WikiJournal Preprints/Beak and feather disease virus
Authors: Subir Sarker[a] , Jade K Forwood, Shane R Raidal
Sarker, S; Forwood, J; Raidal, S.
Beak and feather disease virus (BFDV) is currently a member of the family Circoviridae. Like other circoviruses, BFDV possesses small circular single-stranded DNA (ssDNA) genome (approximately 2.0 kb in length) that is encapsidated into a non-enveloped, spherical icosahedral virion (Sarker et al., 2016b). In order to replicate its genome, BFDV needs to invade the nucleus to access the transcriptional machinery of the host cell, where it causes large globular intracytoplasmic paracrystalline arrays (Figure 1) (Sarker et al., 2016b).
The BFDV genome is bi-directionally transcribed and encodes at least two major proteins; a replication initiation protein (rep) expressed from the virion strand and a capsid protein (cap) expressed from the complementary strand. In order to understand the functionality of cap and its interaction with a range of host and viral proteins, recently a study conducted by Sarker et al. confirmed that the cap protein forms virus-like particles (VLPs) of ~17 nm (mature form), and a smaller assembly of ~10 nm (immature form) (Figure 2), using a combination of X-ray crystallography, cryo-electron microscopy and atomic force microscopy (Sarker et al., 2016b). Furthermore, this study demonstrated that assembly of these two VLPs is regulated by single-stranded DNA (ssDNA), and provide a structural basis of capsid assembly around single-stranded DNA (Sarker et al., 2016b).
Figure 2 | Figure 2. Structural characterisation of two BFDV capsid virion. X-ray crystal structures allow modelling of the two particles to 1.9 Å (10 nm-immature virions, left), and 2.5 Å (60 nm-mature virions, right). The smaller particle is comprised of 10 capsid molecules arranged as two interlocking discs, with each disc containing five capsid molecules. The larger VLP is comprised of 12 pentamers arranged with T=1 icosahedral symmetry (Sarker et al., 2016b).
Host range and transmission
The BFDV infection was thought to be restricted to within Psittaciformes, but evidence of host switch in distantly-related Australian avian species was demonstrated recently in the rainbow bee-eater (Merops ornatus) (Sarker et al., 2015b), powerful owl (Ninox strenua) (Sarker et al., 2016a) and finches (Circella et al., 2014). A large number of other non-psittacine birds are likely susceptible to sporadic spill-over infection (Amery-Gale et al., 2017) and we have unpublished evidence of BFDV-associated feather disease in the Laughing Kookaburra (Daceolo novaeguineae), columbids, corvids and raptors including the Wedge-tailed Eagle (Aquila audax), White-breasted Sea Eagle (Haliaeetus leucogaster), Peregrine Falcon (Falco peregrinus) and Whistling Kite (Haliastur sphenurus) (Raidal and Peters, 2018).
Beak and feather disease virus is the dominant viral pathogen of Psittaciformes in Australasia, where it has been present for at least 10 million years (Raidal and Peters, 2018) and Australia has been identified as the most likely origin of the virus (Harkins et al., 2014). The richness of psittacine avifauna in this region has produced a mixture of potential hosts for the pathogens resulting in competing forces of virus co-evolution, spill-over infection and virus host-switches within parrots, cockatoos and lorikeets. Recent evidence has shown that all threatened and endangered Australian psittacine bird species can be infected by BFDV genotypes from any other closely- or distantly related host reservoir species (Raidal et al., 2015; Sarker et al., 2015a). Currently, more than 78 psittacine bird species globally have been reported to be infected by BFDV, including at least 38 of the 50 Australian native parrot species both in captivity and the wild, and over 25 non-psittacine bird species (Amery-Gale et al., 2017; Das et al., 2016; Department of the Environment and Heritage, 2005; Eastwood et al., 2014; Fogell et al., 2016; Raidal and Peters, 2018; Sarker et al., 2014c; Sarker et al., 2016a; Sarker et al., 2015b; Sarker et al., 2014d).
Transmission is thought to include both horizontal and vertical modalities. In wild bird populations transmission of infection most likely occurs within nest hollows by oral or intracloacal ingestion of the virus possibly sourced from feather dust, crop secretions, or faeces (Ritchie et al., 1991; Wylie and Pass, 1987). Although there has been debate in the literature concerning the role of vertical transmission of avian circovirus, BFDV is suspected to be transmitted vertically because viral DNA can be found in embryos from infected hens (Rahaus et al., 2008). However, this could simply be the result of non-replicative transfer of viral DNA into the yolk of embryonated eggs, which requires to be investigated further.
