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Article

Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Northern Royal Albatross (Diomedea sanfordi)

by
Subir Sarker
1,*,
Ajani Athukorala
1,
Tadiwa Nyandowe
1,
Timothy R. Bowden
2,† and
David B. Boyle
2
1
Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University, Melbourne, VIC 3086, Australia
2
CSIRO Livestock Industries, Australian Animal Health Laboratory, Geelong, VIC 3220, Australia
*
Author to whom correspondence should be addressed.
†
Present address: CSIRO Australian Animal Health Laboratory, Australian Centre for Disease Preparedness, Geelong, VIC 3220, Australia.
Pathogens 2021, 10(5), 575; https://doi.org/10.3390/pathogens10050575
Submission received: 14 April 2021 / Revised: 5 May 2021 / Accepted: 6 May 2021 / Published: 9 May 2021
(This article belongs to the Collection Feature Papers in Viral Pathogens)
Browse Figures
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Abstract

:
Marine bird populations have been declining globally with the factors driving this decline not fully understood. Viral diseases, including those caused by poxviruses, are a concern for endangered seabird species. In this study we have characterised a novel avipoxvirus, tentatively designated albatrosspox virus (ALPV), isolated from a skin lesion of an endangered New Zealand northern royal albatross (Diomedea sanfordi). The ALPV genome was 351.9 kbp in length and contained 336 predicted genes, seven of which were determined to be unique. The highest number of genes (313) in the ALPV genome were homologs of those in shearwaterpox virus 2 (SWPV2), while a further 10 were homologs to canarypox virus (CNPV) and an additional six to shearwaterpox virus 1 (SWPV1). Phylogenetic analyses positioned the ALPV genome within a distinct subclade comprising recently isolated avipoxvirus genome sequences from shearwater, penguin and passerine bird species. This is the first reported genome sequence of ALPV from a northern royal albatross and will help to track the evolution of avipoxvirus infections in this endangered species.

1. Introduction

Marine bird populations have been declining globally [1] with the sustainability of the albatrosses (family Diomedeidae) and large petrels (Macronectes and Procellaria spp.) being of particular concern [2,3,4]. This group includes some of the world’s most endangered bird species, with rapidly decreasing populations and their conservation status markedly deteriorating in recent years [5,6]. The northern royal albatross (Diomedea sanfordi), which is one of the largest seabirds in the world, is categorised as an “endangered” species under the International Union for Conservation of Nature (IUCN) Red List and is ranked as Category B for conservation priority [7]. The northern royal albatrosses range widely throughout the Southern Ocean, though rarely into Antarctic waters. The breeding range is restricted to the Chatham Islands and Taiaroa Head on the Otago Peninsula, Dunedin, New Zealand. The total breeding population in the Chatham Islands colonies (99% of the total) is estimated at approximately 6500–7000 pairs, which equates to a total population of 17,000 mature individuals [8]. Northern royal albatrosses are normally solitary foragers, but they may congregate at food sources at sea. Most of their food is thought to be obtained by seizing dead or dying prey from the surface and also by scavenging discards and offal from fishing boats. Breeding birds forage over the continental shelves to shelf edges in New Zealand waters. Non-breeding and young birds can be found anywhere in the Southern Ocean throughout the year, with the main wintering areas off the coasts of southern South America [8].
Human activities such as fisheries and pollution have been documented as threats for incidental mortality of these species [7,9,10,11,12,13]. Invasive alien species, degradation or loss of nesting habitats, storms and flooding, and marine pollution or plastic ingestion are also significant factors in population declines [6,7]. Infectious diseases, including those caused by avipoxviruses, have been identified as an important risk factor in the conservation of small and endangered bird populations, including albatrosses [14,15,16,17,18,19]. The impact of the introduction of avipoxviruses has been severe for the avifauna of various archipelagos [20]. For example, the emergence of an avipoxvirus with a high prevalence (88%) in Hawaiian Laysan albatrosses (Phoebastria immutabilis) enabled one of the first detailed studies of the epidemiology and population-level impact of the disease in these seabirds [21].
Avipoxviruses are large, double-stranded DNA (dsDNA) viruses comprising the genus Avipoxvirus. They occur worldwide and are known to infect a large number of wild and domestic avian species across 76 families and 20 orders [22,23,24]. The behaviour of wild birds allows avian poxviruses to reach new hosts through bird migration, species introductions, and habitat change. Avipoxviruses have been identified as an important risk factor in the conservation of endangered bird populations [19,25]. In affected birds, avipoxvirus infection can cause two different forms of disease, defined as cutaneous or diphtheritic. The cutaneous form is characterised by proliferative ‘wart-like’ lesions that commonly develop on unfeathered body areas, including the eyes, feet, legs, face and around the beak. The less common diphtheritic form is characterised by soft and yellowish cankers and proliferative lesions on the mucous membranes of the upper alimentary and respiratory tracts [23,26,27].
Little is known about the effects of poxviruses on some bird taxa, particularly for seabird species including the northern royal albatross (D. sanfordi). The aim of the present study was to characterise the genome sequence of a novel poxvirus, which was isolated from a skin lesion that was collected in 1997 from an endangered northern royal albatross on the Otago Peninsula, near Dunedin, on the South Island of New Zealand.

2. Results

2.1. Genome of ALPV

The complete genome of ALPV was assembled into a contiguous sequence of linear double-stranded DNA 351,909 bp in length (the second-largest avipoxvirus genome so far characterised) and submitted to GenBank under accession number MW365933. Like many other avipoxviruses [25,28,29], the ALPV genome contained a well-conserved central coding region surrounded by two identical inverted terminal repeat (ITR) regions, comprising 4069 bp each (coordinates 1–4069 sense and 347,841–351,909 antisense orientation). The nucleotide composition of the ALPV genome was A + T rich (69.9%), which was in agreement with other avipoxviruses isolated from yellow-eyed penguin [19], shearwater [25] and passerine bird species [30,31] (Table 1). The ALPV genome showed the highest nucleotide identities with penguinpox virus 2 (PEPV2, GenBank accession no. MW296038) (98.92%), followed by shearwaterpox virus 2 (SWPV2, GenBank accession no. KX857216) (95.75%), canarypox virus (CNPV, GenBank accession no. AY318871) (92.71%) and mudlarkpox virus (MLPV, GenBank accession no. MK903864) (88.47%) (Table 1).

2.2. Genome Annotation and Comparative Analyses of ALPV

The ALPV genome encoded 336 putative genes, 45 to 1936 amino acids in length, that have been numbered from left to right (Figure 1 and Table 2). Among them, four ORFs were located within the inverted terminal repeats (ITRs) and were therefore present as diploid copies. Comparative analysis of the predicted ORF sequences was performed, and a significant number of ORFs (329) were found to be homologs with other chordopoxvirus (ChPV) gene products (Table 2). Among these conserved ChPV gene products, the highest number of protein-coding genes (313) in ALPV were homologs to the recently isolated SWPV2 [25]. The remaining ten gene products (ALPV-079, -155, -163, -165, -166, -167, -168, -175, -233 and -236) were homologous to ORFs of CNPV, and a further six gene products (ALPV-003, -009, -090, -127, -229 and -334) were homologs to SWPV1 (Table 2). All conserved genes of ALPV showed the highest sequence similarity to homologs of avipoxviruses isolated from Pacific shearwater, canary and yellow-eyed penguin bird species, implying a common evolutionary history [19,25,32]. In comparison to SWPV2, two gene products (SWPV2-121 and -213) were absent from the ALPV genome, and a further nineteen genes were predicted to be truncated/fragmented (Figure 1 and Table 2). In comparison to vaccinia virus strain Copenhagen (VACV-Cop), 138 ORFs of ALPV showed homology to VACV-Cop and the sequence identities ranging from 20.9–76.7% (Table 2).
Interestingly, ALPV contained seven predicted protein-coding genes (ORF030, -067, -080, -081, -213, -226 and -227) that were not present in any other characterised poxvirus genomes, nor did they match any sequences in the NR protein database using BLASTX and BLASTP; these unique ORFs encoded proteins of 51 to 89 amino acids in length (Table 2). Furthermore, four of these unique protein-coding genes (ALPV-ORF030, -213, -226 and -227) were predicted to contain a single transmembrane helix (TMH) using the software packages employed in this study (Table 2). However, we did not find any known motif, nor significant homology with known proteins, for the unique ORFs encoded in the ALPV genome when using the Phyre2, HHpred and SWISS-MODEL, which might be due to the lack of closely related structures in the database.
Comparison of the ALPV genome to that of other avipoxviruses was performed using dot plot analyses. The ALPV genome was shown to be highly syntenic with SWPV2, PEPV2, CNPV and MLPV (Figure 2A–D) and demonstrated significant differences compared to SWPV1, PEPV, FGPV and TKPV (black and orange arrows, Figure 2E–H).

2.3. Evolutionary Relationships of ALPV

Phylogenetic analysis using concatenated amino acid sequences of the selected nine core poxvirus proteins supported the inclusion of the newly assembled ALPV in the genus Avipoxvirus. In the maximum likelihood (ML) tree, ALPV was located within a sub-clade comprising SWPV2, PEPV2 and CNPV with strong bootstrap support (100%) (Figure 3), suggesting that it may represent an ancient evolutionary lineage within the genus. Using the same set of concatenated protein sequences, we found that the maximum inter-lineage sequence identity values were 100% among ALPV, SWPV2 and PEPV2, which mirrored the phylogenetic position of this novel avipoxvirus sequenced from an endangered northern royal albatross. A large number of poxviruses were positioned in the phylogenetic tree when we used partial nucleotide sequences of the DNA polymerase gene (Supplementary Figure S1) and p4b gene (Supplementary Figure S2). We discovered that several other avipoxviruses were represented within the ALPV, PEPV2, CNPV, SWPV2, MPPV and MLPV clade. This included a poxvirus isolated from a common bullfinch (Pyrrhula pyrrhula) in Belgium [35] and a northern harrier (Circus cyaneus) in Spain [35], which is almost identical to ALPV within this relatively small fragment of the genome.

