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Newly characterized arboviruses of northern Australia
Virology Reports 6 (2016) 11–17
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Virology Reports journal homepage: www.elsevier.com/locate/virep
Newly characterized arboviruses of northern Australia Bixing Huang a, Richard Allcock b,c, David Warrilow a,⁎ a b c
Public Health Virology Laboratory, Queensland Health Forensic and Scientific Services, PO Box 594, Archerfield, Queensland 4108, Australia School of Pathology and Laboratory Medicine, University of Western Australia, Nedlands, WA 6009, Australia Translational Cancer Pathology Laboratory, Pathwest Laboratory Medicine WA, QEII Medical Centre, Nedlands, WA 6009, Australia
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Article history: Received 25 October 2015 Received in revised form 22 January 2016 Accepted 26 January 2016 Available online 3 February 2016 Keywords: Rhabdovirus Bunyavirus Arbovirus Sequencing Phylogenetics
a b s t r a c t Arboviruses circulate in the biota of northern Australia, sometimes causing disease in animals and humans. Five different arboviruses, isolated and stored for over 30 years, were re-cultured and sequenced using high-throughput sequencing technology (Ion Torrent PGM) for identification and genetic characterization. Phylogenetic analysis, primarily of sequence fragments of the large segment, indicated classification as members of the Family Bunyaviridae (Belmont, Little Sussex, Parker's Farm, and Thimiri viruses). Another was identified as a member of the Family Rhabdoviridae (Beatrice Hill virus) based on phylogenetic analysis of the RNA polymerase region. Crown Copyright © 2016 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction Arboviruses, or arthopod-borne viruses cause large disease outbreaks in animal and human populations which place a strain on veterinary and medical services and have a huge disease burden globally (Weaver and Reisen, 2010). Hence, surveillance is widely conducted to determine seasonal risk and to facilitate targeted control strategies (Geoghegan et al., 2014). Arboviruses mainly belong to 6 families: Togaviridae, Flaviviridae, Bunyaviridae, Rhabdoviridae, Reoviridae and Orthomyxoviridae (Weaver, 2006). Mosquitoes, ticks, biting midges and sandflies are the main vectors depending on the virus and host. Within Australia, there have been 75 isolations of different arboviruses (Russell and Dwyer, 2000), a proportion of which are associated with animal and human disease. Globally, insect-borne infections with rhabdoviruses cause diseases of veterinary importance, but occasionally result in pathology in humans. For example vesicular stomatitis virus (VSV), a mosquito and sandfly-transmitted arbovirus (Genus Vesiculovirus), is found in the Americas and can cause fever and vesicular lesions in cattle, horses and pigs, and acute fever in humans (Rodriguez, 2002). Bovine ephemeral fever virus (BEFV) is a mosquito and biting midge-transmitted arbovirus (Genus Ephemerovirus) responsible for fever and mucosal discharge in cattle and water buffalo, which causes significant economic impact in affected regions due to reduced milk production (Walker, 2005). In Australia, the virus is enzootic, and outbreaks in cattle occur in summer and autumn (Walker, 2005). There are many other rhabdoviruses that circulate widely in the biota worldwide and have been detected in a wide diversity of hosts including insects, bats, fish, macropods, lizards, birds, ungulates and rodents, but have not been shown to be associated with disease (Walker et al., 2015). Numerous bunyaviruses cause disease in animals and humans worldwide. For example, the bunyaviruses California encephalitis virus and La Crosse virus are both mosquito-transmitted arboviruses (Genus Orthobunyavirus) known to cause encephalitis in ⁎ Corresponding author. E-mail address: [email protected] (D. Warrilow). http://dx.doi.org/10.1016/j.virep.2016.01.001 2214-6695/Crown Copyright © 2016 Published (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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humans in the United States (Rust et al., 1999; Zeller and Bouloy, 2000). Crimean–Congo haemorrhagic fever virus is a ticktransmitted arbovirus (Genus Nairovirus) causing a potentially fatal arboviral hemorrhagic disease also in humans (Zeller and Bouloy, 2000). A number of other viruses such as Rift Valley fever (Genus Phlebovirus), the Bunyamwera group (Genus Orthobunyavirus), Nairobi sheep disease and Dera Ghazi Khan virus group (both Genus Nairovirus) cause disease in both humans and livestock (Schmaljohn and Nichol, 2007). Finally, the tick-borne Uukuniemi (Genus Phlebovirus), Hughes and Qalyub (both Genus Nairovirus) virus groups cause disease in seabirds (Schmaljohn and Nichol, 2007). However, in Australia only Akabane virus (Genus Orthobunyavirus, Simbu group) causes disease of any significance, with infection resulting in abortion and deformities in gestating cattle (Geoghegan et al., 2014). Since the 1950s, arthropod collection and subsequent virus isolation have been conducted across northern Australia to survey for known and novel arboviruses. This has resulted in the collection of numerous virus isolates which have been archived in reference collections. When surveillance for these viruses was initially conducted, and up until the 1980s, characterization was generally limited to experimental pathology in animals and serology-based classification. More recently, virus taxonomy has been simultaneously assisted and challenged by the advent of nucleic acid sequencing. The development of high-throughput sequencing (HTS), also known as next-generation sequencing, has accelerated this process. This sequencing technology is the method of choice to characterize many archived isolates as multiple virus samples can be sequenced in a single experiment using this technology. In this study, we utilized HTS to obtain genome sequences from 5 virus samples stored in archival collections, for which no information or only serological information was available. To facilitate this, a high density chip was used with multiple samples on the Personal Genome Machine (PGM, Life Technologies) platform. The sequences obtained confirmed previous serological classification for two bunyaviruses. Additional isolates were identified as two bunyaviruses and a rhabdovirus. This work confirms the power of HTS to rapidly identify viruses without prior knowledge of their identities or genome sequences. 