Abstract
Hemorrhagic diseases caused by epizootic hemorrhagic disease virus or by bluetongue virus (BTV) are the most important orbivirus diseases affecting ruminants, including white-tailed deer (WTD). Bluetongue virus is of particular concern for farmed WTD in Florida, given its lethality and its wide distribution throughout the state. This study reports the clinical findings, ancillary diagnostics, and genomic characterization of two BTV serotype 1 strains isolated from two farmed WTD, from two different farms in Florida in 2019 and 2022. Phylogenetic and genetic analyses indicated that these two novel BTV-1 strains were reassortants. In addition, our analyses reveal that most genome segments of these strains were acquired from BTVs previously detected in ruminants in Florida, substantiating their endemism in the Southeastern U.S. Our findings underscore the need for additional research to determine the genetic diversity of BTV strains in Florida, their prevalence, and the potential risk of new BTV strains to WTD and other ruminants.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_Fig2_HTML.png)
Similar content being viewed by others
References
Adams KP, Murphy BP, Ross MD (2016) Captive white-tailed deer industry—current status and growing threat. Wildl Soc Bull 40:14–19. https://doi.org/10.1002/wsb.627
Purse BV, Carpenter S, Venter GJ, Bellis G, Mullens BA (2015) Bionomics of temperate and tropical Culicoides midges: knowledge gaps and consequences for transmission of Culicoides-borne viruses. Annu Rev Entomol 60:373–392. https://doi.org/10.1146/annurev-ento-010814-020614
Ahasan MS, Subramaniam K, Lednicky JA, Loeb JC, Sayler KA, Wisely SM, Waltzek TB (2018) Complete genome sequence of epizootic hemorrhagic disease virus serotype 6, isolated from Florida white-tailed deer (Odocoileus virginianus). Genome Announc 6:e00160–e00118. https://doi.org/10.1128/genomeA.00160-18
Ahasan MS, Subramaniam K, Sayler KA, Loeb JC, Popov VL, Lednicky JA, Wisely SM, Campos Krauer JM, Waltzek TB (2019) Molecular characterization of a novel reassortment mammalian orthoreovirus type 2 isolated from a Florida white-tailed deer fawn. Virus Res 270. https://doi.org/10.1016/j.virusres.2019.197642
Ahasan MS, Campos Krauer JM, Subramaniam K, Lednicky JA, Loeb JC, Sayler KA, Wisely SM, Waltzek TB (2019) Complete genome sequence of mobuck virus isolated from a florida white-tailed deer (Odocoileus virginianus). Microbiol Resour Announc 8:e01324–e01318. https://doi.org/10.1128/MRA.01324-18
Ahasan MS, Subramaniam K, Campos Krauer JM, Sayler KA, Loeb JC, Goodfriend OF, Barber HM, Stephenson CJ, Popov VL, Charrel RN et al (2019) Three new orbivirus species isolated from farmed white-tailed deer (Odocoileus virginianus) in the United States. Viruses 12. https://doi.org/10.3390/v12010013
Cauvin A, Dinh ETN, Orange JP, Shuman RM, Blackburn JK, Wisely SM (2020) Antibodies to epizootic hemorrhagic disease virus (EHDV) in farmed and wild florida white-tailed deer (Odocoileus virginianus). J Wildl Dis 56:208–213
Viadanna PHO, Rodrigues TCS, Subramaniam K, Campos Krauer JM, Lednicky JA, Loeb JC, Wisely SM, Waltzek TB (2021) Genome sequence of a yunnan orbivirus isolated from a dead florida white-tailed deer (Odocoileus virginianus). Microbiol Resour Announc 10. https://doi.org/10.1128/MRA.00168-21
Uribasterra MG, Orange JP, Dinh ETN, Peters C, Peters RM, Goodfriend O, Wisely SM, Blackburn JK (2020) Epizootic hemorrhagic disease virus and bluetongue virus seroprevalence in wild white-tailed deer (Odocoileus virginianus) in Florida, USA. J Wildl Dis 56:928–932. https://doi.org/10.7589/2019-10-263