3. Discussion

This study presents the characterisation of the complete genome sequence of a novel avipoxvirus, ALPV, isolated from cutaneous pox lesions in a juvenile northern royal albatross. In addition to the highest number of genes being homologous to SWPV2, a further ten were homologs to CNPV and six to SWPV1. An additional seven genes were not present in any other known poxvirus, nor did they match any sequences in the NR protein database. Given this genome structure, gene content, genome nucleotide similarities and phylogenetic relationships, the authors postulate that the ALPV genome is most closely related to avipoxviruses isolated from shearwater, penguin and canary bird species.
It has been reported that an avipoxvirus may have caused the death of some northern royal albatrosses in 1997 [37]. However, as far as we are aware, there have been no further scientific studies investigating the epidemiology and characteristics of avipoxviruses circulating in this population. Moreover, avipoxviruses have been reported to be a significant cause of chick mortality in several other albatross species. For instance, an avipoxvirus spread by bird fleas has caused high chick mortalities in some seasons within colonies of shy albatrosses (Thalassarche cauta) in Tasmania [38] and may act as a potential threat to adults and chicks of Buller’s albatross (Thalassarche bulleri) [37]. An avipoxvirus has also been described as a key threat for the rapid population decline of a critically endangered seabird, the waved Albatross (Phoebastria irrorata), in the Galápagos Islands, Ecuador [39]. Given the conservation status of the northern royal albatross, it would be important to improve understanding of the epidemiology, transmission and genetic diversity of circulating avipoxviruses, including ALPV, and the threat that they pose to this and other albatross species.
Identifying the transmission mode is essential to characterise incidence, ecology, and effective control of disease in wild populations. However, it is not yet known how this avipoxvirus is transmitted. Mechanical transmission by biting arthropods is thought to play a role in the transmission of avipoxviruses within wild bird populations. Ticks, fleas [40], hippoboscid flies [41], and mosquitos [20,42] are all potential mechanical vectors. It would therefore seem likely that, as for other avipoxviruses, transmission of ALPV in the northern royal albatross is also mediated by insect vectors. Moreover, poxvirus infection can also occur through ingestion, parenteral inoculation, or droplet or aerosol exposure to mucous membranes or broken skin. Some poxviruses can be transmitted by fomites (inanimate objects) [43]. For example, studies have revealed that sheeppox and goatpox viruses are predominantly transmitted via aerosols [44]; whereas poxviruses from the genus Parapoxvirus can pass from one animal to another through direct or indirect contact. However, unfortunately, there are no available studies addressing whether closely related avipoxviruses employ similar or different routes of spread.
There are a number of factors that threaten the populations of large sea birds, particularly albatrosses. Amongst these are longline fishing, climate change and diseases such as those caused by avipoxviruses. It is well-established in the literature that avipoxviruses are mechanically transmitted by biting insects. Although yet to be confirmed, it is therefore expected that this will also be the case for ALPV.

4. Materials and Methods

4.1. Sampling and Virus Isolation

Cutaneous pox lesions were collected from an endangered juvenile northern royal albatross (Diomedea sanfordi), located on the Otago Peninsula, near Dunedin, on the South Island of New Zealand. Sampling was conducted in March 1997 by Wallaceville Animal Research Centre, New Zealand, and lesions sent to the Australian Animal Health Laboratory, Geelong, Victoria, Australia (sample ID: SL 08/05/1997). Virus isolation was undertaken by homogenisation of the tissue samples (~10% w/v) in the presence of antibiotics. This material was then inoculated onto the chorioallantoic membranes (CAMs) of 10 to 12 day old embryonated chicken eggs. The CAMs were harvested 3 to 5 days later and examined for the presence of pock lesions. The infected CAMs were similarly homogenised and passaged onto fresh CAMs. Similarly, the homogenised tissue samples were inoculated onto monolayers of chicken embryo skin cells and examined for 7 to 10 days for the development of cytopathic effect. Additional passages were undertaken with frozen and thawed tissue culture cells inoculated onto fresh chicken embryo skin cells. All passages were stored frozen at −80 °C.

4.2. DNA Extraction and Sequencing

Infected cell culture pellets were digested with DNAase and RNAase, and then with trypsin. Released virus was pelleted through a 36% sucrose cushion for 80 min at 20,000 rpm. Poxvirus cores were released from the pelleted virus with 1% Triton X100 and mercaptoethanol by incubation for 10 min on ice. The released cores were pelleted through a 36% sucrose cushion and the viral DNA released by Proteinase K/RNAase digestion followed by phenol/chloroform extraction and ethanol precipitation, as reported previously [45,46]. Sequencing was undertaken using TruSeq (Illumina) protocols and standard multiplex adaptors available in March 2011. A paired-end 100-base-read protocol was used for sequencing on an Illumina GAIIx instrument using a previously established protocol [47].

4.3. Genome Assembly and Annotation

The resulting 3,343,202 paired-end raw sequence reads were used to assemble the complete genome of ALPV as described previously [25,31,48,49] using CLC Genomics Workbench (version 9.5.4, CLC bio, a QIAGEN Company, Prismet, Aarhus C, Denmark) and Geneious (version 10.2.2, Biomatters, New Zealand). Briefly, the sequences were processed to remove Illumina adapters, low quality reads and ambiguous bases. Trimmed sequence reads were mapped against the chicken genome (Gallus gallus, GenBank accession number NC_006088) to remove likely host DNA contamination. In addition, reads were further mapped to Escherichia coli bacterial genomic sequence (GenBank accession no. U00096) to remove possible bacterial contamination. Unmapped reads were used as input data for de novo assembly using CLC Genomics Workbench (version 9.5.4). This resulted in the generation of a 351,909 bp genome. Clean raw reads (1.15 million) were mapped back to the assembled ALPV genome and resulted in an average coverage of 136.33x. The genome was annotated according to the previously published protocol [19] using Geneious software (version 10.2.2, Biomatters, Auckland, New Zealand). Open reading frames (ORFs) longer than 50 amino acids, with a methionine start codon (ATG) and minimal overlap with other ORFs (not exceeding 50% of one of the genes), were selected and annotated. ORFs shorter than 50 amino acids that had been previously annotated in other poxvirus genomes were also included. Similarity BLAST searches were performed on the predicted ORFs and were annotated as potential genes if predicted ORFs showed significant sequence similarity to known viral or cellular genes (BLAST E value ≤ e−5) [50]. Additional BLAST searches were performed on the predicted ORFs of ALPV against VACV-Cop [51].
To predict the function of unique ORFs tentatively identified in this study, the derived protein sequence of each ORF was searched by multiple applications to identify conserved domains or motifs. Transmembrane helices were searched using the TMHMM package (version 2.0) [52] and TMpred [53]. Additionally, searches for conserved secondary structure (HHpred) [54] and protein homologs using Phyre2 [55] were used to predict the function of unique ORFs identified in this study. To identify the likely promoter sequences of predicted unique ORFs of ALPV, a promoter motif search analysis was conducted using CLC Genomic Workbench (version 9.5.4), where vaccinia virus unique promoter sequences were used [51,56,57,58].

4.4. Comparative Genomics

Genomic features of the newly sequenced ALPV were visualised using Geneious (version 10.2.2). Sequence similarity percentages between representative ChPV and ALPV complete genome sequences were determined using tools available in Geneious (version 10.2.2). Dot plots were created based on the EMBOSS dottup program in Geneious software, with word size = 12 [59].

4.5. Phylogenetic Analyses

Phylogenetic analyses were performed using the novel ALPV genome sequence determined in this study, together with other selected ChPV genome sequences available in GenBank (Table 3). Nucleotide sequences of the partial DNA polymerase and partial p4b genes, as well as concatenated amino acid sequences of the selected nine poxvirus core proteins, were aligned as described previously [30] using the MAFTT L-INS-I algorithm implemented in Geneious (version 7.388) [60]. To determine the best-fit model to construct phylogenetic analyses, a model test was performed using CLC Genomics Workbench (version 9.5.4), which favoured a general-time-reversible model with gamma distribution rate variation and a proportion of invariable sites (GTR+G+I). Phylogenetic analyses for nucleotide sequences were performed using the GTR substitution model with 1000 bootstrap support in CLC Genomics Workbench (version 9.5.4), but the LG substitution model was chosen for concatenated amino acid sequences in Geneious (version 10.2.2).

5. Conclusions

This study reports the genomic characterisation of a novel avipoxvirus, ALPV, isolated from an endangered northern royal albatross. The ALPV genome sequence was sufficiently divergent from other known avipoxviruses to be considered a novel species within the genus Avipoxvirus, family Poxviridae. This discovery has enhanced our understanding of the pathogen landscape relevant to northern royal albatrosses in New Zealand. Obtaining and sequencing additional poxvirus isolates will also be important to further investigate the epidemiology, transmission, pathogenesis and host specificity of ALPV infections in this endangered bird species.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/pathogens10050575/s1, Figure S1: Maximum likelihood (ML) phylogenetic tree from partial nucleotide sequences of the DNA polymerase gene of selected avipoxviruses, Figure S2: Maximum likelihood phylogenetic tree from partial nucleotide sequences of the p4b gene of selected avipoxviruses.

Author Contributions

Conceptualization, S.S., T.R.B. and D.B.B.; Formal analysis, S.S., A.A., T.N. and D.B.B.; Funding acquisition, S.S. and D.B.B.; Investigation, S.S. and D.B.B.; Methodology, S.S. and D.B.B.; Writing—original draft, S.S.; Writing—review and editing, S.S., A.A., T.N., T.R.B. and D.B.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The complete genome sequence and associated datasets generated during this study were deposited in GenBank under the accession number MW365933.

