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Molecular and Microscopic Characterisation of a Novel Veterinary Microbiology 239 (2019) 108428 Contents lists available at ScienceDirect Veterinary Microbiology journal homepage: www.elsevier.com/locate/vetmic Molecular and microscopic characterisation of a novel pathogenic T herpesvirus from Indian ringneck parrots (Psittacula krameri) Michelle Sutherlanda,*, Subir Sarkerb,c,**, Shane R. Raidalc a Burwood Bird and Animal Hospital, 128 Highbury Rd, Burwood, Vic, 3125, Australia b Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University, Bundoora, Vic, 3086, Australia c Veterinary Diagnostic Laboratory, Charles Sturt University, Wagga Wagga, NSW, 2678, Australia ARTICLE INFO ABSTRACT Keywords: A high morbidity, high mortality disease process caused flock deaths in an Indian ringneck parrot (Psittacula Psittacine krameri) aviary flock in Victoria, Australia. Affected birds were either found dead with no prior signs ofillness,or Herpesvirus showed clinical evidence of respiratory tract disease, with snicking, sneezing and dyspnoea present in affected Indian ringneck birds. Necropsy examinations performed on representative birds, followed by cytological and histopathological Next-generation sequencing examination, demonstrated lesions consistent with a herpesvirus bronchointerstitial pneumonia. Transmission Transmission electron microscopy electron microscopy analysis of lung tissue demonstrated typical herpesvirus virions measuring approximately 220 nm in diameter. Next generation sequencing of genomic DNA from lung tissue revealed a highly divergent novel Psittacid alphaherpesvirus of the genus Iltovirus. Iltoviruses have been previously reported to cause re- spiratory disease in a variety of avian species, but molecular characterisation of the viruses implicated has been lacking. This study presents the genome sequence of a novel avian herpesvirus species designated Psittacid al- phaherpesvirus-5 (PsHV-5), providing an insight into the evolutionary relationships of the alphaherpesviruses. 1. Introduction Of the nineteen known avian herpesviruses, alphaherpesviruses of the genus Iltovirus have been documented to cause respiratory disease. The Herpesviridae are a diverse family of enveloped, double-stranded Gallid alphaherpesvirus-1 (GaHV-1) causes infectious laryngotracheitis DNA viruses found in many different orders of vertebrates, including (ILT) in gallinaceous birds. This manifests as either a mild form asso- birds, reptiles, amphibians, fish and mammals (McGeoch and Davison, ciated with moderate mucoid tracheitis, conjunctivitis, and laryngeal 1999). Herpesviruses have been further classified into the subfamilies and tracheal haemorrhage, or a severe form causing diptheritic plaque that include alpha-, beta- and gammaherpesviruses. These classifica- formation in the larynx and trachea that may extend into the lungs and tions were initially based on the properties of the viruses described, air sacs (Benton and Cover, 1958; Garcia et al., 2013). with alphaherpesviruses associated with rapid viral replication, the In parrots, three alphaherpesviruses have been described; Psittacid ability to cause host cell lysis, and the capacity to establish latent in- alphaherpesvirus-1 (PsHV-1; also known as Pacheco’s Disease), PsHV-2, fections (Lazic et al., 2008). However, phylogenetic relationships of and PsHV-3. The viral genome of PsHV-1 consists of 163,025 base pairs herpesviruses are now formally based on their genetic characteristics, (bp) (GenBank accession no. AY372243), and has been classified into as defined by homology or nucleic acid sequences and the identification four genotypes with distinct biological characteristics (Thureen and of particular genes that are unique to each subfamily (McGeoch and Keeler, 2006; Tomaszewski et al., 2003). Psittacid alphaherpesvirus-2 and Davison, 1999). All currently available sequence data derived from PsHV-1 are closely related viruses, and both have the ability to cause avian herpesviruses have been consistent with the alphaherpesvirus mucosal papilloma development, while PsHV-1 additionally causes an subfamily (McGeoch and Davison, 1999; VanDevanter et al., 1996). acute, rapidly fatal hepatic necrosis, or the insidious development bile Although alphaherpesviruses are fairly species specific, they typically duct and pancreatic duct neoplasms some months or years after initial exhibit a more variable host range compared to beta- or gamma- infection. In addition, a herpesvirus with a tropism for the respiratory herpesviruses, and are able to establish latent infections in sensory tract has been reported in various avian species, but confirmed by ge- ganglia (Roizman et al., 1992). netic sequencing only in Bourke’s parrots (Neopsephotus bourkii) and ⁎ Corresponding author. Present address: The Unusual Pet Vets, 210 Karingal Drive, Frankston, Vic, 3199, Australia. ⁎⁎ Corresponding author at: Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University, Bundoora, Vic, 3086, Australia. E-mail addresses: [email protected] (M. Sutherland), [email protected] (S. Sarker), [email protected] (S.R. Raidal). https://doi.org/10.1016/j.vetmic.2019.108428 Received 24 July 2019; Received in revised form 19 September 2019; Accepted 20 September 2019 0378-1135/ © 2019 Elsevier B.V. All rights reserved. M. Sutherland, et al. Veterinary Microbiology 239 (2019) 108428 eclectus parrots (Eclectus roratus)(Gabor et al., 2013; Shivaprasad and 0.45 μm filter. The filtrate was then adsorbed onto a 400-mesh copper Phalen, 2012). Phylogenetic analysis of the virus affecting these species EM grid coated with a thin film of carbon for 5 min. Excess solution was suggested a novel psittacid alphaherpesvirus in the genus Iltovirus, with removed using 3 MM filter paper (Whatman) and the grid rinsed briefly the suggested name Psittacid alphaherpesvirus-3 (PsHV-3) (Shivaprasad with distilled water before negative staining with three 10 s applica- and Phalen, 2012). However, this nomenclature has yet to be ratified by tions of 2% [w/v] uranyl acetate (Electron Microscopy Sciences, PA, the International Committee on Taxonomy of Viruses (ICTV, 2018). USA) followed by removal of excess stain on filter paper after each Typical histological lesions associated with PsHV-3 as reported in these application. Grids were air-dried for 20 min before imaging on a JEOL species included the presence of intranuclear inclusion bodies within JEM-2100 transmission electron microscope as previously described epithelial and syncytial cells of the trachea, bronchi, air capillaries and (Sarker et al., 2017a, 2018). air sacs, with an absence of upper respiratory tract disease (Lazic et al., 2008; Raidal et al., 1995; Shivaprasad and Phalen, 2012). A viral re- 2.4. DNA extraction, library construction, and sequencing spiratory infection with similar histopathological findings has also been described in Indian ringneck parrots (Psittacula krameri), Amazon par- Based on the suspicion that the herpesvirus inclusions seen on his- rots (Amazona spp.), cockatiels (Nymphicus hollandicus) eastern rosellas topathology in this case may be caused by the same herpesvirus as (Platycercus eximus) and princess parrots (Polyterlis alexandrae)(Lazic previously described in Indian ringnecks, (Helfer et al., 1980; Lazic et al., 2008; Tsai et al., 1993). However, in these reports, phylogenetic et al., 2008; Tsai et al., 1993) an attempt to determine the genome analyses of the implicated virus were not performed, so while it has sequence of the virus was undertaken. been supposed that PsHV-3 was the causative agent based on simila- Collected lung tissue was aseptically dissected and mechanically rities in clinical findings and histopathology, a definitive aetiological homogenised in lysis buffer using disposable tissue grinder pestles, then diagnosis should not be assumed in these cases. Phylogenetic analysis transferred into a 1.5 mL microcentrifuge tube (Eppendorf). Total has shown that Psittacid alphaherpesvirus-3 is more closely related to genomic DNA was isolated according to established methods (Sarker GaHV-1 and Passerid herpesvirus-1, a virus causing tracheitis and et al., 2018) using a ReliaPrep gDNA Tissue Miniprep System (Promega, bronchitis in Gouldian finches (Erythrura gouldiae)(Wellehan et al., USA). The Illumina Nextera XT DNA Library Prep V3 Kit was used for 2003), than PsHV-1 or PsHV-2. Additionally, Magellanic penguin her- quantification and quality assessment of the extracted DNA, followed pesvirus-1 (MagHV-1) has been associated with an outbreak of high by library preparation according to our published protocol (Sarker mortality respiratory disease in Magellanic penguins (Sphensicus ma- et al., 2018, 2017b). The quality and quantity of the prepared library gellanicus) in a rehabilitation facility (Niemeyer et al., 2017). Phylo- was assessed using an Agilent Tape Station (Agilent Technologies) genetic analyses grouped this virus with Gaviid herpesvirus-1 (GavHV-1), under the La Trobe University Genomics Platform. The prepared library a virus associated with respiratory disease in common loons (Gavia was normalised and pooled in equimolar quantity. The quality and immer)(Niemeyer et al., 2017; Quesada et al., 2011). quantity of the final pooled library was further assessed as described The aims of this study were to report the clinical, pathological and above before sequencing by the facility. Cluster generation and se- microscopic findings associated with a novel herpesvirus causing dis- quencing of
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