2. Methods 2.1. Virus collection, isolation and culture Viruses were isolated from collections of mosquito and biting midges as previously described (Doherty et al., 1979, 1972; Standfast et al., 1984). Virus samples were thawed and re-cultured in Vero cells for one passage, and then subsequently in C6/36 cells for another passage. Tissue culture supernatant was harvested and then stored at −80 °C prior to use. 2.2. Viral genome sequencing The sequencing of viral RNA genomes was conducted as described previously (Warrilow et al., 2014). In brief, virus was purified from tissue culture supernatant using preferential nuclease digestion and ultra-centrifugation (RNase ONE and RQ1 DNase, Promega), followed by sequence-independent amplification. A library was constructed from the products which were then sequenced on a Personal Genome Machine (Ion Torrent PGM™, Life Technologies) using a 318 chip. 2.3. Virus sequence assembly and phylogenetic analysis The virus genome sequence was assembled de novo using Geneious R8 (Kearse et al., 2012). The generated contiguous sequences (contigs) were then mapped using related rhabdovirus or bunyavirus segments from GenBank (large, L; medium, M; and small, S) as scaffolds. The combined contigs were then used as a reference sequence with the complete sequence data to generate the final contigs to each of the segments. The open reading frames (ORFs) of each segment were used for phylogenetic analysis. Best match by Basic Local Alignment Sequence Tool for protein (BLASTP) was performed using the National Center for Biotechnology Information online tool (http://www.ncbi.nlm.nih.gov). Multiple sequence alignments were generated using the MAFFT plugin of Geneious R8 (Kearse et al., 2012). The alignment was then used as input for determining phylogenetic relationships by the maximum likelihood model using MEGA5 software (Tamura et al., 2011) with an appropriate outgroup. Robustness of the generated trees was determined using 1000 bootstrap replicates. 3. Results 3.1. Sequencing of multiple viruses on a high density semiconductor chip Eleven uncharacterized isolates were barcoded and sequenced on the Personal Genome Machine using a high density semiconductor chip. Two (Taggert and Yacaaba viruses) will be described elsewhere (Huang and Warrilow, unpublished data). Genome sequences were obtained from another three (Maprik, Mapputta and Upolu viruses), but studies describing these were published by other groups in the interim (Briese et al., 2014; Gauci et al., 2015); therefore, they were not analysed further. One virus (Tzipori virus) was determined to be a strain of bovine ephemeral fever virus (data not shown), and was not analysed further. The sequence of fragments of the remaining 5 virus genomes (Fig. 1 and Table 1) was analysed here.
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Fig. 1. Coverage density plots of virus genome sequence contigs. (A) Beatrice Hill virus; (B) Belmont virus L segment contigs 1 and 2 (upper and middle), respectively, and M segment (lower); (C) Little Sussex virus; (D) Parker's Farm virus; and (E) Thimiri virus. The maximum depth of reads is indicated on the left of the density plots, which are not presented to scale.
3.2. Beatrice Hill virus: a newly identified tibrovirus After assembly of reads from HTS of Beatrice Hill virus, a 2965 nt fragment was obtained including a large uninterrupted ORF which gave the best match by BLASTP to the L segment of a rhabdovirus (Tibrogargan virus, YP_007641376.1, 84% amino acid identity) in the “supergroup” dimarhabdovirus. On this basis, a multiple sequence alignment was conducted with members of this group to determine an appropriate classification. The phylogenetic tree generated gave good support for its classification as a new viral member assigned to the Genus Tibrovirus (Fig. 2). As there was no previous serological data, this is the first proposed taxonomic classification of this virus.
Table 1 Arboviruses characterized in this study. Name (strain)
Region(s) isolated
Insect species
Segment(s) sequenced Serological classification Neurovirulent1 Reference (average read density) (serogroup)
Beatrice Hill virus (CSIRO25) Belmont virus (CSIRO148)
Beatrice Hill, Northern Territory Rockhampton, Queensland; Beatrice Hill, Northern Territory
Genome (5734)
ND
ND
L (27,788 & 4090), M (18,733)
“Bunyavirus-like”
Yes
Little Sussex virus (Ch19546)
Charleville, Queensland
L (10,665)
ND
ND
(Doherty et al., 1979)
Parker's Farm virus (Ch19520)
Charleville, Queensland; Beatrice Hill, Northern Territory
L (1370)
ND
ND
(Doherty et al., 1972; Standfast et al., 1984)
Thimiri virus (CSIRO1)
Beatrice Hill, Northern Territory
Culicoides peregrinus Culex annulirostris, Culicoides marksi Culex annulirostris, Aedes normanensis Culex annulirostris, Culicoides marksi Culicoides histrio
L (483)
Bunyaviridae (Simbu)
Yes
(Standfast et al., 1984)