Acknowledgments

Subir Sarker is the recipient of an Australian Research Council Discovery Early Career Researcher Award (grant number DE200100367) funded by the Australian Government. We also gratefully acknowledge the funding contributed by the Australian Biosecurity CRC for Emerging Infectious Disease in support of this work. The authors are thankful to the New Zealand Ministry for Primary Industries, Animal Health Laboratory, for providing the skin lesion from which ALPV was isolated.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

References

  1. Croxall, J.P.; Butchart, S.H.M.; Lascelles, B.E.N.; Stattersfield, A.J.; Sullivan, B.E.N.; Symes, A.; Taylor, P. Seabird conservation status, threats and priority actions: A global assessment. Bird Conserv. Int. 2012, 22, 1–34. [Google Scholar] [CrossRef] [Green Version]
  2. Croxall, J.P.; Gales, R. An assessment of the conservation status of albatrosses. In Albatross Biology and Conservation; Robertson, G., Gales, R., Eds.; Surrey Beatty & Sons: Chipping Norton, UK, 1998; pp. 46–65. [Google Scholar]
  3. Cooper, J.; Baker, G.B.; Double, M.C.; Gales, R.; Papworth, W.; Tasker, M.L.; Waugh, S.M. The agreement on the conservation of albatrosses and petrels: Rationale, history, progress and the way forward. Mar. Ornithol. 2006, 34, 1–5. [Google Scholar]
  4. Marcela, M.; Uhart, L.G.; Flavio, Q. Review of diseases (pathogen isolation, direct recovery and antibodies) in albatrosses and large petrels worldwide. Bird Conserv. Int. 2017, 28, 1–28. [Google Scholar] [CrossRef] [Green Version]
  5. Paleczny, M.; Hammill, E.; Karpouzi, V.; Pauly, D. Population Trend of the World’s Monitored Seabirds, 1950–2010. PLoS ONE 2015, 10, e0129342. [Google Scholar] [CrossRef]
  6. Phillips, R.A.; Gales, R.; Baker, G.B.; Double, M.C.; Favero, M.; Quintana, F.; Tasker, M.L.; Weimerskirch, H.; Uhart, M.; Wolfaardt, A. The conservation status and priorities for albatrosses and large petrels. Biol. Conserv. 2016, 201, 169–183. [Google Scholar] [CrossRef]
  7. BirdLife International. Diomedea Sanfordi. The IUCN Red List of Threatened Species 2018: E.T22728323A132656392. 2018. Available online: https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22728323A132656392.en (accessed on 30 January 2021).
  8. Sugishita, J. Northern royal albatross. In New Zealand Birds Online; Miskelly, C.M., Ed.; 2013; Available online: http://www.nzbirdsonline.org.nz/species/northern-royal-albatross (accessed on 20 January 2021).
  9. Halpern, B.S.; Walbridge, S.; Selkoe, K.A.; Kappel, C.V.; Micheli, F.; D’Agrosa, C.; Bruno, J.F.; Casey, K.S.; Ebert, C.; Fox, H.E.; et al. A global map of human impact on marine ecosystems. Science 2008, 319, 948–952. [Google Scholar] [CrossRef] [Green Version]
  10. Tuck, G.N.; Polacheck, T.; Croxall, J.P.; Weimerskirch, H. Modelling the impact of fishery by-catches on albatross populations. J. Appl. Ecol. 2001, 38, 1182–1196. [Google Scholar] [CrossRef] [Green Version]
  11. Baker, G.B.; Gales, R.; Hamilton, S.; Wilkinson, V. Albatrosses and petrels in Australia: A review of their conservation and management. Emu Austral Ornithol. 2002, 102, 71–97. [Google Scholar] [CrossRef]
  12. Lewison, R.L.; Crowder, L.B.; Read, A.J.; Freeman, S.A. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 2004, 19, 598–604. [Google Scholar] [CrossRef]
  13. Rolland, V.; Barbraud, C.; Weimerskirch, H. Assessing the impact of fisheries, climate and disease on the dynamics of the Indian yellow-nosed Albatross. Biol. Conserv. 2009, 142, 1084–1095. [Google Scholar] [CrossRef]
  14. Department of Sustainability, Environment, Water, Population and Communities (2011) Background Paper, Population Status and Threats to Albatrosses and Giant Petrels Listed as Threatened under the Environment Protection and Biodiversity Conservation Act 1999. Commonwealth of Australia, Hobart. 2011. Available online: https://www.environment.gov.au/resource/background-paper-population-status-and-threats-albatrosses-and-giant-petrels-listed. (accessed on 29 January 2021).
  15. Illera, J.C.; Emerson, B.C.; Richardson, D.S. Genetic characterization, distribution and prevalence of avian pox and avian malaria in the Berthelot’s pipit (Anthus berthelotii) in Macaronesia. Parasitol. Res. 2008, 103, 1435–1443. [Google Scholar] [CrossRef]
  16. Lecis, R.; Secci, F.; Antuofermo, E.; Nuvoli, S.; Scagliarini, A.; Pittau, M.; Alberti, A. Multiple gene typing and phylogeny of avipoxvirus associated with cutaneous lesions in a stone curlew. Vet. Res. Commun. 2017, 1–7. [Google Scholar] [CrossRef]
  17. Woolaver, L.G.; Nichols, R.K.; Morton, E.S.; Stutchbury, B.J.M. Population genetics and relatedness in a critically endangered island raptor, Ridgway’s Hawk Buteo ridgwayi. Conserv. Genet. 2013, 14, 559–571. [Google Scholar] [CrossRef]
  18. Thiel, T.; Whiteman, N.K.; Tirape, A.; Baquero, M.I.; Cedeno, V.; Walsh, T.; Uzcategui, G.J.; Parker, P.G. Characterization of canarypox-like viruses infecting endemic birds in the Galapagos Islands. J. Wildl. Dis. 2005, 41, 342–353. [Google Scholar] [CrossRef] [Green Version]
  19. Sarker, S.; Athukorala, A.; Bowden, T.R.; Boyle, D.B. Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Yellow-Eyed Penguin (Megadyptes antipodes). Viruses 2021, 13, 194. [Google Scholar] [CrossRef]
  20. van Riper, C., III; van Riper, S.G.; Hansen, W.R. Epizootiology and Effect of Avian Pox on Hawaiian Forest Birds. Auk 2002, 119, 929–942. [Google Scholar] [CrossRef]
  21. Young, L.C.; VanderWerf, E.A. Prevalence of avian pox virus and effect on the fledging success of Laysan Albatross. J. Field Ornithol. 2008, 79, 93–98. [Google Scholar] [CrossRef]
  22. Bolte, A.L.; Meurer, J.; Kaleta, E.F. Avian host spectrum of avipoxviruses. Avian Pathol. 1999, 28, 415–432. [Google Scholar] [CrossRef] [Green Version]
  23. van Riper, C.; Forrester, D.J. Avian Pox. In Infectious Diseases of Wild Birds; Thomas, N.J., Hunter, D.B., Atkinson, C.T., Eds.; Wiley Blackwell Publishing: Oxford, UK, 2007; pp. 131–176. [Google Scholar]
  24. Carulei, O.; Douglass, N.; Williamson, A.-L. Comparative analysis of avian poxvirus genomes, including a novel poxvirus from lesser flamingos (Phoenicopterus minor), highlights the lack of conservation of the central region. BMC Genom. 2017, 18, 947. [Google Scholar] [CrossRef]
  25. Sarker, S.; Das, S.; Lavers, J.L.; Hutton, I.; Helbig, K.; Imbery, J.; Upton, C.; Raidal, S.R. Genomic characterization of two novel pathogenic avipoxviruses isolated from pacific shearwaters (Ardenna spp.). BMC Genom. 2017, 18, 298. [Google Scholar] [CrossRef] [Green Version]
  26. Tripathy, D.N.; Schnitzlein, W.M.; Morris, P.J.; Janssen, D.L.; Zuba, J.K.; Massey, G.; Atkinson, C.T. Characterization of poxviruses from forest birds in Hawaii. J. Wildl. Dis. 2000, 36, 225–230. [Google Scholar] [CrossRef] [Green Version]
  27. Niemeyer, C.; Favero, C.M.; Kolesnikovas, C.K.M.; Bhering, R.C.C.; Brandão, P.; Catão-Dias, J.L. Two different avipoxviruses associated with pox disease in Magellanic penguins (Spheniscus magellanicus) along the Brazilian coast. Avian Pathol. 2013, 42, 546–551. [Google Scholar] [CrossRef] [Green Version]
  28. Joshi, L.R.; Bauermann, F.V.; Hain, K.S.; Kutish, G.F.; Armién, A.G.; Lehman, C.P.; Neiger, R.; Afonso, C.L.; Tripathy, D.N.; Diel, D.G. Detection of Fowlpox virus carrying distinct genome segments of Reticuloendotheliosis virus. Virus Res. 2019, 260, 53–59. [Google Scholar] [CrossRef]
  29. Afonso, C.L.; Tulman, E.R.; Lu, Z.; Zsak, L.; Kutish, G.F.; Rock, D.L. The genome of fowlpox virus. J. Virol. 2000, 74, 3815–3831. [Google Scholar] [CrossRef] [Green Version]
  30. Sarker, S.; Athukorala, A.; Raidal, S.R. Molecular characterisation of a novel pathogenic avipoxvirus from an Australian passerine bird, mudlark (Grallina cyanoleuca). Virology 2021, 554, 66–74. [Google Scholar] [CrossRef]
  31. Sarker, S.; Batinovic, S.; Talukder, S.; Das, S.; Park, F.; Petrovski, S.; Forwood, J.K.; Helbig, K.J.; Raidal, S.R. Molecular characterisation of a novel pathogenic avipoxvirus from the Australian magpie (Gymnorhina tibicen). Virology 2020, 540, 1–16. [Google Scholar] [CrossRef]
  32. Tulman, E.R.; Afonso, C.L.; Lu, Z.; Zsak, L.; Kutish, G.F.; Rock, D.L. The Genome of Canarypox Virus. J. Virol. 2004, 78, 353–366. [Google Scholar] [CrossRef] [Green Version]
