Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sequence Dataset Preparation
2.2. Phylodynamic and Phylogeographic Analysis
2.3. Selective Pressure Analysis
2.4. Homology Modelling
3. Results
3.1. Datasets
3.2. Phylodynamic and Phylogeographic Analyses
3.3. Selective Pressures Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Benavente, J.; Martínez-Costas, J. Avian Reovirus: Structure and Biology. Virus Res. 2007, 123, 105–119. [Google Scholar] [CrossRef]
- Egana-Labrin, S.; Broadbent, A.J. Avian Reovirus: A Furious and Fast Evolving Pathogen. J. Med. Microbiol. 2023, 72, 1761. [Google Scholar] [CrossRef]
- Kumar, D.; Dhama, K.; Agarwal, R.K.; Sonal; Singh, P.; Ravikumar, G.; Malik, Y.S.; Mishra, B.P. Avian Reoviruses. In Recent Advances in Animal Virology; Springer: Singapore, 2019; pp. 289–300. [Google Scholar] [CrossRef]
- Pitcovski, J.; Goyal, S.M. Avian Reovirus Infections. In Diseases of Poultry; Wiley: Hoboken, NJ, USA, 2019; pp. 382–400. [Google Scholar] [CrossRef]
- Chengcheng, Z.; Qingqing, Z.; Xiaomiao, H.; Wei, L.; Xiaorong, Z.; Yantao, W. IFI16 Plays a Critical Role in Avian Reovirus Induced Cellular Immunosuppression and Suppresses Virus Replication. Poult. Sci. 2024, 103, 103506. [Google Scholar] [CrossRef]
- Lin, H.Y.; Chuang, S.T.; Chen, Y.T.; Shih, W.L.; Chang, C.D.; Liu, H.J. Avian Reovirus-Induced Apoptosis Related to Tissue Injury. Avian Pathol. 2007, 36, 155–159. [Google Scholar] [CrossRef]
- Shih, W.L.; Hsu, H.W.; Liao, M.H.; Lee, L.H.; Liu, H.J. Avian Reovirus ΣC Protein Induces Apoptosis in Cultured Cells. Virology 2004, 1, 65–74. [Google Scholar] [CrossRef]
- Labrada, L.; Bodelón, G.; Viñuela, J.; Benavente, J. Avian Reoviruses Cause Apoptosis in Cultured Cells: Viral Uncoating, but Not Viral Gene Expression, Is Required for Apoptosis Induction. J. Virol. 2002, 76, 7932. [Google Scholar] [CrossRef]
- Egaña-Labrin, S.; Jerry, C.; Roh, H.J.; da Silva, A.P.; Corsiglia, C.; Crossley, B.; Rejmanek, D.; Gallardo, R.A. Avian Reoviruses of the Same Genotype Induce Different Pathology in Chickens. Avian Dis. 2021, 65, 530–540. [Google Scholar] [CrossRef]
- Sellers, H.S. Avian Reoviruses from Clinical Cases of Tenosynovitis: An Overview of Diagnostic Approaches and 10-Year Review of Isolations and Genetic Characterization. Avian Dis. 2023, 66, 420–426. [Google Scholar] [CrossRef]
- Sellers, H.S. Current Limitations in Control of Viral Arthritis and Tenosynovitis Caused by Avian Reoviruses in Commercial Poultry. Vet. Microbiol. 2017, 206, 152–156. [Google Scholar] [CrossRef] [PubMed]
- Wickramasinghe, R.; Meanger, J.; Enriquez, C.E.; Wilcox, G.E. Avian Reovirus Proteins Associated with Neutralization of Virus Infectivity. Virology 1993, 194, 688–696. [Google Scholar] [CrossRef] [PubMed]
- Lu, H.; Tang, Y.; Dunn, P.A.; Wallner-Pendleton, E.A.; Lin, L.; Knoll, E.A. Isolation and Molecular Characterization of Newly Emerging Avian Reovirus Variants and Novel Strains in Pennsylvania, USA, 2011–2014. Sci. Rep. 2015, 5, 14727. [Google Scholar] [CrossRef]
- Kant, A.; Balk, F.; Born, L.; Van Roozelaar, D.; Heijmans, J.; Gielkens, A.; Ter Huurne, A. Classification of Dutch and German Avian Reoviruses by Sequencing the Sigma C Protein. Vet. Res. 2003, 34, 203–212. [Google Scholar] [CrossRef]
- Liu, H.J.; Lee, L.H.; Hsu, H.W.; Kuo, L.C.; Liao, M.H. Molecular Evolution of Avian Reovirus:: Evidence for Genetic Diversity and Reassortment of the S-Class Genome Segments and Multiple Cocirculating Lineages. Virology 2003, 314, 336–349. [Google Scholar] [CrossRef]