1. Indicated by death in weanling mice (Arbovirus Catalogue, CDC); ND, not determined.
(Standfast et al., 1984) (Doherty et al., 1972; Standfast et al., 1984)
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Fig. 2. The relationship of Beatrice Hill virus within the supergroup dimarhabdovirus. A maximum likelihood phylogenetic tree based on predicted amino acid sequences using the Jones–Taylor–Thornton (JTT) substitution model is shown. There are members of three genera, and Beatrice Hill virus (bold) is placed in the Genus Tibrovirus. Australian bat lyssavirus (ABL) was used to root the tree. Topological support values from 1000 bootstrap replicates are given as a percentage (those over 50 shown). GenBank accession numbers: Beatrice Hill virus, KT20480; vesicular stomatitis Indiana virus, J02428.1; bovine ephemeral fever virus, NC_002526.1; spring viremia of carp virus, U18101.2; Australian bat lyssavirus, AF418014.1; Tupaia virus, NC_007020.1; Cocal virus Indiana 2, EU373657.1; Obodhiang virus, NC_017685.1; Adelaide River virus isolate DPP61, JN935380.1; Bas-Congo virus isolate BASV-1, JX297815.1; Tibrogargan virus strain CS132, NC_020804.1; Chandipura virus strain CH157, KF468773.1; Kimberley virus isolate CS368, NC_025396.1; Coastal Plains virus strain DPP53, NC_025397.1.
3.3. Belmont virus When assembled, the reads from the Belmont virus isolate generated three sequence fragments. An initial BLASTP search of predicted ORFs resulted in best matches for two (1015 and 911 nt fragments) with the L segment of members of the Genus Orthobunyavirus (Facey's Paddock virus, AHY22330.1, 61% amino acid identity and Leanyer virus, AEA02985.1, 69% amino acid identity; respectively). The predicted ORF of the third fragment (1138 nt) had the best match with the M segment of a virus in the same genus (Utinga virus, AHY22345.1, 56% amino acid identity). To maximize sequence information for analysis, the three fragments were concatenated and used as input for multiple sequence alignments with other orthobunyaviruses. A phylogenetic tree generated from the alignment output indicated its closest relative (Leanyer virus) to be a member of the Simbu group of orthobunyaviruses (Fig. 3A). The bootstrap value (60%) indicated some support for inclusion of this virus within a clade which includes the Simbu group, but did not further resolve its classification. This is consistent with previous serology which indicated that it was “bunyavirus-like” (Standfast et al., 1984).
Fig. 3. The relationship of four uncharacterized arboviruses within the Genus Orthobunyavirus. A maximum likelihood phylogenetic tree based on predicted amino acid sequences using the Jones–Taylor–Thornton (JTT) substitution model, showing members of 5 groups within the orthobunyaviruses. (A) Belmont, (B) Little Sussex, (C) Parker's Farm and (D) Thimiri viruses are indicated in bold. Rift Valley fever virus was used to root the tree. Topological support values from 1000 bootstrap replicates are given as a percentage (those over 50 shown). GenBank accession numbers: Belmont virus L and M segments, KT720481 and KT720482 respectively; Little Sussex virus L segment, KT20483; Parker's Farm, KT20484; and Thimiri virus, KT20485. For other viruses, the L and M segments, respectively, are: Bunyamwera virus, NC_001925.1 and NC_001926.1; La Crosse, NC_004108.1 and NC_004109.1; Oropouche virus, NC_005775.1 and NC_005776.1; Akabane virus, NC_009894.1 and NC_009895.1; Chatanga virus strain LEIV-17756, EU616903.1 and EU621834.1; Rift Valley fever virus, NC_014397.1 and JF784387.1; Tahyna virus isolate 22595-6, HM036219.1 and HM036218.1; Leanyer virus isolate AusN16701, HM627178.1 and HM627176.1; Iaco virus strain BeAn314206, JN572065.1 and JN572066.1; Macaua virus strain BeAr306329, JN572068.1 and JN572069.1; Sororoca virus strain BeAr32149, JN572071.1 and JN572072.1; Wyeomyia virus, JN572080.1 and JN801034.2; Simbu virus, HE795108.1 and NC_018478.1; Sathuperi virus, NC_018461.1 and NC_018466.1; Aino virus, NC_018465.1 and NC_018459.1; Batai virus, JX846606.1 and JX846605.1; Cache Valley virus strain MNZ-92011, KC436106.1 and KC436107.1; Oya virus strain SC0806 segment L only, JX983194.1; Ilesha virus strain R5964, KF234075.1 and KF234074.1; Madrid virus strain BT4075, KF254779.1 and KF254780.1; Caraparu virus strain FMD0783, KF254793.1 and KF254788.1; Kowanyama virus, KT820202 and KT820203; Yacaaba virus, KT820208 and KT820209; Murrumbidgee virus isolate 934, KF234253.1 and NC_022596.1; Salt ash virus isolate 931, KF234256.1 and KF234257.1; Mermet virus isolate AV 782L segment only, KF697153.1; Cat Que Virus strain VN04-2108L segment only, NC_024076.1; Manzanilla virus strain DHL10M107 L segment only, KP016012.1.