Beak and feather disease virus is the cause of Psittacine circoviral disease (or psittacine beak and feather disease (PBFD)) which is recognised as an infectious threat for endangered Australian psittacine birds and is a well characterised threat to a wide variety of psittacine and non-psittacine bird species globally (Amery-Gale et al., 2017; Das et al., 2016; Eastwood et al., 2014; Fogell et al., 2016; Raidal and Peters, 2018; Sarker et al., 2014a; Sarker et al., 2014b; Sarker et al., 2015a; Sarker et al., 2014c; Sarker et al., 2016a; Sarker et al., 2015b; Varsani et al., 2011). The disease presents as an immunosuppressive condition with chronic symmetrical irreversible loss of feather, as well as beak and claw deformities eventually leading to death (Figure 3) (Latimer et al., 1990; Pass and Perry, 1984; Raidal et al., 1993; Ritchie et al., 1990; Ritchie et al., 1989) or it can be expressed peracutely, ranging from sudden death, particularly in neonates (Ritchie, 1995) or as an acute form in nestling and fledglings, characterised by feather dystrophy, diarrhoea, weakness and depression ultimately leading to death within 1-2 weeks (Ritchie, 1995).
Secondary viral, fungal, bacterial, or parasitic infections often occur as a result of diminished immunity caused by a PBFD viral infection. Additional symptoms not mentioned above, including elevated white blood cell counts, are generally due to secondary infections and may not be directly related to PBFD virus infections.
Treatment and control
Currently, there is no specific treatment commercially viable for infected birds. Culling of infected birds is normally performed in infected captive or commercial flocks. There is an ongoing need to develop a vaccine to combat BFDV infection. It has been recommended that a combination of quarantine and hygiene control, diagnostic testing and enhancing flock adaptive immunity should be practised to provide the most effective and sustainable control (Raidal and Peters, 2018).
S.S. is funded by the Discovery Early Career Researcher Award of the Australian Research Council.
The authors have no competing interest.
Amery-Gale, J., Marenda, M.S., Owens, J., Eden, P.A., Browning, G.F., Devlin, J.M., 2017. A high prevalence of beak and feather disease virus in non-psittacine Australian birds. J Med Microbiol 66, 1005-1013.
Circella, E., Legretto, M., Pugliese, N., Caroli, A., Bozzo, G., Accogli, G., Lavazza, A., Camarda, A., 2014. Psittacine Beak and Feather Disease–like Illness in Gouldian Finches (Chloebia gouldiae). Avian Dis 58, 482-487, 486.
Das, S., Sarker, S., Peters, A., Ghorashi, S.A., Phalen, D., Forwood, J.K., Raidal, S.R., 2016. Evolution of circoviruses in lorikeets lags behind its hosts. Molecular Phylogenetics and Evolution 100, 281-291.
Department of the Environment and Heritage 2005. Threat Abatement Plan for Psittacine Beak and Feather Disease affecting endangered psittacine species. Canberra, ACT 2601: Department of the Environment and Heritage, Commonwealth of Australia. 2005. Available: http://www.environment.gov.au/system/files/resources/5764cda0-5e94-48c7-8841-49b09ff7398c/files/beak-feather-tap.pdf (Canberra, ACT, Department of the Environment and Heritage).
Eastwood, J.R., Berg, M.L., Ribot, R.F., Raidal, S.R., Buchanan, K.L., Walder, K.R., Bennett, A.T., 2014. Phylogenetic analysis of beak and feather disease virus across a host ring-species complex. Proc Natl Acad Sci U S A 111, 14153-14158.
Fogell, D.J., Martin, R.O., Groombridge, J.J., 2016. Beak and feather disease virus in wild and captive parrots: an analysis of geographic and taxonomic distribution and methodological trends. Arch Virol, 1-16.
Harkins, G.W., Martin, D.P., Christoffels, A., Varsani, A., 2014. Towards inferring the global movement of beak and feather disease virus. Virology 450–451, 24-33.
Latimer, K.S., Rakich, P.M., Kircher, I.M., Ritchie, B.W., Niagro, F.D., Steffens, W.L., Lukert, P.D., 1990. Extracutaneous viral inclusions in psittacine beak and feather disease. J Vet Diagn Invest 2, 204-207.