- Gamble, T.C.; Sellers, H.S. Field Control of Avian Reoviruses in Commercial Broiler Production. Avian Dis. 2022, 66, 427–431. [Google Scholar] [CrossRef]
- Troxler, S.; Rigomier, P.; Bilic, I.; Liebhart, D.; Prokofieva, I.; Robineau, B.; Hess, M. Identification of a New Reovirus Causing Substantial Losses in Broiler Production in France, despite Routine Vaccination of Breeders. Vet. Rec. 2013, 172, 556. [Google Scholar] [CrossRef]
- Lublin, A.; Goldenberg, D.; Rosenbluth, E.; Heller, E.D.; Pitcovski, J. Wide-Range Protection against Avian Reovirus Conferred by Vaccination with Representatives of Four Defined Genotypes. Vaccine 2011, 29, 8683–8688. [Google Scholar] [CrossRef]
- Standley, K. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability.(Outlines Version 7). Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef]
- Nguyen, L.T.; Schmidt, H.A.; Von Haeseler, A.; Minh, B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
- Kosakovsky Pond, S.L.; Posada, D.; Gravenor, M.B.; Woelk, C.H.; Frost, S.D.W. GARD: A Genetic Algorithm for Recombination Detection. Bioinformatics 2006, 22, 3096–3098. [Google Scholar] [CrossRef]
- Rambaut, A.; Lam, T.T.; Max Carvalho, L.; Pybus, O.G. Exploring the Temporal Structure of Heterochronous Sequences Using TempEst (Formerly Path-O-Gen). Virus Evol. 2016, 2, vew007. [Google Scholar] [CrossRef]
- Layan, M.; Müller, N.F.; Dellicour, S.; De Maio, N.; Bourhy, H.; Cauchemez, S.; Baele, G. Impact and Mitigation of Sampling Bias to Determine Viral Spread: Evaluating Discrete Phylogeography through CTMC Modeling and Structured Coalescent Model Approximations. Virus Evol. 2023, 9, vead010. [Google Scholar] [CrossRef] [PubMed]
- Suchard, M.A.; Lemey, P.; Baele, G.; Ayres, D.L.; Drummond, A.J.; Rambaut, A. Bayesian Phylogenetic and Phylodynamic Data Integration Using BEAST 1.10. Virus Evol. 2018, 4, vey016. [Google Scholar] [CrossRef]
- Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. JModelTest 2: More Models, New Heuristics and Parallel Computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [PubMed]
- Baele, G.; Lemey, P.; Bedford, T.; Rambaut, A.; Suchard, M.A.; Alekseyenko, A.V. Improving the Accuracy of Demographic and Molecular Clock Model Comparison While Accommodating Phylogenetic Uncertainty. Mol. Biol. Evol. 2012, 29, 2157–2167. [Google Scholar] [CrossRef] [PubMed]
- Hill, V.; Baele, G. Bayesian Estimation of Past Population Dynamics in BEAST 1.10 Using the Skygrid Coalescent Model. Mol. Biol. Evol. 2019, 36, 2620–2628. [Google Scholar] [CrossRef] [PubMed]
- Lemey, P.; Rambaut, A.; Drummond, A.J.; Suchard, M.A. Bayesian Phylogeography Finds Its Roots. PLoS Comput. Biol. 2009, 5, e1000520. [Google Scholar] [CrossRef] [PubMed]
- Bielejec, F.; Baele, G.; Vrancken, B.; Suchard, M.A.; Rambaut, A.; Lemey, P. SpreaD3: Interactive Visualization of Spatiotemporal History and Trait Evolutionary Processes. Mol. Biol. Evol. 2016, 33, 2167–2169. [Google Scholar] [CrossRef] [PubMed]
- Team, R.C. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2013. [Google Scholar]
- Murrell, B.; Moola, S.; Mabona, A.; Weighill, T.; Sheward, D.; Kosakovsky Pond, S.L.; Scheffler, K. FUBAR: A Fast, Unconstrained Bayesian AppRoximation for Inferring Selection. Mol. Biol. Evol. 2013, 30, 1196–1205. [Google Scholar] [CrossRef]
- Kosakovsky Pond, S.L.; Frost, S.D.W. Not so Different after All: A Comparison of Methods for Detecting Amino Acid Sites under Selection. Mol. Biol. Evol. 2005, 22, 1208–1222. [Google Scholar] [CrossRef]