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3.4. Little Sussex virus: a newly identified orthobunyavirus A 5800 nt fragment was assembled from the Little Sussex virus data. BLASTP analysis of its predicted ORF indicated that it gave the best match with a member of the Genus Orthobunyavirus (Gamboa virus, AIS74636.1, 62% amino acid identity). A single large ORF was aligned with other members of the genus and used to build a phylogenetic tree as described (Fig. 3B). The analysis indicated that it
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formed a clade with members of the California encephalitis virus group and two recently sequenced orthobunyaviruses (Kowanyama and Yacaaba viruses), branching basally within the clade. As there were no previous serological data, this is the first indication of taxonomic classification for this virus. 3.5. Parker's Farm virus: a newly identified orthobunyavirus A 960 nt sequence fragment was obtained from the assembled data. Its predicted ORF gave the best match by BLASTP to the L segment of a member of the Genus Orthobunyavirus (Facey's Paddock, AHY22330.1, 62% amino acid identity). Alignment and phylogenetic analysis indicated that it could be placed in a clade with the Simbu group of the orthobunyaviruses (Fig. 3C). As there were no previous serological data, this is also the first indication of taxonomic classification for this virus. 3.6. Thimiri virus A 958 nt sequence fragment was obtained from the isolate of Thimiri virus. Its predicted ORF gave the best match by BLASTP to the L segment of a member of the Genus Orthobunyavirus (Mermet virus, AHY22335.1, 90% amino acid identity) and a phylogenetic tree revealed the virus formed a clade with Mermet, Oya, Manzanilla and Cat Que orthobunyaviruses (Fig. 3D). These viruses are also in the Simbu group, suggesting Thimiri virus may also be a member. This result supports previous serological classification of the virus in the Simbu group (Standfast et al., 1984). 4. Discussion In this work, we have genetically characterized a number of isolates of arboviruses and demonstrated the power of HTS technologies to rapidly identify and determine the genetic relationships of viruses in samples stored for more than 30 years. This application of HTS is of particular importance in the case of responding to an emerging virus, and to identify viruses that have the potential for emergence. Virus virulence and emergence are complex issues involving the genetics of the host and the pathogen, the interplay between them, vector behaviour and environmental factors. At the level of the genetics of the virus, emergence potential is suggested by the relatedness of a particular virus to others of known virulence. In the case of the viruses characterized in this study, there are associations which suggest emergence potential in each case. Firstly, Beatrice Hill virus, which is comfortably placed in a clade with other tibroviruses, is therefore related to Bas-Congo virus, a hemorrhagic fever virus from Central Africa (Grard et al., 2012). In addition, Little Sussex virus is in a clade which includes the California encephalitis group. Finally, Belmont, Parker's Farm and Thimiri viruses are most likely related to the Simbu group which includes the cattle pathogen Akabane virus. Understanding emergence potential is not limited to the genetic relatedness of a novel virus to another of known pathology. To illustrate, the naturally attenuated West Nile virus strain in Australia (Kunjin virus or WNVKUN) has 98% amino acid identity to the pathogenic New York strain (Audsley et al., 2011). Hence, a further consideration is that the risk of emergence may be enhanced by a small number of nucleotide changes within a virulence determinant. For example, a single amino acid change in a low virulence strain of WNV (T249P in the NS3 helicase) resulted in increased virulence in American crows (Brault et al., 2007). Hence, a new virulent strain may conceivably emerge from a less virulent strain. This was exemplified, again by WNVKUN, when it emerged as a more pathogenic strain in Australian horses in 2011 (Frost et al., 2012). With regard to the viruses in this study, previous studies in animal models indicated that Belmont and Thimiri viruses are potentially neurovirulent (Table 1) so there is the potential to cause clinical disease for these viruses. The virulence of the other viruses is yet to be established. Beatrice Hill and Thimiri viruses were isolated from single species of biting midge (Table 1). Interestingly, three of the other viruses described were isolated from two different species of vector, either from a mosquito and a biting midge (Little Sussex and Parker's Farm viruses) or two species of biting midge (Belmont virus). All vectors with the exception of the vector for Thimiri virus (Culicoides histrio) have been observed to feed on mammals including humans (Jansen et al., 2009; Muller et al., 1981; Van Den Hurk et al., 2003). However, there have been no recorded cases of disease associated with any of these viruses. But in consideration of their phylogenetics, neurovirulence in animals, and vector feeding behaviour, a risk of causing disease in future is theoretically possible. In particular, Belmont virus meets all the discussed criteria for emergence potential, and could be considered in cases of unexplained febrile disease in northern Australia. In conclusion, this study identified one isolate, Beatrice Hill virus, as a tibrovirus. Also, the study expanded the number of known orthobunyaviruses, characterizing three probable members of the Simbu group (Belmont, Parker's Farm and Thimiri viruses), and an additional orthobunyavirus outside this group (Little Sussex virus). The sequence data obtained will enable the design of reagents for PCR-based assays for future disease surveillance. Our findings have elucidated our understanding of the relationships among the arboviruses of northern Australia. They also reveal the rich diversity of viruses in the Australian landscape, and suggest that there are many yet to be discovered. Acknowledgements We would like to acknowledge those who originally obtained the virus isolates including R.L. Doherty, H.A. Standfast, T.D. St George and their colleagues; without whose labours, this work would not have been possible. We thank Andrew Van Den
