OIE, 114 2012). Newcastle disease has a global impact and 109 of 200 countries have reported the disease 115 to the OIE in the last five years (OIE, 2018). Between 2006 and 2009, ND was ranked the 8th most 116 important wildlife disease and the 3rd most significant poultry disease (Anonymous, 2011). The 117 importance of NDV infections to avian health has long been recognized, and the viruses have been 118 the subject of considerable scientific investigations over the past several decades (Alexander et al., 119 2012; Miller and Koch, 2013). The need for NDV classification has resulted in a variety of methods 120 for strain identification and differentiation (Alexander et al., 1985; Bankowski and Kinjo, 121 1965; Pennington, 1978). These early techniques were mainly based on biological properties of 122 the virus, such as pathogenicity, plaque formation, thermostability, analyses of structural 123 polypeptides, and hemagglutination inhibition patterns using monoclonal antibodies (Ballági- 124 Pordany et al., 1996; Russell and Alexander, 1983). 125 The broad circulation of NDV in poultry populations led to significant genetic diversity of 126 the virus, with the constant emergence of NDV variants. Given the clinical and economical 127 relevance of NDV to

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