- Murrell, B.; Wertheim, J.O.; Moola, S.; Weighill, T.; Scheffler, K.; Kosakovsky Pond, S.L. Detecting Individual Sites Subject to Episodic Diversifying Selection. PLoS Genet. 2012, 8, e1002764. [Google Scholar] [CrossRef]
- Kosakovsky Pond, S.L.; Frost, S.D.W.; Muse, S.V. HyPhy: Hypothesis Testing Using Phylogenies. Bioinformatics 2005, 21, 676–679. [Google Scholar] [CrossRef]
- Kosakovsky Pond, S.L.; Wisotsky, S.R.; Escalante, A.; Magalis, B.R.; Weaver, S. Contrast-FEL—A Test for Differences in Selective Pressures at Individual Sites among Clades and Sets of Branches. Mol. Biol. Evol. 2021, 38, 1184–1198. [Google Scholar] [CrossRef]
- Weaver, S.; Shank, S.D.; Spielman, S.J.; Li, M.; Muse, S.V.; Kosakovsky Pond, S.L. Datamonkey 2.0: A Modern Web Application for Characterizing Selective and Other Evolutionary Processes. Mol. Biol. Evol. 2018, 35, 773–777. [Google Scholar] [CrossRef]
- Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; De Beer, T.A.P.; Rempfer, C.; Bordoli, L.; et al. SWISS-MODEL: Homology Modelling of Protein Structures and Complexes. Nucleic Acids Res. 2018, 46, W296–W303. [Google Scholar] [CrossRef]
- Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera—A Visualization System for Exploratory Research and Analysis. J. Comput. Chem. 2004, 25, 1605–1612. [Google Scholar] [CrossRef]
- Jendele, L.; Krivak, R.; Skoda, P.; Novotny, M.; Hoksza, D. PrankWeb: A Web Server for Ligand Binding Site Prediction and Visualization. Nucleic Acids Res. 2019, 47, W345–W349. [Google Scholar] [CrossRef]
- Goldenberg, D. Avian Reovirus in Israel, Variants and Vaccines—A Review. Avian Dis. 2022, 66, 447–451. [Google Scholar] [CrossRef]
- Liu, R.; Luo, D.; Gao, J.; Li, K.; Liu, C.; Qi, X.; Cui, H.; Zhang, Y.; Wang, S.; Wang, X.; et al. A Novel Variant of Avian Reovirus Is Pathogenic to Vaccinated Chickens. Viruses 2023, 15, 1800. [Google Scholar] [CrossRef]
- Vasserman, Y.; Eliahoo, D.; Hemsani, E.; Kass, N.; Ayali, G.; Pokamunski, S.; Pitcovski, J. The Influence of Reovirus Sigma C Protein Diversity on Vaccination Efficiency. Avian Dis. 2004, 48, 271–278. [Google Scholar] [CrossRef]
- Yamaguchi, M.; Miyaoka, Y.; Hasan, M.A.; Kabir, M.H.; Shoham, D.; Murakami, H.; Takehara, K. Isolation and Molecular Characterization of Fowl Adenovirus and Avian from Breeder Chickens in Japan in 2019–2021. J. Vet. Med. Sci. 2022, 84, 238. [Google Scholar] [CrossRef]
- Ho, S.Y.W.; Shapiro, B. Skyline-Plot Methods for Estimating Demographic History from Nucleotide Sequences. Mol. Ecol. Resour. 2011, 11, 423–434. [Google Scholar] [CrossRef]
- Gandon, S.; Mackinnon, M.; Nee, S.; Read, A. Imperfect Vaccination: Some Epidemiological and Evolutionary Consequences. Proc. R. Soc. B Biol. Sci. 2003, 270, 1129–1136. [Google Scholar] [CrossRef]
- Bernhauerová, V. Adapting to Vaccination. Nat. Ecol. Evol. 2022, 6, 673–674. [Google Scholar] [CrossRef]
- Gandon, S.; Day, T. The Evolutionary Epidemiology of Vaccination. J. R. Soc. Interface 2007, 4, 803–817. [Google Scholar] [CrossRef]
- Read, A.F.; Baigent, S.J.; Powers, C.; Kgosana, L.B.; Blackwell, L.; Smith, L.P.; Kennedy, D.A.; Walkden-Brown, S.W.; Nair, V.K. Imperfect Vaccination Can Enhance the Transmission of Highly Virulent Pathogens. PLoS Biol. 2015, 13, e1002198. [Google Scholar] [CrossRef]
- Franzo, G.; Legnardi, M.; Tucciarone, C.M.; Drigo, M.; Martini, M.; Cecchinato, M. Evolution of Infectious Bronchitis Virus in the Field after Homologous Vaccination Introduction. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842459/ (accessed on 7 April 2020).