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Newly characterized arboviruses of northern Australia Bixing Huang a, Richard Allcock b,c, David Warrilow a,⁎ a b c
Public Health Virology Laboratory, Queensland Health Forensic and Scientific Services, PO Box 594, Archerfield, Queensland 4108, Australia School of Pathology and Laboratory Medicine, University of Western Australia, Nedlands, WA 6009, Australia Translational Cancer Pathology Laboratory, Pathwest Laboratory Medicine WA, QEII Medical Centre, Nedlands, WA 6009, Australia
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Article history: Received 25 October 2015 Received in revised form 22 January 2016 Accepted 26 January 2016 Available online 3 February 2016 Keywords: Rhabdovirus Bunyavirus Arbovirus Sequencing Phylogenetics
a b s t r a c t Arboviruses circulate in the biota of northern Australia, sometimes causing disease in animals and humans. Five different arboviruses, isolated and stored for over 30 years, were re-cultured and sequenced using high-throughput sequencing technology (Ion Torrent PGM) for identification and genetic characterization. Phylogenetic analysis, primarily of sequence fragments of the large segment, indicated classification as members of the Family Bunyaviridae (Belmont, Little Sussex, Parker's Farm, and Thimiri viruses). Another was identified as a member of the Family Rhabdoviridae (Beatrice Hill virus) based on phylogenetic analysis of the RNA polymerase region. Crown Copyright © 2016 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction Arboviruses, or arthopod-borne viruses cause large disease outbreaks in animal and human populations which place a strain on veterinary and medical services and have a huge disease burden globally (Weaver and Reisen, 2010). Hence, surveillance is widely conducted to determine seasonal risk and to facilitate targeted control strategies (Geoghegan et al., 2014). Arboviruses mainly belong to 6 families: Togaviridae, Flaviviridae, Bunyaviridae, Rhabdoviridae, Reoviridae and Orthomyxoviridae (Weaver, 2006). Mosquitoes, ticks, biting midges and sandflies are the main vectors depending on the virus and host. Within Australia, there have been 75 isolations of different arboviruses (Russell and Dwyer, 2000), a proportion of which are associated with animal and human disease. Globally, insect-borne infections with rhabdoviruses cause diseases of veterinary importance, but occasionally result in pathology in humans. For example vesicular stomatitis virus (VSV), a mosquito and sandfly-transmitted arbovirus (Genus Vesiculovirus), is found in the Americas and can cause fever and vesicular lesions in cattle, horses and pigs, and acute fever in humans (Rodriguez, 2002). Bovine ephemeral fever virus (BEFV) is a mosquito and biting midge-transmitted arbovirus (Genus Ephemerovirus) responsible for fever and mucosal discharge in cattle and water buffalo, which causes significant economic impact in affected regions due to reduced milk production (Walker, 2005). In Australia, the virus is enzootic, and outbreaks in cattle occur in summer and autumn (Walker, 2005). There are many other rhabdoviruses that circulate widely in the biota worldwide and have been detected in a wide diversity of hosts including insects, bats, fish, macropods, lizards, birds, ungulates and rodents, but have not been shown to be associated with disease (Walker et al., 2015). Numerous bunyaviruses cause disease in animals and humans worldwide. For example, the bunyaviruses California encephalitis virus and La Crosse virus are both mosquito-transmitted arboviruses (Genus Orthobunyavirus) known to cause encephalitis in ⁎ Corresponding author. E-mail address: [email protected] (D. Warrilow). http://dx.doi.org/10.1016/j.virep.2016.01.001 2214-6695/Crown Copyright © 2016 Published (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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humans in the United States (Rust et al., 1999; Zeller and Bouloy, 2000). Crimean–Congo haemorrhagic fever virus is a ticktransmitted arbovirus (Genus Nairovirus) causing a potentially fatal arboviral hemorrhagic disease also in humans (Zeller and Bouloy, 2000). A number of other viruses such as Rift Valley fever (Genus Phlebovirus), the Bunyamwera group (Genus Orthobunyavirus), Nairobi sheep disease and Dera Ghazi Khan virus group (both Genus Nairovirus) cause disease in both humans and livestock (Schmaljohn and Nichol, 2007). Finally, the tick-borne Uukuniemi (Genus Phlebovirus), Hughes and Qalyub (both Genus Nairovirus) virus groups cause disease in seabirds (Schmaljohn and Nichol, 2007). However, in Australia only Akabane virus (Genus Orthobunyavirus, Simbu group) causes disease of any significance, with infection resulting in abortion and deformities in gestating cattle (Geoghegan et al., 2014). Since the 1950s, arthropod collection and subsequent virus isolation have been conducted across northern Australia to survey for known and novel arboviruses. This has resulted in the collection of numerous virus isolates which have been archived in reference collections. When surveillance for these viruses was initially conducted, and up until the 1980s, characterization was generally limited to experimental pathology in animals and serology-based classification. More recently, virus taxonomy has been simultaneously assisted and challenged by the advent of nucleic acid sequencing. The development of high-throughput sequencing (HTS), also known as next-generation sequencing, has accelerated this process. This sequencing technology is the method of choice to characterize many archived isolates as multiple virus samples can be sequenced in a single experiment using this technology. In this study, we utilized HTS to obtain genome sequences from 5 virus samples stored in archival collections, for which no information or only serological information was available. To facilitate this, a high density chip was used with multiple samples on the Personal Genome Machine (PGM, Life Technologies) platform. The sequences obtained confirmed previous serological classification for two bunyaviruses. Additional isolates were identified as two bunyaviruses and a rhabdovirus. This work confirms the power of HTS to rapidly identify viruses without prior knowledge of their identities or genome sequences. 