Pass, D.A., Perry, R.A., 1984. The pathology of psittacine beak and feather disease. Australian Veterinary Journal 61, 69-74. Rahaus, M., Desloges, N., Probst, S., Loebbert, B., Lantermann, W., Wolff, M.H., 2008. Detection of beak and feather disease virus DNA in embryonated eggs of psittacine birds. Veterinarni Medicina 53, 53–58.
Raidal, S.R., McElnea, C.L., Cross, G.M., 1993. Seroprevalence of psittacine beak and feather disease in wild psittacine birds in New South Wales. Australian Veterinary Journal 70, 137-139.
Raidal, S.R., Peters, A., 2018. Psittacine beak and feather disease: ecology and implications for conservation. Emu - Austral Ornithology 118, 80-93. Raidal, S.R., Sarker, S., Peters, A., 2015. Review of psittacine beak and feather disease and its effect on Australian endangered species. Australian Veterinary Journal 93, 466-470.
Ritchie, B.W. 1995. Circoviridae, In: Avian viruses, function and control. Wingers Publishing Inc, Lake Worth, 223-252.
Ritchie, B.W., Niagro, F.D., Latimer, K.S., Lukert, P.D., L., S.W., Rakich, P.M., Pritchard, N., 1990. Ultrastructural, protein composition, and antigenic comparison of psittacine beak and feather disease virus purified from four genera of psittacine birds. J Wildl Dis 26, 196-203.
Ritchie, B.W., Niagro, F.D., Latimer, K.S., Steffens, W.L., Pesti, D., Ancona, J., Lukert, P.D., 1991. Routes and prevalence of shedding of psittacine beak and feather disease virus. Am J Vet Res. 52, 1804-1809.
Ritchie, B.W., Niagro, F.D., Lukert, P.D., Steffens Iii, W.L., Latimer, K.S., 1989. Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology 171, 83-88.
Sarker, S., Das, S., Ghorashi, S.A., Forwood, J.K., Raidal, S.R., 2014a. Molecular characterization of genome sequences of beak and feather disease virus from the Australian Twenty-Eight Parrot (Barnardius zonarius semitorquatus). Genome Announcements 2, e01255-01214.
Sarker, S., Forwood, J.K., Ghorashi, S.A., McLelland, D., Peters, A., Raidal, S.R., 2014b. Whole-genome sequence characterization of a beak and feather disease virus in a wild regent parrot (Polytelis anthopeplus monarchoides). Genome Announcements 2, 01243-01213.
Sarker, S., Forwood, J.K., Ghorashi, S.A., Peters, A., Raidal, S.R., 2015a. Beak and feather disease virus genotypes in Australian parrots reveal flexible host-switching. Australian Veterinary Journal 93, 471-475.
Sarker, S., Ghorashi, S.A., Forwood, J.K., Bent, J.S., Peters, A., Raidal, S.R., 2014c. Phylogeny of beak and feather disease virus in cockatoos demonstrates host generalism and multiple-variant infections within Psittaciformes. Virology 460-461, 72-82.
Sarker, S., Lloyd, C., Forwood, J., Raidal, S.R., 2016a. Forensic genetic evidence of beak and feather disease virus infection in a Powerful Owl, Ninox strenua. Emu 116, 71-74.
Sarker, S., Moylan, K.G., Ghorashi, S.A., Forwood, J.K., Peters, A., Raidal, S.R., 2015b. Evidence of a deep viral host switch event with beak and feather disease virus infection in rainbow bee-eaters (Merops ornatus). Scientific Reports 5, 14511.
Sarker, S., Patterson, E.I., Peters, A., Baker, B.G., Forwood, J.K., Ghorashi, S.A., Holdsworth, M., Baker, R., Murray, N., Raidal, S.R., 2014d. Mutability dynamics of an emergent single-stranded DNA virus in a naïve host. PloS one 9, e85370.
Sarker, S., Terron, M.C., Khandokar, Y., Aragao, D., Hardy, J.M., Radjainia, M., Jimenez-Zaragoza, M., de Pablo, P.J., Coulibaly, F., Luque, D., Raidal, S.R., Forwood, J.K., 2016b. Structural insights into the assembly and regulation of distinct viral capsid complexes. Nat Commun 7, 13014.
Varsani, A., Regnard, G.L., Bragg, R., Hitzeroth, I.I., Rybicki, E.P., 2011. Global genetic diversity and geographical and host-species distribution of beak and feather disease virus isolates. Journal of General Virology 92, 752-767.
Wylie, S.L., Pass, D.A., 1987. Experimental reproduction of psittacine beak and feather disease french moult. Avian Pathol 16(2), 269-81.