Rodrigues TCS, Lednicky JA, Loeb JC, Campos Krauer JM, Wisely SM, Waltzek TB, Subramaniam K (2020) Genome sequence of a CHeRI orbivirus 3 strain isolated from a dead white-tailed deer (Odocoileus virginianus) in Florida, USA. Microbiol Resour Announc 9:e00523–e00520. https://doi.org/10.1128/MRA.00523-20
Rodrigues TCS, Viadanna PHO, Subramaniam K, Hawkins IK, Jeon AB, Loeb JC, Krauer JMC, Lednicky JA, Wisely SM, Waltzek TB (2022) Characterization of a novel reassortant epizootic hemorrhagic disease virus serotype 6 strain isolated from diseased white-tailed deer (Odocoileus virginianus) on a Florida farm. Viruses 14(5):1012. https://doi.org/10.3390/v14051012
Cottingham SL, White ZS, Wisely SM, Campos-Krauer JM (2021) A mortality-based description of EHDV and BTV prevalence in farmed white-tailed deer (Odocoileus virginianus) in Florida, USA. Viruses 13(8):1443. https://doi.org/10.3390/v13081443
Du Toit RM (1944) The transmission of bluetongue and horsesickness by Culicoides. Onderstepoort J Vet Sci 19:7–16
Erasmus BJ (1990) Chapter 21 - Bluetongue Virus. In Virus Infections of Vertebrates Series; Dinter, Z., Morein, B.B.T.-V.I. of R., Eds.; Elsevier, ; pp. 227–237 ISBN 978-0-444-87312-5
U.S. Department of Agriculture. Bluetongue (2022) Available at: https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/animal-disease-information/cattle-disease-information/bluetongue-disease-info
Mertens PPC, Diprose J (2004) The bluetongue virus core: a nano-scale transcription machine. Virus Res 101:29–43. https://doi.org/10.1016/j.virusres.2003.12.004
Ratinier M, Caporale M, Golder M, Franzoni G, Allan K, Nunes SF, Armezzani A, Bayoumy A, Rixon F, Shaw A et al (2011) Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog 7:e1002477. https://doi.org/10.1371/journal.ppat.1002477
Roy P, Urakawa T, Van Dijk AA, Erasmus BJ (1990) Recombinant virus vaccine for bluetongue disease in sheep. J Virol 64:1998–2003. https://doi.org/10.1128/JVI.64.5.1998-2003.1990
Roy P, Noad R (2006) Bluetongue virus assembly and morphogenesis. Curr Top Microbiol Immunol 309:87–116. https://doi.org/10.1007/3-540-30773-7_4
Hofmann MA, Renzullo S, Mader M, Chaignat V, Worwa G, Thuer B (2008) Genetic characterization of toggenburg orbivirus, a new bluetongue virus, from goats, Switzerland. Emerg Infect Dis 14:1855–1861. https://doi.org/10.3201/eid1412.080818
Lorusso A, Sghaier S, Di Domenico M, Barbria ME, Zaccaria G, Megdich A, Portanti O, Seliman I, Ben; Spedicato M, Pizzurro F et al (2018) Analysis of bluetongue serotype 3 spread in Tunisia and discovery of a novel strain related to the bluetongue virus isolated from a commercial sheep pox vaccine. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 59:63–71. https://doi.org/10.1016/j.meegid.2018.01.025
Maan S, Maan NS, Nomikou K, Veronesi E, Bachanek-Bankowska K, Belaganahalli MN, Attoui H, Mertens (2011) P.P.C. complete genome characterisation of a novel 26th bluetongue virus serotype from Kuwait. PLoS ONE 6:e26147. https://doi.org/10.1371/journal.pone.0026147
Marcacci M, Sant S, Mangone I, Goria M, Dondo A, Zoppi S, van Gennip RGP, Radaelli MC, Cammà C, van Rijn PA et al (2018) One after the other: a novel Bluetongue virus strain related to Toggenburg virus detected in the Piedmont region (North-western Italy), extends the panel of novel atypical BTV strains. Transbound Emerg Dis 65:370–374. https://doi.org/10.1111/tbed.12822