2. Methods 2.1. Virus collection, isolation and culture Viruses were isolated from collections of mosquito and biting midges as previously described (Doherty et al., 1979, 1972; Standfast et al., 1984). Virus samples were thawed and re-cultured in Vero cells for one passage, and then subsequently in C6/36 cells for another passage. Tissue culture supernatant was harvested and then stored at −80 °C prior to use. 2.2. Viral genome sequencing The sequencing of viral RNA genomes was conducted as described previously (Warrilow et al., 2014). In brief, virus was purified from tissue culture supernatant using preferential nuclease digestion and ultra-centrifugation (RNase ONE and RQ1 DNase, Promega), followed by sequence-independent amplification. A library was constructed from the products which were then sequenced on a Personal Genome Machine (Ion Torrent PGM™, Life Technologies) using a 318 chip. 2.3. Virus sequence assembly and phylogenetic analysis The virus genome sequence was assembled de novo using Geneious R8 (Kearse et al., 2012). The generated contiguous sequences (contigs) were then mapped using related rhabdovirus or bunyavirus segments from GenBank (large, L; medium, M; and small, S) as scaffolds. The combined contigs were then used as a reference sequence with the complete sequence data to generate the final contigs to each of the segments. The open reading frames (ORFs) of each segment were used for phylogenetic analysis. Best match by Basic Local Alignment Sequence Tool for protein (BLASTP) was performed using the National Center for Biotechnology Information online tool (http://www.ncbi.nlm.nih.gov). Multiple sequence alignments were generated using the MAFFT plugin of Geneious R8 (Kearse et al., 2012). The alignment was then used as input for determining phylogenetic relationships by the maximum likelihood model using MEGA5 software (Tamura et al., 2011) with an appropriate outgroup. Robustness of the generated trees was determined using 1000 bootstrap replicates. 3. Results 3.1. Sequencing of multiple viruses on a high density semiconductor chip Eleven uncharacterized isolates were barcoded and sequenced on the Personal Genome Machine using a high density semiconductor chip. Two (Taggert and Yacaaba viruses) will be described elsewhere (Huang and Warrilow, unpublished data). Genome sequences were obtained from another three (Maprik, Mapputta and Upolu viruses), but studies describing these were published by other groups in the interim (Briese et al., 2014; Gauci et al., 2015); therefore, they were not analysed further. One virus (Tzipori virus) was determined to be a strain of bovine ephemeral fever virus (data not shown), and was not analysed further. The sequence of fragments of the remaining 5 virus genomes (Fig. 1 and Table 1) was analysed here.
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Fig. 1. Coverage density plots of virus genome sequence contigs. (A) Beatrice Hill virus; (B) Belmont virus L segment contigs 1 and 2 (upper and middle), respectively, and M segment (lower); (C) Little Sussex virus; (D) Parker's Farm virus; and (E) Thimiri virus. The maximum depth of reads is indicated on the left of the density plots, which are not presented to scale.
3.2. Beatrice Hill virus: a newly identified tibrovirus After assembly of reads from HTS of Beatrice Hill virus, a 2965 nt fragment was obtained including a large uninterrupted ORF which gave the best match by BLASTP to the L segment of a rhabdovirus (Tibrogargan virus, YP_007641376.1, 84% amino acid identity) in the “supergroup” dimarhabdovirus. On this basis, a multiple sequence alignment was conducted with members of this group to determine an appropriate classification. The phylogenetic tree generated gave good support for its classification as a new viral member assigned to the Genus Tibrovirus (Fig. 2). As there was no previous serological data, this is the first proposed taxonomic classification of this virus.
Table 1 Arboviruses characterized in this study. Name (strain)
Region(s) isolated
Insect species
Segment(s) sequenced Serological classification Neurovirulent1 Reference (average read density) (serogroup)
Beatrice Hill virus (CSIRO25) Belmont virus (CSIRO148)
Beatrice Hill, Northern Territory Rockhampton, Queensland; Beatrice Hill, Northern Territory
Genome (5734)
ND
ND
L (27,788 & 4090), M (18,733)
“Bunyavirus-like”
Yes
Little Sussex virus (Ch19546)
Charleville, Queensland
L (10,665)
ND
ND
(Doherty et al., 1979)
Parker's Farm virus (Ch19520)
Charleville, Queensland; Beatrice Hill, Northern Territory
L (1370)
ND
ND
(Doherty et al., 1972; Standfast et al., 1984)
Thimiri virus (CSIRO1)
Beatrice Hill, Northern Territory
Culicoides peregrinus Culex annulirostris, Culicoides marksi Culex annulirostris, Aedes normanensis Culex annulirostris, Culicoides marksi Culicoides histrio
L (483)
Bunyaviridae (Simbu)
Yes
(Standfast et al., 1984)
1. Indicated by death in weanling mice (Arbovirus Catalogue, CDC); ND, not determined.
(Standfast et al., 1984) (Doherty et al., 1972; Standfast et al., 1984)
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Fig. 2. The relationship of Beatrice Hill virus within the supergroup dimarhabdovirus. A maximum likelihood phylogenetic tree based on predicted amino acid sequences using the Jones–Taylor–Thornton (JTT) substitution model is shown. There are members of three genera, and Beatrice Hill virus (bold) is placed in the Genus Tibrovirus. Australian bat lyssavirus (ABL) was used to root the tree. Topological support values from 1000 bootstrap replicates are given as a percentage (those over 50 shown). GenBank accession numbers: Beatrice Hill virus, KT20480; vesicular stomatitis Indiana virus, J02428.1; bovine ephemeral fever virus, NC_002526.1; spring viremia of carp virus, U18101.2; Australian bat lyssavirus, AF418014.1; Tupaia virus, NC_007020.1; Cocal virus Indiana 2, EU373657.1; Obodhiang virus, NC_017685.1; Adelaide River virus isolate DPP61, JN935380.1; Bas-Congo virus isolate BASV-1, JX297815.1; Tibrogargan virus strain CS132, NC_020804.1; Chandipura virus strain CH157, KF468773.1; Kimberley virus isolate CS368, NC_025396.1; Coastal Plains virus strain DPP53, NC_025397.1.