  33. Offerman, K.; Carulei, O.; van der Walt, A.P.; Douglass, N.; Williamson, A.-L. The complete genome sequences of poxviruses isolated from a penguin and a pigeon in South Africa and comparison to other sequenced avipoxviruses. BMC Genom. 2014, 15, 1–17. [Google Scholar] [CrossRef] [Green Version]
  34. Banyai, K.; Palya, V.; Denes, B.; Glavits, R.; Ivanics, E.; Horvath, B.; Farkas, S.L.; Marton, S.; Balint, A.; Gyuranecz, M.; et al. Unique genomic organization of a novel Avipoxvirus detected in turkey (Meleagris gallopavo). Infect Genet. Evol. 2015, 35, 221–229. [Google Scholar] [CrossRef]
  35. Gyuranecz, M.; Foster, J.T.; Dán, Á.; Ip, H.S.; Egstad, K.F.; Parker, P.G.; Higashiguchi, J.M.; Skinner, M.A.; Höfle, U.; Kreizinger, Z.; et al. Worldwide Phylogenetic Relationship of Avian Poxviruses. J. Virol. 2013, 87, 4938–4951. [Google Scholar] [CrossRef] [Green Version]
  36. Sarker, S.; Isberg, S.R.; Milic, N.L.; Lock, P.; Helbig, K.J. Molecular characterization of the first saltwater crocodilepox virus genome sequences from the world’s largest living member of the Crocodylia. Sci. Rep. 2018, 8, 5623. [Google Scholar] [CrossRef] [Green Version]
  37. Graeme, A.T. Action Plan for Seabird Conservation in New Zealand. Part A: Threatened Seabirds. Threatened Species Occasional Publication, 1170-3709; 16, Biodiversity Recovery Unit, Department of Conservation, Wellington, New Zealand. 2000. Available online: https://www.doc.govt.nz/documents/science-and-technical/tsop16.pdf (accessed on 30 January 2021).
  38. Woods, R. Results of a Preliminary Disease Survey in Shy Albatross (Thalassarche Cauta Gould 1841) Chicks at Albatross Island, Bass Strait, Tasmania; Woods, R., Ed.; Australian Association of Veterinary Conservation Biologists: Canberra, Australia, 2004; pp. 98–104. [Google Scholar]
  39. Tompkins, E.M.; Anderson, D.J.; Pabilonia, K.L.; Huyvaert, K.P. Avian Pox Discovered in the Critically Endangered Waved Albatross (Phoebastria irrorata) from the Galápagos Islands, Ecuador. J. Wildl. Dis. 2017, 53, 891–895. [Google Scholar] [CrossRef] [PubMed]
  40. Kane, O.J.; Uhart, M.M.; Rago, V.; Pereda, A.J.; Smith, J.R.; Van Buren, A.; Clark, J.A.; Boersma, P.D. Avian pox in Magellanic Penguins (Spheniscus magellanicus). J. Wildl. Dis. 2012, 48, 790–794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  41. Warner, R.E. The Role of Introduced Diseases in the Extinction of the Endemic Hawaiian Avifauna. Condor 1968, 70, 101–120. [Google Scholar] [CrossRef]
  42. Annuar, B.O.; Mackenzie, J.S.; Lalor, P.A. Isolation and characterization of avipoxviruses from wild birds in Western Australia. Arch. Virol. 1983, 76, 217–229. [Google Scholar] [CrossRef]
  43. Aleksandr, K.; Olga, B.; David, W.B.; Pavel, P.; Yana, P.; Svetlana, K.; Alexander, N.; Vladimir, R.; Dmitriy, L.; Alexander, S. Non-vector-borne transmission of lumpy skin disease virus. Sci. Rep. 2020, 10, 7436. [Google Scholar] [CrossRef] [PubMed]
  44. Kitching, R.P.; Taylor, W.P. Transmission of capripoxvirus. Res. Vet. Sci. 1985, 39, 196–199. [Google Scholar] [CrossRef]
  45. Nakano, E.; Panicali, D.; Paoletti, E. Molecular genetics of vaccinia virus: Demonstration of marker rescue. Proc. Natl. Acad. Sci. USA 1982, 79, 1593–1596. [Google Scholar] [CrossRef] [Green Version]
  46. Prideaux, C.T.; Boyle, D.B. Fowlpox virus polypeptides: Sequential appearance and virion associated polypeptides. Arch. Virol. 1987, 96, 185–199. [Google Scholar] [CrossRef]
  47. Sarker, S.; Roberts, H.K.; Tidd, N.; Ault, S.; Ladmore, G.; Peters, A.; Forwood, J.K.; Helbig, K.; Raidal, S.R. Molecular and microscopic characterization of a novel Eastern grey kangaroopox virus genome directly from a clinical sample. Sci. Rep. 2017, 7, 16472. [Google Scholar] [CrossRef] [Green Version]
  48. Boyle, D.B.; Bulach, D.M.; Amos-Ritchie, R.; Adams, M.M.; Walker, P.J.; Weir, R. Genomic sequences of Australian blue-tongue virus prototype serotypes reveal global relationships and possible routes of entry into Australia. J. Virol. 2012, 86, 6724–6731. [Google Scholar] [CrossRef] [Green Version]
  49. Sarker, S.; Isberg, S.R.; Athukorala, A.; Mathew, R.; Capati, N.; Haque, M.H.; Helbig, K.J. Characterization of a Complete Genome Sequence of Molluscum Contagiosum Virus from an Adult Woman in Australia. Microbiol. Resour. Announc. 2021, 10, e00939-20. [Google Scholar] [CrossRef]
  50. Benson, D.A.; Cavanaugh, M.; Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2013, 41, D36–D42. [Google Scholar] [CrossRef] [Green Version]
  51. Yang, Z.; Bruno, D.P.; Martens, C.A.; Porcella, S.F.; Moss, B. Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc. Natl. Acad. Sci. USA 2010, 107, 11513. [Google Scholar] [CrossRef] [Green Version]
  52. Krogh, A.; Larsson, B.; von Heijne, G.; Sonnhammer, E.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001, 305, 567–580. [Google Scholar] [CrossRef] [Green Version]
  53. Hofmann, K.; Stoffel, W. TMBASE—A database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 1993, 374, 166. [Google Scholar]
  54. Zimmermann, L.; Stephens, A.; Nam, S.Z.; Rau, D.; Kubler, J.; Lozajic, M.; Gabler, F.; Soding, J.; Lupas, A.N.; Alva, V. A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core. J. Mol. Biol. 2018, 430, 2237–2243. [Google Scholar] [CrossRef]
  55. Kelley, L.A.; Mezulis, S.; Yates, C.M.; Wass, M.N.; Sternberg, M.J.E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 2015, 10, 845. [Google Scholar] [CrossRef] [Green Version]
  56. Yang, Z.; Reynolds, S.E.; Martens, C.A.; Bruno, D.P.; Porcella, S.F.; Moss, B. Expression profiling of the intermediate and late stages of poxvirus replication. J. Virol. 2011, 85, 9899–9908. [Google Scholar] [CrossRef] [Green Version]
  57. Yang, Z.; Maruri-Avidal, L.; Sisler, J.; Stuart, C.A.; Moss, B. Cascade regulation of vaccinia virus gene expression is modulated by multistage promoters. Virology 2013, 447, 213–220. [Google Scholar] [CrossRef] [Green Version]
  58. Goebel, S.J.; Johnson, G.P.; Perkus, M.E.; Davis, S.W.; Winslow, J.P.; Paoletti, E. The complete DNA sequence of vaccinia virus. Virology 1990, 179, 247–266. [Google Scholar] [CrossRef]
  59. Maizel, J.V., Jr.; Lenk, R.P. Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc. Natl. Acad. Sci. USA 1981, 78, 7665–7669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Sarker, S.; Hannon, C.; Athukorala, A.; Bielefeldt-Ohmann, H. Emergence of a Novel Pathogenic Poxvirus Infection in the Endangered Green Sea Turtle (Chelonia mydas) Highlights a Key Threatening Process. Viruses 2021, 13, 219. [Google Scholar] [CrossRef]
  62. Croville, G.; Le Loc’h, G.; Zanchetta, C.; Manno, M.; Camus-Bouclainville, C.; Klopp, C.; Delverdier, M.; Lucas, M.-N.; Donnadieu, C.; Delpont, M.; et al. Rapid whole-genome based typing and surveillance of avipoxviruses using nanopore sequencing. J. Virol. Methods 2018, 261, 34–39. [Google Scholar] [CrossRef]
  63. Sarker, S.; Athukorala, A.; Bowden, T.R.; Boyle, D.B. Characterisation of an Australian fowlpox virus carrying a near-full-length provirus of reticuloendotheliosis virus. Arch. Virol. 2021, 166, 1485–1488. [Google Scholar] [CrossRef]
  64. Afonso, C.L.; Tulman, E.R.; Delhon, G.; Lu, Z.; Viljoen, G.J.; Wallace, D.B.; Kutish, G.F.; Rock, D.L. Genome of Crocodilepox Virus. J. Virol. 2006, 80, 4978–4991. [Google Scholar] [CrossRef] [Green Version]
  65. Sarker, S.; Isberg, R.S.; Moran, L.J.; Araujo, D.R.; Elliott, N.; Melville, L.; Beddoe, T.; Helbig, J.K. Crocodilepox Virus Evolutionary Genomics Supports Observed Poxvirus Infection Dynamics on Saltwater Crocodile (Crocodylus porosus). Viruses 2019, 11, 1116. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. Comparative genomic illustration of the novel ALPV. A sequence alignment using MAFFT in Geneious (version 10.2.2) was performed to compare ORFs between albatrosspox virus (ALPV, GenBank accession no. MW365933) and shearwaterpox virus 2 (SWPV2, GenBank accession no. KX857215). The arrows symbolise genes and open reading frames (ORFs), with orientation indicating their direction of transcription. Each gene or ORF is colour coded, as indicated by the key in the legend. The top graph represents the mean pairwise sequence identity over all pairs in the column between ALPV and SWPV2 (green: 100% identity; mustard: ≥30% and <100% identity; red: <30% identity).