Savini G, Puggioni G, Meloni G, Marcacci M, Di Domenico M, Rocchigiani AM, Spedicato M, Oggiano A, Manunta D, Teodori L et al (2017) Novel putative Bluetongue virus in healthy goats from Sardinia, Italy. Infect Genet Evol 51:108–117. https://doi.org/10.1016/j.meegid.2017.03.021
Yang H, Gu W, Li Z, Zhang L, Liao D, Song J, Shi B, Hasimu J, Li Z, Yang Z et al (2021) Novel putative bluetongue virus serotype 29 isolated from inapparently infected goat in **njiang of China. Transbound Emerg Dis 68:2543–2555. https://doi.org/10.1111/tbed.13927
Zientara S, Sailleau C, Viarouge C, Höper D, Beer M, Jenckel M, Hoffmann B, Romey A, Bakkali-Kassimi L, Fablet A et al (2014) Novel bluetongue virus in goats, Corsica, France, 2014. Emerg Infect Dis 20:2123–2125. https://doi.org/10.3201/eid2012.140924
Maclachlan NJ, Mayo CE (2013) Potential strategies for control of bluetongue, a globally emerging, Culicoides-transmitted viral disease of ruminant livestock and wildlife. Antiviral Res 99:79–90. https://doi.org/10.1016/j.antiviral.2013.04.021
Bonneau KR, Mullens BA, MacLachlan NJ (2001) Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J Virol 75:8298–8305. https://doi.org/10.1128/jvi.75.17.8298-8305.2001
Mayo C, McDermott E, Kopanke J, Stenglein M, Lee J, Mathiason C, Carpenter M, Reed K, Perkins TA (2020) Ecological dynamics impacting bluetongue virus transmission in North America. Front Vet Sci 7:186. https://doi.org/10.3389/fvets.2020.00186
Vijaykrishna D, Mukerji R, Smith (2015) G.J.D. RNA virus reassortment: an evolutionary mechanism for host jumps and immune evasion. PLOS Pathog 11:e1004902
Gaudreault NN, Mayo CE, Jasperson DC, Crossley BM, Breitmeyer RE, Johnson DJ, Ostlund EN, MacLachlan NJ, Wilson WC (2014) Whole genome sequencing and phylogenetic analysis of Bluetongue virus serotype 2 strains isolated in the Americas including a novel strain from the western United States. J Vet diagnostic Investig 26:553–557. https://doi.org/10.1177/1040638714536902
Schirtzinger EE, Jasperson DC, Ostlund EN, Johnson DJ, Wilson WC (2018) Recent US bluetongue virus serotype 3 isolates found outside of Florida indicate evidence of reassortment with co-circulating endemic serotypes. J Gen Virol 99:157–168. https://doi.org/10.1099/jgv.0.000965
AVMA Guidelines for Euthanasia of Animals, American Veterinary Medical Association;
Lambert AJ, Martin DA, Lanciotti RS (2003) Detection of north american eastern and western equine encephalitis viruses by nucleic acid amplification assays. J Clin Microbiol 41:379–385. https://doi.org/10.1128/JCM.41.1.379-385.2003
Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE et al (2000) Rapid detection of west nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol 38:4066–4071. https://doi.org/10.1128/JCM.38.11.4066-4071.2000
Wernike K, Hoffmann B, Beer M (2015) Simultaneous detection of five notifiable viral diseases of cattle by single-tube multiplex real-time RT-PCR. J Virol Methods 217:28–35. https://doi.org/10.1016/j.jviromet.2015.02.023
Wood DE, Salzberg SL (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46. https://doi.org/10.1186/gb-2014-15-3-r46
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Caporale M, Di Gialleonorado L, Janowicz A, Wilkie G, Shaw A, Savini G, Van Rijn PA, Mertens P, Di Ventura M, Palmarini M (2014) Virus and host factors affecting the clinical outcome of bluetongue virus infection. J Virol 88:10399–10411. https://doi.org/10.1128/JVI.01641-14