3.3. Belmont virus When assembled, the reads from the Belmont virus isolate generated three sequence fragments. An initial BLASTP search of predicted ORFs resulted in best matches for two (1015 and 911 nt fragments) with the L segment of members of the Genus Orthobunyavirus (Facey's Paddock virus, AHY22330.1, 61% amino acid identity and Leanyer virus, AEA02985.1, 69% amino acid identity; respectively). The predicted ORF of the third fragment (1138 nt) had the best match with the M segment of a virus in the same genus (Utinga virus, AHY22345.1, 56% amino acid identity). To maximize sequence information for analysis, the three fragments were concatenated and used as input for multiple sequence alignments with other orthobunyaviruses. A phylogenetic tree generated from the alignment output indicated its closest relative (Leanyer virus) to be a member of the Simbu group of orthobunyaviruses (Fig. 3A). The bootstrap value (60%) indicated some support for inclusion of this virus within a clade which includes the Simbu group, but did not further resolve its classification. This is consistent with previous serology which indicated that it was “bunyavirus-like” (Standfast et al., 1984).
Fig. 3. The relationship of four uncharacterized arboviruses within the Genus Orthobunyavirus. A maximum likelihood phylogenetic tree based on predicted amino acid sequences using the Jones–Taylor–Thornton (JTT) substitution model, showing members of 5 groups within the orthobunyaviruses. (A) Belmont, (B) Little Sussex, (C) Parker's Farm and (D) Thimiri viruses are indicated in bold. Rift Valley fever virus was used to root the tree. Topological support values from 1000 bootstrap replicates are given as a percentage (those over 50 shown). GenBank accession numbers: Belmont virus L and M segments, KT720481 and KT720482 respectively; Little Sussex virus L segment, KT20483; Parker's Farm, KT20484; and Thimiri virus, KT20485. For other viruses, the L and M segments, respectively, are: Bunyamwera virus, NC_001925.1 and NC_001926.1; La Crosse, NC_004108.1 and NC_004109.1; Oropouche virus, NC_005775.1 and NC_005776.1; Akabane virus, NC_009894.1 and NC_009895.1; Chatanga virus strain LEIV-17756, EU616903.1 and EU621834.1; Rift Valley fever virus, NC_014397.1 and JF784387.1; Tahyna virus isolate 22595-6, HM036219.1 and HM036218.1; Leanyer virus isolate AusN16701, HM627178.1 and HM627176.1; Iaco virus strain BeAn314206, JN572065.1 and JN572066.1; Macaua virus strain BeAr306329, JN572068.1 and JN572069.1; Sororoca virus strain BeAr32149, JN572071.1 and JN572072.1; Wyeomyia virus, JN572080.1 and JN801034.2; Simbu virus, HE795108.1 and NC_018478.1; Sathuperi virus, NC_018461.1 and NC_018466.1; Aino virus, NC_018465.1 and NC_018459.1; Batai virus, JX846606.1 and JX846605.1; Cache Valley virus strain MNZ-92011, KC436106.1 and KC436107.1; Oya virus strain SC0806 segment L only, JX983194.1; Ilesha virus strain R5964, KF234075.1 and KF234074.1; Madrid virus strain BT4075, KF254779.1 and KF254780.1; Caraparu virus strain FMD0783, KF254793.1 and KF254788.1; Kowanyama virus, KT820202 and KT820203; Yacaaba virus, KT820208 and KT820209; Murrumbidgee virus isolate 934, KF234253.1 and NC_022596.1; Salt ash virus isolate 931, KF234256.1 and KF234257.1; Mermet virus isolate AV 782L segment only, KF697153.1; Cat Que Virus strain VN04-2108L segment only, NC_024076.1; Manzanilla virus strain DHL10M107 L segment only, KP016012.1.