Figure 1. Comparative genomic illustration of the novel ALPV. A sequence alignment using MAFFT in Geneious (version 10.2.2) was performed to compare ORFs between albatrosspox virus (ALPV, GenBank accession no. MW365933) and shearwaterpox virus 2 (SWPV2, GenBank accession no. KX857215). The arrows symbolise genes and open reading frames (ORFs), with orientation indicating their direction of transcription. Each gene or ORF is colour coded, as indicated by the key in the legend. The top graph represents the mean pairwise sequence identity over all pairs in the column between ALPV and SWPV2 (green: 100% identity; mustard: ≥30% and <100% identity; red: <30% identity).
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Figure 2. Dot plots of the ALPV genome (x-axis) vs. other poxvirus genomes (y-axis). (A) ALPV vs SWPV2, (B) ALPV vs PEPV2, (C) ALPV vs CNPV, (D) ALPV vs MLPV, (E) ALPV vs SWPV1, (F) ALPV vs PEPV, (G) ALPV vs FGPV and (H) ALPV vs TKPV (refer to Table 2 for virus details and GenBank accession numbers). The Classic colour scheme was chosen in Geneious (version 10.2.2) for the dot plot lines according to the length of the match, from blue for short matches to red for matches over 100 bp long. Window size = 12.
Figure 2. Dot plots of the ALPV genome (x-axis) vs. other poxvirus genomes (y-axis). (A) ALPV vs SWPV2, (B) ALPV vs PEPV2, (C) ALPV vs CNPV, (D) ALPV vs MLPV, (E) ALPV vs SWPV1, (F) ALPV vs PEPV, (G) ALPV vs FGPV and (H) ALPV vs TKPV (refer to Table 2 for virus details and GenBank accession numbers). The Classic colour scheme was chosen in Geneious (version 10.2.2) for the dot plot lines according to the length of the match, from blue for short matches to red for matches over 100 bp long. Window size = 12.
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Figure 3. Phylogenetic relationships between ALPV and other chordopoxviruses. A maximum likelihood (ML) tree was constructed from multiple alignments of the concatenated amino acid sequences of the selected nine poxvirus core proteins using CLC Genomic Workbench (version 9.5.4, CLC bio, a QIAGEN Company, Prismet, Aarhus C, Denmark). The numbers on the left show bootstrap values as percentages. The ML tree is displayed as a phylogram. The labels at branch tips refer to original ChPV GenBank accession numbers followed by abbreviated species names. Saltwater crocodilepox virus (SwCRV1) [36] was used as an outgroup. The position of the novel ALPV is highlighted using a purple box and the subclade relevant to ALPV is shown with pink shading.
Figure 3. Phylogenetic relationships between ALPV and other chordopoxviruses. A maximum likelihood (ML) tree was constructed from multiple alignments of the concatenated amino acid sequences of the selected nine poxvirus core proteins using CLC Genomic Workbench (version 9.5.4, CLC bio, a QIAGEN Company, Prismet, Aarhus C, Denmark). The numbers on the left show bootstrap values as percentages. The ML tree is displayed as a phylogram. The labels at branch tips refer to original ChPV GenBank accession numbers followed by abbreviated species names. Saltwater crocodilepox virus (SwCRV1) [36] was used as an outgroup. The position of the novel ALPV is highlighted using a purple box and the subclade relevant to ALPV is shown with pink shading.
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Table
Table 1. Comparative analysis of representative avipoxviruses and ALPV based on complete genome nucleotide sequences.
Table 1. Comparative analysis of representative avipoxviruses and ALPV based on complete genome nucleotide sequences.
Avipoxviruses (Abbreviation)GenBank Accession NumbersGenome Identity (%)Genome Length (kbp)A + T Content (%)Number of ORFsReferences
Albatrosspox virus (ALPV)MW365933 35269.9336This study
Penguinpox virus 2 (PEPV2)MW29603898.9235069.9327[19]
Shearwaterpox virus 2 (SWPV2)KX85721595.7535169.8312[25]
Canarypox virus (CNPV)AY31887192.7136069.6328[32]
Mudlarkpox virus (MLPV)MT97805188.4734370.2352[30]
Magpiepox virus (MPPV)MK90386478.7529370.4301[31]
Shearwaterpox virus 1 (SWPV1)KX85721661.4432772.4310[25]
Penguinpox virus (PEPV)KJ85967749.8330770.5285[33]
Fowlpox virus (FWPV)AF19810048.8928969.1260[29]
Pigeonpox virus (FeP2)KJ80192047.5428270.5271[33]
Flamingopox virus (FGPV)MF67879646.5129370.5285[24]
Turkeypox virus (TKPV)KP72811033.3918970.2171[34]
Table
Table 2. Albatrosspox virus (ALPV) genome annotations and comparative analysis of ORFs.
Table 2. Albatrosspox virus (ALPV) genome annotations and comparative analysis of ORFs.
ALPV SyntenyALPV Genome CoordinatesSWPV2 SyntenyALPV AA SizeSWPV2 AA SizeSWPV2 BLAST HitsALPV AA Identity (%) Compared to AvipoxvirusesALPV AA Identity (%) Compared to VACV-CopVACV BLAST HitsNotes
ALPV-001827-1342SWPV2-001171171SWPV2-001 hypothetical protein100 identical to ALPV-336
ALPV-0022271-1645SWPV2-002208208SWPV2-002 C-type lectin-like protein100 identical to ALPV-335
ALPV-0032553-2326 75 56.1 SWPV1-002 C-type lectin-like protein, identical to ALPV-334
ALPV-0042679-3347SWPV2-003222222SWPV2-003 conserved hypothetical protein100 identical to ALPV-333
ALPV-0053464-3925SWPV2-004153134SWPV2-004 conserved hypothetical protein86.9 identical to ALPV-332
ALPV-0064899-4042SWPV2-005285169SWPV2-005 C-type lectin-like protein46.9
ALPV-0075455-4946SWPV2-005169169SWPV2-005 C-type lectin-like protein100
ALPV-0087809-5743SWPV2-006688688SWPV2-006 ankyrin repeat protein100 23.9 B4R
ALPV-0098828-8184 214 43.1 SWPV1-006 ankyrin repeat protein
ALPV-01011218-9458SWPV2-007586586SWPV2-007 ankyrin repeat protein100 28.8 M1L
ALPV-01111483-12052SWPV2-008189189SWPV2-008 conserved hypothetical protein100
ALPV-01212765-12259SWPV2-009168168SWPV2-009 conserved hypothetical protein100
ALPV-01314555-13083SWPV2-010490490SWPV2-010 Ig-like domain protein100
ALPV-01414719-16368SWPV2-011549528SWPV2-011 ankyrin repeat protein96.2 28.7 M1L
ALPV-01516429-16935SWPV2-012168168SWPV2-012 C-type lectin-like protein100 24.0 A40R
ALPV-01617039-18478SWPV2-013479479SWPV2-013 ankyrin repeat protein100 26.7 B4R
ALPV-01719149-18577SWPV2-014190190SWPV2-014 IL-10-like protein100
ALPV-01820576-19266SWPV2-015436436SWPV2-015 ankyrin repeat protein100 27.5 M1L
ALPV-01920767-22026SWPV2-016419419SWPV2-016 ankyrin repeat protein100 38.2 M1L
ALPV-02023769-22162SWPV2-017535535SWPV2-017 ankyrin repeat protein100 21.5 B4R
ALPV-02124886-23810SWPV2-018358358SWPV2-018 putative serpin100 27.9 C12L
ALPV-02226242-24968SWPV2-019424424SWPV2-019 vaccinia C4L/C10L-like protein100-
ALPV-02326520-27056SWPV2-020178178SWPV2-020 hypothetical protein100
ALPV-02428172-27270SWPV2-021300300SWPV2-021 alpha-SNAP-like protein100
ALPV-02529443-28295SWPV2-022382382SWPV2-022 ankyrin repeat protein100 22.0 C9L
ALPV-02631392-29512SWPV2-023626626SWPV2-023 ankyrin repeat protein100
ALPV-02732608-31511SWPV2-024365365SWPV2-024 ankyrin repeat protein100
ALPV-02833146-32718SWPV2-025142142SWPV2-025 C-type lectin-like protein100
ALPV-02934224-33202SWPV2-026340340SWPV2-026 ankyrin repeat protein100 26.8 B4R
ALPV-03034487-34287 66 hypothetical protein, unique to ALPV, containing a transmembrane helix
ALPV-03134467-34826SWPV2-027119119SWPV2-027 hypothetical protein100
ALPV-03235782-35054SWPV2-028242242SWPV2-028 Ig-like domain putative IFN-gamma binding protein100
ALPV-03336598-35858SWPV2-029246246SWPV2-029 Ig-like domain protein100
ALPV-03438673-36694SWPV2-030659659SWPV2-030 ankyrin repeat protein100 23.5 K1L
ALPV-03539392-38991SWPV2-031133133SWPV2-031 C-type lectin-like protein100
ALPV-03639776-39489SWPV2-0329595SWPV2-032 conserved hypothetical protein100
ALPV-03739840-40379SWPV2-033179179SWPV2-033 conserved hypothetical protein100
ALPV-03841625-40384SWPV2-034413413SWPV2-034 vaccinia C4L/C10L-like protein99.8 24.3 C10L
ALPV-03941743-42726SWPV2-035327327SWPV2-035 G protein-coupled receptor-like protein100
ALPV-04044520-42745SWPV2-036591591SWPV2-036 ankyrin repeat protein99.7 23.2 B4R
ALPV-04145885-44593SWPV2-037430430SWPV2-037 ankyrin repeat protein100 27.7 B18R
ALPV-04247751-45934SWPV2-038605605SWPV2-038 ankyrin repeat protein100 21.6 B4R
ALPV-04348462-47857SWPV2-039201201SWPV2-039 conserved hypothetical protein100
ALPV-04449946-48504SWPV2-040480480SWPV2-040 ankyrin repeat protein100 25.2 B18R
ALPV-04550212-51210SWPV2-041332332SWPV2-041 G protein-coupled receptor-like protein100-
ALPV-04652589-51237SWPV2-042450450SWPV2-042 ankyrin repeat protein100 29.7 VACV-Cop-B4R
ALPV-04753030-52656SWPV2-043124124SWPV2-043 conserved hypothetical protein100
ALPV-04855603-53198SWPV2-044801801SWPV2-044 alkaline phosphodiesterase-like protein100
ALPV-04956143-55691SWPV2-045150150SWPV2-045 hypothetical protein100