- Franzo, G.; Faustini, G.; Tucciarone, C.M.; Poletto, F.; Tonellato, F.; Cecchinato, M.; Legnardi, M. The Effect of Global Spread, Epidemiology, and Control Strategies on the Evolution of the GI-19 Lineage of Infectious Bronchitis Virus. Viruses 2024, 16, 481. [Google Scholar] [CrossRef]
- Franzo, G.; Tucciarone, C.M.; Blanco, A.; Nofrarías, M.; Biarnés, M.; Cortey, M.; Majó, N.; Catelli, E.; Cecchinato, M. Effect of Different Vaccination Strategies on IBV QX Population Dynamics and Clinical Outbreaks. Vaccine 2016, 34, 5670–5676. [Google Scholar] [CrossRef]
- Calvo, P.G.; Fox, G.C.; Hermo Parrado, X.L.; Llamas-Saiz, A.L.; Costas, C.; Martínez-Costas, J.; Benavente, J.; Van Raaij, M.J. Structure of the Carboxy-Terminal Receptor-Binding Domain of Avian Reovirus Fibre SigmaC. J. Mol. Biol. 2005, 354, 137–149. [Google Scholar] [CrossRef]
- Franzo, G.; Massi, P.; Tucciarone, C.M.; Barbieri, I.; Tosi, G.; Fiorentini, L.; Ciccozzi, M.; Lavazza, A.; Cecchinato, M.; Moreno, A. Think Globally, Act Locally: Phylodynamic Reconstruction of Infectious Bronchitis Virus (IBV) QX Genotype (GI-19 Lineage) Reveals Different Population Dynamics and Spreading Patterns When Evaluated on Different Epidemiological Scales. PLoS ONE 2017, 12, e0184401. [Google Scholar] [CrossRef]
- Franzo, G.; Cecchinato, M.; Tosi, G.; Fiorentini, L.; Faccin, F.; Tucciarone, C.M.; Trogu, T.; Barbieri, I.; Massi, P.; Moreno, A. GI-16 Lineage (624/I or Q1), There and Back Again: The History of One of the Major Threats for Poultry Farming of Our Era. PLoS ONE 2018, 13, e0203513. [Google Scholar] [CrossRef]
- Houta, M.H.; Hassan, K.E.; Legnardi, M.; Tucciarone, C.M.; Abdel-Moneim, A.S.; Cecchinato, M.; El-Sawah, A.A.; Ali, A.; Franzo, G. Phylodynamic and Recombination Analyses of Avian Infectious Bronchitis Gi-23 Reveal a Widespread Recombinant Cluster and New among-Countries Linkages. Animals 2021, 11, 3182. [Google Scholar] [CrossRef]
- Hall, M.D.; Woolhouse, M.E.J.; Rambaut, A. The Effects of Sampling Strategy on the Quality of Reconstruction of Viral Population Dynamics Using Bayesian Skyline Family Coalescent Methods: A Simulation Study. Virus Evol. 2016, 2, vew003. [Google Scholar] [CrossRef]
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Franzo, G.; Tucciarone, C.M.; Faustini, G.; Poletto, F.; Baston, R.; Cecchinato, M.; Legnardi, M. Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study. Viruses 2024, 16, 796. https://doi.org/10.3390/v16050796
Franzo G, Tucciarone CM, Faustini G, Poletto F, Baston R, Cecchinato M, Legnardi M. Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study. Viruses. 2024; 16(5):796. https://doi.org/10.3390/v16050796
Chicago/Turabian StyleFranzo, Giovanni, Claudia Maria Tucciarone, Giulia Faustini, Francesca Poletto, Riccardo Baston, Mattia Cecchinato, and Matteo Legnardi. 2024. "Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study" Viruses 16, no. 5: 796. https://doi.org/10.3390/v16050796
APA StyleFranzo, G., Tucciarone, C. M., Faustini, G., Poletto, F., Baston, R., Cecchinato, M., & Legnardi, M. (2024). Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study. Viruses, 16(5), 796. https://doi.org/10.3390/v16050796