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3.4. Little Sussex virus: a newly identified orthobunyavirus A 5800 nt fragment was assembled from the Little Sussex virus data. BLASTP analysis of its predicted ORF indicated that it gave the best match with a member of the Genus Orthobunyavirus (Gamboa virus, AIS74636.1, 62% amino acid identity). A single large ORF was aligned with other members of the genus and used to build a phylogenetic tree as described (Fig. 3B). The analysis indicated that it
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formed a clade with members of the California encephalitis virus group and two recently sequenced orthobunyaviruses (Kowanyama and Yacaaba viruses), branching basally within the clade. As there were no previous serological data, this is the first indication of taxonomic classification for this virus. 3.5. Parker's Farm virus: a newly identified orthobunyavirus A 960 nt sequence fragment was obtained from the assembled data. Its predicted ORF gave the best match by BLASTP to the L segment of a member of the Genus Orthobunyavirus (Facey's Paddock, AHY22330.1, 62% amino acid identity). Alignment and phylogenetic analysis indicated that it could be placed in a clade with the Simbu group of the orthobunyaviruses (Fig. 3C). As there were no previous serological data, this is also the first indication of taxonomic classification for this virus. 3.6. Thimiri virus A 958 nt sequence fragment was obtained from the isolate of Thimiri virus. Its predicted ORF gave the best match by BLASTP to the L segment of a member of the Genus Orthobunyavirus (Mermet virus, AHY22335.1, 90% amino acid identity) and a phylogenetic tree revealed the virus formed a clade with Mermet, Oya, Manzanilla and Cat Que orthobunyaviruses (Fig. 3D). These viruses are also in the Simbu group, suggesting Thimiri virus may also be a member. This result supports previous serological classification of the virus in the Simbu group (Standfast et al., 1984). 4. Discussion In this work, we have genetically characterized a number of isolates of arboviruses and demonstrated the power of HTS technologies to rapidly identify and determine the genetic relationships of viruses in samples stored for more than 30 years. This application of HTS is of particular importance in the case of responding to an emerging virus, and to identify viruses that have the potential for emergence. Virus virulence and emergence are complex issues involving the genetics of the host and the pathogen, the interplay between them, vector behaviour and environmental factors. At the level of the genetics of the virus, emergence potential is suggested by the relatedness of a particular virus to others of known virulence. In the case of the viruses characterized in this study, there are associations which suggest emergence potential in each case. Firstly, Beatrice Hill virus, which is comfortably placed in a clade with other tibroviruses, is therefore related to Bas-Congo virus, a hemorrhagic fever virus from Central Africa (Grard et al., 2012). In addition, Little Sussex virus is in a clade which includes the California encephalitis group. Finally, Belmont, Parker's Farm and Thimiri viruses are most likely related to the Simbu group which includes the cattle pathogen Akabane virus. Understanding emergence potential is not limited to the genetic relatedness of a novel virus to another of known pathology. To illustrate, the naturally attenuated West Nile virus strain in Australia (Kunjin virus or WNVKUN) has 98% amino acid identity to the pathogenic New York strain (Audsley et al., 2011). Hence, a further consideration is that the risk of emergence may be enhanced by a small number of nucleotide changes within a virulence determinant. For example, a single amino acid change in a low virulence strain of WNV (T249P in the NS3 helicase) resulted in increased virulence in American crows (Brault et al., 2007). Hence, a new virulent strain may conceivably emerge from a less virulent strain. This was exemplified, again by WNVKUN, when it emerged as a more pathogenic strain in Australian horses in 2011 (Frost et al., 2012). With regard to the viruses in this study, previous studies in animal models indicated that Belmont and Thimiri viruses are potentially neurovirulent (Table 1) so there is the potential to cause clinical disease for these viruses. The virulence of the other viruses is yet to be established. Beatrice Hill and Thimiri viruses were isolated from single species of biting midge (Table 1). Interestingly, three of the other viruses described were isolated from two different species of vector, either from a mosquito and a biting midge (Little Sussex and Parker's Farm viruses) or two species of biting midge (Belmont virus). All vectors with the exception of the vector for Thimiri virus (Culicoides histrio) have been observed to feed on mammals including humans (Jansen et al., 2009; Muller et al., 1981; Van Den Hurk et al., 2003). However, there have been no recorded cases of disease associated with any of these viruses. But in consideration of their phylogenetics, neurovirulence in animals, and vector feeding behaviour, a risk of causing disease in future is theoretically possible. In particular, Belmont virus meets all the discussed criteria for emergence potential, and could be considered in cases of unexplained febrile disease in northern Australia. In conclusion, this study identified one isolate, Beatrice Hill virus, as a tibrovirus. Also, the study expanded the number of known orthobunyaviruses, characterizing three probable members of the Simbu group (Belmont, Parker's Farm and Thimiri viruses), and an additional orthobunyavirus outside this group (Little Sussex virus). The sequence data obtained will enable the design of reagents for PCR-based assays for future disease surveillance. Our findings have elucidated our understanding of the relationships among the arboviruses of northern Australia. They also reveal the rich diversity of viruses in the Australian landscape, and suggest that there are many yet to be discovered. Acknowledgements We would like to acknowledge those who originally obtained the virus isolates including R.L. Doherty, H.A. Standfast, T.D. St George and their colleagues; without whose labours, this work would not have been possible. We thank Andrew Van Den
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Hurk and Ian Mackay for comments on the manuscript. This was an internally funded project of Queensland Health. The authors have no conflict of interest to declare. References Arbovirus Catalogue (CDC). June 2015 ed. https://wwwn.cdc.gov/Arbocat/Default.aspx. Audsley, M., Edmonds, J., Liu, W., Mokhonov, V., Mokhonova, E., Melian, E.B., Prow, N., Hall, R.A., Khromykh, A.A., 2011. Virulence determinants between New York 99 and Kunjin strains of West Nile virus. Virology 414 (1), 63–73. Brault, A.C., Huang, C.Y., Langevin, S.A., Kinney, R.M., Bowen, R.A., Ramey, W.N., Panella, N.A., Holmes, E.C., Powers, A.M., Miller, B.R., 2007. A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat. Genet. 39 (9), 1162–1166. Briese, T., Chowdhary, R., Travassos da Rosa, A., Hutchison, S.K., Popov, V., Street, C., Tesh, R.B., Lipkin, W.I., 2014. 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