ALPV-05057255-56197SWPV2-046352352SWPV2-046 ankyrin repeat protein100
ALPV-05158528-57302SWPV2-047408408SWPV2-047 DNase II-like protein100
ALPV-05259069-58554SWPV2-048171171SWPV2-048 C-type lectin-like protein100
ALPV-05359689-59249SWPV2-049146146SWPV2-049 conserved hypothetical protein100
ALPV-05460104-59682SWPV2-050140140SWPV2-050 conserved hypothetical protein100
ALPV-05560647-60156SWPV2-051163163SWPV2-051 conserved hypothetical protein100
ALPV-05661081-60644SWPV2-052145145SWPV2-052 CNLV056 dUTPase100 52.8 F2L
ALPV-05762028-61108SWPV2-053306306SWPV2-053 putative serpin100
ALPV-05862601-62059SWPV2-054180180SWPV2-054 bcl-2 like protein100
ALPV-05963674-62658SWPV2-055338338SWPV2-055 putative serpin100
ALPV-06064555-63743SWPV2-056270206SWPV2-056 conserved hypothetical protein99.5
ALPV-06166342-64645SWPV2-057565565SWPV2-057 DNA ligase100 46.9 A50R
ALPV-06267433-66381SWPV2-058350350SWPV2-058 putative serpin100 25.0 K2L
ALPV-06368580-67504SWPV2-059358358SWPV2-059 hydroxysteroid dehydrogenase-like protein100 38.2 A44L
ALPV-06469493-68642SWPV2-060283283SWPV2-060 TGF-beta-like protein100
ALPV-06571324-69573SWPV2-061583583SWPV2-061 semaphorin-like protein100 31.7 A39R
ALPV-06671606-71424SWPV2-06260399SWPV2-062 hypothetical protein100
ALPV-06771608-71784 59 hypothetical protein, unique to ALPV
ALPV-06872000-71728SWPV2-06290399SWPV2-062 hypothetical protein90.8
ALPV-06972255-72082SWPV2-0635757SWPV2-063 hypothetical protein100
ALPV-07072415-73188SWPV2-064257257SWPV2-064 GNS1/SUR4-like protein100
ALPV-07173281-73748SWPV2-065155155SWPV2-065 late transcription factor VLTF-210046.6A1L
ALPV-07273765-75420SWPV2-066551551SWPV2-066 putative rifampicin resistance protein, IMV assembly10056.2D13L
ALPV-07375452-76321SWPV2-067289289SWPV2-067 mRNA capping enzyme small subunit100 57.5 D12L
ALPV-07476342-77283SWPV2-068313132SWPV2-068 CC chemokine-like protein100
ALPV-07577690-77361SWPV2-069109109SWPV2-069 hypothetical protein100
ALPV-07677761-79668SWPV2-070635635SWPV2-070 NPH-I, transcription termination factor100 60.8 D11L
ALPV-07780351-79665SWPV2-071228228SWPV2-071 mutT motif putative gene expression regulator100 38.0 D10R
ALPV-07881048-80335SWPV2-072237232SWPV2-072 mutT motif97.9 46.3 D9R
ALPV-07981601-81287 104 100 CNPV-077 hypothetical protein
ALPV-08081796-82065 89 hypothetical protein, unique to ALPV
ALPV-08182693-82448 81 hypothetical protein, unique to ALPV
ALPV-08283172-82690SWPV2-073160160SWPV2-073 RNA polymerase subunit RPO18100 57.5 D7R
ALPV-08384332-83508SWPV2-074274274SWPV2-074 Ig-like domain protein100
ALPV-08486356-84455SWPV2-075633633SWPV2-075 early transcription factor small subunit VETFS100 72.2 D6R
ALPV-08587561-86560SWPV2-076333334SWPV2-076 Ig-like domain protein98.8
ALPV-08690271-87887SWPV2-077794794SWPV2-077 NTPase, DNA replication100 54.3 D5R
ALPV-08791091-90426SWPV2-078221221SWPV2-078 CC chemokine-like protein100
ALPV-08891830-91174SWPV2-079218218SWPV2-079 uracil DNA glycosylase99.5 54.2 D4R
ALPV-08992626-91871SWPV2-080251303SWPV2-080 putative RNA phosphatase94.734.1H1L
ALPV-09093861-92674 395 71.9 SWPV1-075 conserved hypothetical protein
ALPV-09193946-94311SWPV2-081121112SWPV2-081 TNFR-like protein80.833.9B28R
ALPV-09296471-96866SWPV2-082131131SWPV2-082 putative glutathione peroxidase100
ALPV-09396891-97193SWPV2-083100100SWPV2-083 conserved hypothetical protein100
ALPV-09497677-97198SWPV2-084159159SWPV2-084 conserved hypothetical protein100
ALPV-09598047-97664SWPV2-085127127SWPV2-085 conserved hypothetical protein100
ALPV-09698384-98133SWPV2-0868383SWPV2-086 HT motif protein100
ALPV-09799122-98736SWPV2-087128146SWPV2-087 conserved hypothetical protein87.7
ALPV-098100027-99224SWPV2-088267267SWPV2-088 virion protein100
ALPV-099100102-100929SWPV2-089275275SWPV2-089 T10-like protein100
ALPV-100101074-100937SWPV2-0904545SWPV2-090 conserved hypothetical protein100
ALPV-101101313-101056SWPV2-0918585SWPV2-091 ubiquitin100
ALPV-102102422-101445SWPV2-092325339SWPV2-092 conserved hypothetical protein95.9
ALPV-103102692-102450SWPV2-0938080SWPV2-093 hypothetical protein100
ALPV-104103285-102698SWPV2-094195195SWPV2-094 beta-NGF-like protein100
ALPV-105103815-103309SWPV2-095168168SWPV2-095 putative interleukin binding protein100
ALPV-106104127-103870SWPV2-0968585SWPV2-096 hypothetical protein100
ALPV-107104455-104138SWPV2-097105105SWPV2-097 conserved hypothetical protein100
ALPV-108105044-104472SWPV2-098190190SWPV2-098 N1R/p28-like protein100
ALPV-109105246-105623SWPV2-099125125SWPV2-099 putative glutaredoxin 2, virion morphogenesis10032.2G4L
ALPV-110106270-105566SWPV2-100234234SWPV2-100 putative elongation factor100
ALPV-111106264-106572SWPV2-101102102SWPV2-101 conserved hypothetical protein100
ALPV-112106708-106941SWPV2-1027777SWPV2-102 hypothetical protein100
ALPV-113107186-109084SWPV2-103632632SWPV2-103 putative metalloprotease, virion morphogenesis100 43.9 G1L
ALPV-114111113-109068SWPV2-104681681SWPV2-104 NPH-II, RNA helicase100 43.8 I8R
ALPV-115111148-112416SWPV2-105422422SWPV2-105 virion core proteinase100 54.4 I7L
ALPV-116112421-113596SWPV2-106391391SWPV2-106 DNA-binding protein100 34.8 I6L
ALPV-117113597-113842SWPV2-1078181SWPV2-107 putative IMV membrane protein100
ALPV-118113864-114403SWPV2-108179179SWPV2-108 thymidine kinase100 52.0 J2R
ALPV-119114524-114772SWPV2-1098282SWPV2-109 HT motif protein100
ALPV-120114842-115711SWPV2-110289289SWPV2-110 DNA-binding phosphoprotein99.7 33.5 I3L
ALPV-121115712-115921SWPV2-1116969SWPV2-111 conserved hypothetical protein100
ALPV-122115928-116860SWPV2-112310310SWPV2-112 DNA-binding virion protein100 58.0 I1L
ALPV-123117040-118998SWPV2-113652652SWPV2-113 conserved hypothetical protein100 20.9 O1L
ALPV-124118928-119323SWPV2-114131131SWPV2-114 virion core protein100 34.98 E11L
ALPV-125119601-119320SWPV2-1159393SWPV2-115 putative IMV redox protein, virus assembly100 51.6 E10R
ALPV-126119628-122594SWPV2-116988988SWPV2-116 DNA polymerase100 50.3 E9L
ALPV-127123413-122586 275 80.4 48.2 E8RSWPV1-111 putative membrane protein
ALPV-128125130-123415SWPV2-117571502SWPV2-117 conserved hypothetical protein87.2 49.9 E6R
ALPV-129130930-125192SWPV2-11819121916SWPV2-118 variola B22R-like protein99.8
ALPV-130136264-130997SWPV2-11917551767SWPV2-119 variola B22R-like protein99.3
ALPV-131142243-136544SWPV2-12018991839SWPV2-120 variola B22R-like protein95.5
ALPV-132142444-142992SWPV2-122182182SWPV2-122 RNA polymerase subunit RPO30100 57.0 E4L
ALPV-133143024-145189SWPV2-123721721SWPV2-123 conserved hypothetical protein100 28.0 E2L
ALPV-134145182-146600SWPV2-124472472SWPV2-124 poly(A) polymerase large subunit PAPL100 50.5 E1L
ALPV-135146953-146594SWPV2-125119119SWPV2-125 DNA-binding virion core protein100 38.8 F17R
ALPV-136147029-147652SWPV2-126207207SWPV2-126 conserved hypothetical protein100
ALPV-137147746-148192SWPV2-127148148SWPV2-127 conserved hypothetical protein100 40.4 F15L
ALPV-138148426-148725SWPV2-1289999SWPV2-128 conserved hypothetical protein100
ALPV-139154234-148796SWPV2-12918121801SWPV2-129 variola B22R-like protein99.4
ALPV-140154384-155520SWPV2-130378378SWPV2-130 putative palmitoylated EEV envelope lipase100 38.0 F13L
ALPV-141155598-157475SWPV2-131625625SWPV2-131 putative EEV maturation protein100 26.3 F12L
ALPV-142157518-158906SWPV2-132462462SWPV2-132 conserved hypothetical protein100 27.0 F11L
ALPV-143158997-160331SWPV2-133444444SWPV2-133 putative serine/threonine protein kinase, virus assembly100 53.6 F10L
ALPV-144160306-160947SWPV2-134213213SWPV2-134 conserved hypothetical protein100 31.5 F9L
ALPV-145161030-161230SWPV2-1356666SWPV2-135 conserved hypothetical protein100
ALPV-146161556-162110SWPV2-136184184SWPV2-136 HAL3-like domain protein100
ALPV-147162371-163336SWPV2-137321321SWPV2-137 N1R/p28-like protein100
ALPV-148163448-165463SWPV2-138671671SWPV2-138 ankyrin repeat protein100 26.0 M1L
ALPV-149165489-167159SWPV2-139556556SWPV2-139 ankyrin repeat protein100 26.1 B4R
ALPV-150167380-168702SWPV2-140440440SWPV2-140 conserved hypothetical protein100 33.3 G5R
ALPV-151168710-168898SWPV2-1416262SWPV2-141 RNA polymerase subunit RPO798.4 55.2 G5.5R
ALPV-152168891-169457SWPV2-142188188SWPV2-142 conserved hypothetical protein100 31.8 G6R
ALPV-153170468-169422SWPV2-143348348SWPV2-143 virion core protein100 34.6 G7L
ALPV-154171554-170634SWPV2-144306306SWPV2-144 putative thioredoxin binding protein100
ALPV-155171682-171915 77 97.1 CNPV-150 ankyrin repeat protein
ALPV-156173269-172031SWPV2-145412412SWPV2-145 ankyrin repeat protein100 42.9 M1L