Parsonson IM (1990) Pathology and pathogenesis of bluetongue infections. Curr Top Microbiol Immunol 162:119–141. https://doi.org/10.1007/978-3-642-75247-6_5
Rivera NA, Varga C, Ruder MG, Dorak SJ, Roca AL, Novakofski JE, Mateus-Pinilla NE (2021) Bluetongue and epizootic hemorrhagic disease in the United States of America at the wildlife-livestock interface. Pathog 10. https://doi.org/10.3390/pathogens10080915
Johnson DJ, Ostlund EN, Stallknecht DE, Goekjian VH, Jenkins-Moore M, Harris SC (2006) First report of bluetongue virus serotype 1 isolated from a white-tailed deer in the United States. J Vet diagnostic Investig 18:398–401. https://doi.org/10.1177/104063870601800415
Alkhamis MA, Aguilar-Vega C, Fountain-Jones NM, Lin K, Perez AM, Sánchez-Vizcaíno JM (2020) Global emergence and evolutionary dynamics of bluetongue virus. Sci Rep 10:21677. https://doi.org/10.1038/s41598-020-78673-9
Nason EL, Rothagel R, Mukherjee SK, Kar AK, Forzan M, Prasad BVV, Roy P (2004) Interactions between the inner and outer capsids of bluetongue virus. J Virol 78:8059–8067. https://doi.org/10.1128/JVI.78.15.8059-8067.2004
Gumm ID, Newman JF (1982) The preparation of purified bluetongue virus group antigen for use as a diagnostic reagent. Arch Virol 72:83–93. https://doi.org/10.1007/BF01314453
Roy P (1992) Bluetongue virus proteins. J Gen Virol 73(12):3051–3064. https://doi.org/10.1099/0022-1317-73-12-3051
Carpi G, Holmes EC, Kitchen A (2010) The evolutionary dynamics of bluetongue virus. J Mol Evol 70:583–592. https://doi.org/10.1007/s00239-010-9354-y
Anderson J, Bréard E, Lövgren Bengtsson K, Grönvik K-O, Zientara S, Valarcher J-F, Hägglund S (2014) Purification, stability, and immunogenicity analyses of five bluetongue virus proteins for use in development of a subunit vaccine that allows differentiation of infected from vaccinated animals. Clin Vaccine Immunol 21:443–452. https://doi.org/10.1128/CVI.00776-13
Author information
Authors and Affiliations
Contributions
Conceptualization: P.H.O.V.; S.M.W.; K.S.Methodology: P.H.O.V.; J.C.L.; Z.S.W.; J.A.L.; K.S.Formal analysis: P.H.O.V.; K.S.Investigation: P.H.O.V.; T.D.L.; E.D.; J.C.L.; K.N.W.; Z.S.W.Resources: S.M.W.; K.S.Writing - Original Draft: P.H.O.V.; S.G.G.; K.S.Writing - Review & Editing: P.H.O.V.; J.M.C.K.; J.A.L.; T.B.W.; S.M.W.; K.S.Visualization: P.H.O.V.Supervision: K.S.Project administration: S.M.W.; K.S.Funding acquisition: S.M.W.; K.S.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Edited by Zhen Fu.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
![](http://media.springernature.com/lw1/springer-static/esm/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_MOESM1_ESM.png)
![](http://media.springernature.com/lw1/springer-static/esm/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_MOESM2_ESM.png)
![](http://media.springernature.com/lw1/springer-static/esm/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_MOESM3_ESM.png)
![](http://media.springernature.com/lw1/springer-static/esm/art%3A10.1007%2Fs11262-023-02019-6/MediaObjects/11262_2023_2019_MOESM4_ESM.png)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Viadanna, P.H.O., Grace, S.G., Logan, T.D. et al. Characterization of two novel reassortant bluetongue virus serotype 1 strains isolated from farmed white-tailed deer (Odocoileus virginianus) in Florida, USA. Virus Genes 59, 732–740 (2023). https://doi.org/10.1007/s11262-023-02019-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-023-02019-6