ALPV-157173945-173496SWPV2-146149149SWPV2-146 hypothetical protein100
ALPV-158175111-174173SWPV2-147312312SWPV2-147 Rep-like protein100
ALPV-159181355-175545SWPV2-1481936875SWPV2-148 variola B22R-like protein 98.2
ALPV-160186885-181408SWPV2-14918251831SWPV2-149 variola B22R-like protein99.7
ALPV-161187202-189685SWPV2-150827834SWPV2-150 hypothetical protein90.5
ALPV-162190813-189782SWPV2-151343343SWPV2-151 TGF-beta-like protein100
ALPV-163190815-191294 159 64.7 CNPV-157 TGF-beta-like protein
ALPV-164191763-192263SWPV2-150166834SWPV2-150 hypothetical protein47.8
ALPV-165192733-193446 237 97.2 CNPV-159 N1R/p28-like protein
ALPV-166193490-194494 334 91.3 CNPV-169 N1R/p28-like protein
ALPV-167194549-195412 287 78.7 CNPV-169 N1R/p28-like protein
ALPV-168195417-195821 134 98.5 CNPV-160 N1R/p28-like protein
ALPV-169197008-195920SWPV2-152362358SWPV2-152 TGF-beta-like protein98.9
ALPV-170197058-197507SWPV2-153149149SWPV2-153 TGF-beta-like protein100
ALPV-171197843-198883SWPV2-154346320SWPV2-154 N1R/p28-like protein95.3
ALPV-172199118-200155SWPV2-155345345SWPV2-155 Ig-like domain protein99.7
ALPV-173200427-200933SWPV2-156168168SWPV2-156 Ig-like domain protein97
ALPV-174201028-202059SWPV2-157343350SWPV2-157 N1R/p28-like protein93.6
ALPV-175202011-202415 134 92.5 CNPV-226 N1R/p28-like protein
ALPV-176202488-203126SWPV2-158212212SWPV2-158 thymidylate kinase10045.2A48R
ALPV-177203179-203961SWPV2-159260260SWPV2-159 late transcription factor VLTF-110066.2G8R
ALPV-178203975-204982SWPV2-160335335SWPV2-160 putative myristylated protein100 38.0 G9R
ALPV-179204983-205714SWPV2-161243243SWPV2-161 putative myristylated IMV envelope protein100 54.7 L1R
ALPV-180205774-206064SWPV2-1629696SWPV2-162 conserved hypothetical protein100
ALPV-181206965-206054SWPV2-163303303SWPV2-163 conserved hypothetical protein100 42.0 L3L
ALPV-182206991-207749SWPV2-164252252SWPV2-164 DNA-binding virion core protein100 36.3 L4R
ALPV-183207750-208142SWPV2-165130130SWPV2-165 conserved hypothetical protein100 41.6 L5R
ALPV-184208096-208542SWPV2-166148148SWPV2-166 putative IMV membrane protein100 42.5 J1R
ALPV-185208576-209484SWPV2-167302302SWPV2-167 poly(A) polymerase small subunit PAPS100 56.0 J3R
ALPV-186209481-210041SWPV2-168186186SWPV2-168 RNA polymerase subunit RPO22100 55.0 J4R
ALPV-187210444-210034SWPV2-169136136SWPV2-169 conserved hypothetical protein100 47.9 J5L
ALPV-188210487-214353SWPV2-17012881288SWPV2-170 RNA polymerase subunit RPO147100 70.6 J6R
ALPV-189214856-214356SWPV2-171166166SWPV2-171 putative protein-tyrosine phosphatase, virus assembly100 47.6 H1L
ALPV-190214872-215441SWPV2-172189189SWPV2-172 conserved hypothetical protein100 48.9 H2R
ALPV-191216503-215517SWPV2-173328328SWPV2-173 ankyrin repeat protein100
ALPV-192217538-216546SWPV2-174330330SWPV2-174 putative IMV envelope protein100 32.2 H3L
ALPV-193220029-217630SWPV2-175799799SWPV2-175 RNA polymerase associated protein RAP94100 55.2 H4L
ALPV-194220198-220710SWPV2-176170170SWPV2-176 late transcription factor VLTF-4100
ALPV-195220711-221661SWPV2-177316316SWPV2-177 DNA topoisomerase100 58.0 H6R
ALPV-196221666-222127SWPV2-178153153SWPV2-178 conserved hypothetical protein100 33.8 H7R
ALPV-197222401-222090SWPV2-179103103SWPV2-179 conserved hypothetical protein100
ALPV-198222409-224949SWPV2-180846846SWPV2-180 mRNA capping enzyme large subunit100 53.9 D1R
ALPV-199225020-225340SWPV2-181106106SWPV2-181 HT motif protein100
ALPV-200225759-225337SWPV2-182140140SWPV2-182 virion protein100
ALPV-201225813-226247SWPV2-183144144SWPV2-183 hypothetical protein100
ALPV-202226312-226884SWPV2-184190190SWPV2-184 conserved hypothetical protein100
ALPV-203226950-227777SWPV2-185275275SWPV2-185 N1R/p28-like protein100
ALPV-204228314-227844SWPV2-186156156SWPV2-186 C-type lectin-like protein100 30.8 A34R
ALPV-205228622-229299SWPV2-187225225SWPV2-187 deoxycytidine kinase-like protein100
ALPV-206229305-229805SWPV2-188166166SWPV2-188 Rep-like protein99.4
ALPV-207229864-230367SWPV2-189167167SWPV2-189 conserved hypothetical protein100
ALPV-208230421-231251SWPV2-190276276SWPV2-190 N1R/p28-like protein100
ALPV-209231324-232472SWPV2-191382382SWPV2-191 N1R/p28-like protein100
ALPV-210232528-232713SWPV2-1926161SWPV2-192 conserved hypothetical protein100
ALPV-211232932-233888SWPV2-193318318SWPV2-193 N1R/p28-like protein100
ALPV-212233949-235367SWPV2-194472472SWPV2-194 putative photolyase100
ALPV-213235424-235579 51 hypothetical protein, unique to ALPV, containing a transmembrane helix
ALPV-214235557-236078SWPV2-195173173SWPV2-195 N1R/p28-like protein100
ALPV-215236184-236723SWPV2-196179200SWPV2-196 conserved hypothetical protein89
ALPV-216236767-237699SWPV2-197310310SWPV2-197 N1R/p28-like protein100
ALPV-217237747-238142SWPV2-198131131SWPV2-198 N1R/p28-like protein100
ALPV-218238197-238361SWPV2-1995454SWPV2-199 conserved hypothetical protein100
ALPV-219238421-238951SWPV2-200176176SWPV2-200 N1R/p28-like protein100
ALPV-220239662-239012SWPV2-201216216SWPV2-201 deoxycytidine kinase-like protein100
ALPV-221239836-240906SWPV2-202356356SWPV2-202 vaccinia C4L/C10L-like protein100 28.1 C10L
ALPV-222241181-241795SWPV2-203204204SWPV2-203 CC chemokine-like protein100
ALPV-223241885-243090SWPV2-204401401SWPV2-204 conserved hypothetical protein100
ALPV-224243204-244196SWPV2-205330330SWPV2-205 N1R/p28-like protein100
ALPV-225244284-245555SWPV2-206423223SWPV2-206 N1R/p28-like protein99.5
ALPV-226245795-245619 58 hypothetical protein, unique to ALPV, containing a transmembrane helix
ALPV-227246013-245858 51 hypothetical protein, unique to ALPV, containing a transmembrane helix
ALPV-228246363-247412SWPV2-207349349SWPV2-207 N1R/p28-like protein100
ALPV-229247466-248308 280 80.9 SWPV1-198 N1R/p28-like protein
ALPV-230248847-248644SWPV2-2086785SWPV2-208 N1R/p28-like protein62.7
ALPV-231249295-249483SWPV2-20962213SWPV2-209 N1R/p28-like protein100
ALPV-232250029-250292SWPV2-21087285SWPV2-210 N1R/p28-like protein100
ALPV-233250283-250615 110 98.2 CNPV-227 N1R/p28-like protein
ALPV-234253677-251134SWPV2-211847847SWPV2-211 ankyrin repeat protein99.931.6B4R
ALPV-235253931-254650SWPV2-212239239SWPV2-212 hypothetical protein100
ALPV-236254650-255027 125 73.3 CNPV-227 N1R/p28-like protein
ALPV-237255062-255346SWPV2-21494126SWPV2-214 N1R/p28-like protein96.4
ALPV-238257103-255799SWPV2-215434434SWPV2-215 ankyrin repeat protein10027.3B4R
ALPV-239257301-257498SWPV2-2166565SWPV2-216 hypothetical protein100
ALPV-240257446-257922SWPV2-217158158SWPV2-217 MyD116-like domain protein100
ALPV-241257952-258566SWPV2-218204204SWPV2-218 CC chemokine-like protein98
ALPV-242258748-260163SWPV2-219471471SWPV2-219 ankyrin repeat protein100 31.4 M1L
ALPV-243260183-261709SWPV2-220508508SWPV2-220 ankyrin repeat protein100 37.0 M1L
ALPV-244261780-263084SWPV2-221434432SWPV2-221 conserved hypothetical protein99.5
ALPV-245263129-264100SWPV2-222323323SWPV2-222 ribonucleotide reductase small subunit100 70.9 F4L
ALPV-246264281-265606SWPV2-223441441SWPV2-223 ankyrin repeat protein99.8 33.3 B4R
ALPV-247266342-265665SWPV2-224225225SWPV2-224 late transcription factor VLTF-3100 76.7 A2L
ALPV-248266557-266330SWPV2-2257575SWPV2-225 virion redox protein100
ALPV-249268550-266571SWPV2-226659659SWPV2-226 virion core protein P4b100 54.1 A3L
ALPV-250269284-268637SWPV2-227215215SWPV2-227 immunodominant virion protein100
ALPV-251269323-269832SWPV2-228169169SWPV2-228 RNA polymerase subunit RPO19100 55.2 A5R
ALPV-252270948-269827SWPV2-229373373SWPV2-229 conserved hypothetical protein100 39.3 A6L
ALPV-253273084-270955SWPV2-230709709SWPV2-230 early transcription factor large subunit VETFL100 59.6 A7L
ALPV-254273148-274050SWPV2-231300300SWPV2-231 intermediate transcription factor VITF-3100 38.7 A8R
ALPV-255274242-274015SWPV2-2327575SWPV2-232 putative IMV membrane protein100
ALPV-256276924-274243SWPV2-233893893SWPV2-233 virion core protein P4a100 39.6 A10L
ALPV-257276942-277781SWPV2-234279279SWPV2-234 conserved hypothetical protein100 39.5 A11R
ALPV-258278284-277778SWPV2-235168168SWPV2-235 virion protein99.4 32.9 A12L
ALPV-259278299-278556SWPV2-2368556SWPV2-236 conserved hypothetical protein87.0
ALPV-260278754-278545SWPV2-2376969SWPV2-237 putative IMV membrane protein100
ALPV-261279080-278802SWPV2-2389292SWPV2-238 putative IMV membrane protein100 27.5 A14L
ALPV-262279258-279097SWPV2-2395353SWPV2-239 putative IMV membrane virulence factor100 35.3 A 14.5L
ALPV-263279564-279274SWPV2-2409696SWPV2-240 conserved hypothetical protein100
ALPV-264280654-279548SWPV2-241368368SWPV2-241 predicted myristylated protein100 43.0 A16L
ALPV-265281248-280670SWPV2-242192192SWPV2-242 putative phosphorylated IMV membrane protein100 33.2 A17L
ALPV-266281266-282654SWPV2-243462462SWPV2-243 DNA helicase, transcriptional elongation100 50.2 A18R
ALPV-267282891-282622SWPV2-2448989SWPV2-244 conserved hypothetical protein100 42.9 A19L
ALPV-268283237-282899SWPV2-245112112SWPV2-245 conserved hypothetical protein100 45.3 A21L
ALPV-269283236-284540SWPV2-246434434SWPV2-246 DNA polymerase processivity factor100 25.9 A20R
ALPV-270284537-284995SWPV2-247152152SWPV2-247 Holliday junction resolvase protein100 45.0 A22R
ALPV-271285012-286163SWPV2-248383383SWPV2-248 intermediate transcription factor VITF-3100 51.3 A23R
ALPV-272286189-289662SWPV2-24911571157SWPV2-249 RNA polymerase subunit RPO132100 74.6 A24R
ALPV-273291456-289651SWPV2-250601601SWPV2-250 A type inclusion-like protein100
ALPV-274292918-291491SWPV2-251475475SWPV2-251 A type inclusion-like/fusion protein100 56.4 A27L
ALPV-275293341-292919SWPV2-252140140SWPV2-252 conserved hypothetical protein100 41.8 A28L
ALPV-276294263-293346SWPV2-253305305SWPV2-253 RNA polymerase subunit RPO35100 42.6 A29L
ALPV-277294465-294238SWPV2-2547575SWPV2-254 conserved hypothetical protein100
ALPV-278294590-294931SWPV2-255113113SWPV2-255 conserved hypothetical protein100 31.6 A31R
ALPV-279294940-295302SWPV2-256120120SWPV2-256 conserved hypothetical protein100
ALPV-280296145-295291SWPV2-257284284SWPV2-257 DNA packaging protein100 47.1 A32L
ALPV-281296260-296805SWPV2-258181181SWPV2-258 C-type lectin-like EEV protein100
ALPV-282297030-297854SWPV2-259274274SWPV2-259 conserved hypothetical protein100
ALPV-283297914-298723SWPV2-260269269SWPV2-260 putative tyrosine protein kinase100
ALPV-284298766-299782SWPV2-261338338SWPV2-261 putative serpin100
ALPV-285300562-299804SWPV2-262252252SWPV2-262 conserved hypothetical protein100
ALPV-286300672-301604SWPV2-263310310SWPV2-263 G protein-coupled receptor-like protein100
ALPV-287301615-301905SWPV2-2649696SWPV2-264 conserved hypothetical protein100
ALPV-288301971-302501SWPV2-265176169SWPV2-265 beta-NGF-like protein96
ALPV-289302911-302519SWPV2-266130130SWPV2-266 HT motif protein100
ALPV-290303015-303659SWPV2-267214214SWPV2-267 conserved hypothetical protein100
ALPV-291304032-303670SWPV2-268120120SWPV2-268 HT motif protein100
ALPV-292304198-304533SWPV2-269111111SWPV2-269 CC chemokine-like protein100
ALPV-293304612-305193SWPV2-270193193SWPV2-270 putative interleukin binding protein100
ALPV-294305303-305683SWPV2-271126126SWPV2-271 EGF-like protein100 34.8 C11R
ALPV-295305685-306602SWPV2-272305305SWPV2-272 putative serine/threonine protein kinase100 41.1 B1R
ALPV-296306645-307127SWPV2-273160160SWPV2-273 conserved hypothetical protein100
ALPV-297307210-307677SWPV2-274155147SWPV2-274 C-type lectin-like protein99.3 22.6 A34R
ALPV-298307720-308139SWPV2-275139139SWPV2-275 putative interleukin binding protein100
ALPV-299308208-308435SWPV2-2767575SWPV2-276 conserved hypothetical protein100
ALPV-300308637-310421SWPV2-277594594SWPV2-277 ankyrin repeat protein99.8 22.3 B4R
ALPV-301310445-310669SWPV2-2787474SWPV2-278 hypothetical protein100
ALPV-302310712-311566SWPV2-279284284SWPV2-279 ankyrin repeat protein99.6 33.9 B24R
ALPV-303311621-312913SWPV2-280430430SWPV2-280 ankyrin repeat protein99.8 C18L
ALPV-304313106-314296SWPV2-281396396SWPV2-281 ankyrin repeat protein100 28.6 M1L
ALPV-305314299-315675SWPV2-282458458SWPV2-282 ankyrin repeat protein100 32.5 B4R
ALPV-306315784-317997SWPV2-283737737SWPV2-283 ankyrin repeat protein100 25.8 M1L
ALPV-307318053-319768SWPV2-284571571SWPV2-284 ankyrin repeat protein100 28.8 B4R
ALPV-308319772-320674SWPV2-285300300SWPV2-285 putative serine/threonine protein kinase100 24.6 M1L
ALPV-309320747-321481SWPV2-286244244SWPV2-286 ankyrin repeat protein100 32.8 B1R
ALPV-310322082-323665SWPV2-287527527SWPV2-287 ankyrin repeat protein100 23.7 M1L
ALPV-311324261-323680SWPV2-288193193SWPV2-288 conserved hypothetical protein100 26.1 B18R
ALPV-312324329-325831SWPV2-289500500SWPV2-289 ankyrin repeat protein100
ALPV-313326047-327447SWPV2-290466466SWPV2-290 ankyrin repeat protein100 28.3 M1L
ALPV-314327518-328306SWPV2-291262262SWPV2-291 N1R/p28-like protein100 28.2 B4R
ALPV-315328368-328586SWPV2-2927272SWPV2-292 hypothetical protein100
ALPV-316329054-328590SWPV2-293154154SWPV2-293 C-type lectin-like protein100
ALPV-317329231-330304SWPV2-294357357SWPV2-294 ankyrin repeat protein100 34.4 A40R
ALPV-318330452-331042SWPV2-295196196SWPV2-295 ankyrin repeat protein100
ALPV-319331147-332760SWPV2-296537537SWPV2-296 ankyrin repeat protein100 37.4 M1L
ALPV-320332794-333168SWPV2-297124124SWPV2-297 EFc-like protein100
ALPV-321333178-333678SWPV2-298166166SWPV2-298 conserved hypothetical protein100
ALPV-322333750-334406SWPV2-299218218SWPV2-299 Ig-like domain protein100
ALPV-323334433-336322SWPV2-300629629SWPV2-300 ankyrin repeat protein99.8
ALPV-324336421-337368SWPV2-301315315SWPV2-301 G protein-coupled receptor-like protein100 40.8 B4R
ALPV-325337435-339069SWPV2-302544544SWPV2-302 ankyrin repeat protein99.8
ALPV-326339250-339417SWPV2-3035555SWPV2-303 hypothetical protein10033.9B4R
ALPV-327339592-341124SWPV2-304510514SWPV2-304 ankyrin repeat protein99.2
ALPV-328341457-343424SWPV2-305655637SWPV2-305 ankyrin repeat protein96.636.8M1L
ALPV-329343616-345025SWPV2-306469469SWPV2-306 Ig-like domain protein100 25.8 M1L
ALPV-330345157-345531SWPV2-307124124SWPV2-307 EFc-like protein100
ALPV-331345865-347868SWPV2-308667689SWPV2-308 ankyrin repeat protein96.5
ALPV-332348446-347985SWPV2-309153186SWPV2-309 conserved hypothetical protein86.9 identical to ALPV-005
ALPV-333349231-348563SWPV2-310222222SWPV2-310 conserved hypothetical protein100 identical to ALPV-004
ALPV-334349357-349584 75 56.1 SWPV1-002 C-type lectin-like protein, identical to ALPV-003
ALPV-335349639-350265SWPV2-311208208SWPV2-311 C-type lectin-like protein100 identical to ALPV-002
ALPV-336351083-350568SWPV2-312171171SWPV2-312 hypothetical protein100 identical to ALPV-001
Note: ALPV, albatrosspox virus (GenBank accession no. MW365933); SWPV1, shearwaterpox virus 1 (GenBank accession no. KX857216); SWPV2, shearwaterpox virus 2 (GenBank accession no. KX857215); CNPV, canarypox virus (GenBank accession no. AY318871). Avipoxviruses as being identity to SWPV2 unless indicated in the note column. Truncated or fragmented ORFs of ALPV compared to SWPV2 are highlighted in italic font.
Table
Table 3. Related poxvirus genome sequences used in further analysis of ALPV.
Table 3. Related poxvirus genome sequences used in further analysis of ALPV.
VirusAbbreviationGenBank Accession NumberReference
Albatrosspox virusALPVMW365933This study
Canarypox virusCNPVAY318871[32]
Cheloniidpox virus 1ChePV-1MT799800[61]
Fowlpox virusFWPVAF198100, MF766430-32,
MH709124-25,
MH719203, MH734528,
AJ581527, MW142017		[28,29,62,63]
Flamingopox virusFGPVMF678796[24]
Magpiepox virusMPPVMK903864[31]
Mudlarkpox virusMLPVMT978051[30]
Nile crocodilepox virusCRVDQ356948[64]
Penguinpox virusPEPVKJ859677[33]
Penguinpox virus 2PEPV2MW296038[19]
Pigeonpox virusFeP2KJ801920[33]
Saltwater crocodilepox virus 1SwCRV1MG450915[36,65]
Shearwaterpox virus 1SWPV1KX857216[25]
Shearwaterpox virus 2SWPV2KX857215[25]
Turkeypox virusTKPVNC_028238[34]
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MDPI and ACS Style

Sarker, S.; Athukorala, A.; Nyandowe, T.; Bowden, T.R.; Boyle, D.B. Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Northern Royal Albatross (Diomedea sanfordi). Pathogens 2021, 10, 575. https://doi.org/10.3390/pathogens10050575

AMA Style

Sarker S, Athukorala A, Nyandowe T, Bowden TR, Boyle DB. Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Northern Royal Albatross (Diomedea sanfordi). Pathogens. 2021; 10(5):575. https://doi.org/10.3390/pathogens10050575

Chicago/Turabian Style

Sarker, Subir, Ajani Athukorala, Tadiwa Nyandowe, Timothy R. Bowden, and David B. Boyle. 2021. "Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Northern Royal Albatross (Diomedea sanfordi)" Pathogens 10, no. 5: 575. https://doi.org/10.3390/pathogens10050575

APA Style

Sarker, S., Athukorala, A., Nyandowe, T., Bowden, T. R., & Boyle, D. B. (2021). Genomic Characterisation of a Novel Avipoxvirus Isolated from an Endangered Northern Royal Albatross (Diomedea sanfordi). Pathogens, 10(5), 575. https://doi.org/10.3390/pathogens10050575

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