Impact of viral features, host jumps and phylogeography on the rapid evolution of Aleutian mink disease virus (AMDV).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 08 2021
12 08 2021
Historique:
received:
27
03
2021
accepted:
03
08
2021
entrez:
13
8
2021
pubmed:
14
8
2021
medline:
16
11
2021
Statut:
epublish
Résumé
Aleutian mink disease virus (AMDV) is one the most relevant pathogens of domestic mink, where it can cause significant economic losses, and wild species, which are considered a threat to mink farms. Despite their relevance, many aspects of the origin, evolution, and geographic and host spreading patterns of AMDV have never been investigated on a global scale using a comprehensive biostatistical approach. The present study, benefitting from a large dataset of sequences collected worldwide and several phylodynamic-based approaches, demonstrates the ancient origin of AMDV and its broad, unconstrained circulation from the initial intercontinental spread to the massive among-country circulation, especially within Europe, combined with local persistence and evolution. Clear expansion of the viral population size occurred over time until more effective control measures started to be applied. The role of frequent changes in epidemiological niches, including different hosts, in driving the high nucleotide and amino acid evolutionary rates was also explored by comparing the strengths of selective pressures acting on different populations. The obtained results suggest that the viral passage among locations and between wild and domesticated animals poses a double threat to farm profitability and animal welfare and health, which is particularly relevant for endangered species. Therefore, further efforts must be made to limit viral circulation and to refine our knowledge of factors enhancing AMDV spread, particularly at the wild-domestic interface.
Identifiants
pubmed: 34385578
doi: 10.1038/s41598-021-96025-z
pii: 10.1038/s41598-021-96025-z
pmc: PMC8360955
doi:
Substances chimiques
DNA, Viral
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
16464Informations de copyright
© 2021. The Author(s).
Références
Ryt-Hansen, P. et al. Global phylogenetic analysis of contemporary aleutian mink disease viruses (AMDVs). Virol. J. 14, 1–6 (2017).
doi: 10.1186/s12985-017-0898-y
Best, S. M. & Bloom, M. E. Pathogenesis of Aleutian mink disease parvovirus and similarities to B19 infection. J. Vet. Med. Ser. B 52, 331–334 (2005).
doi: 10.1111/j.1439-0450.2005.00864.x
Porter, D. D., Larsen, A. E. & Porter, H. G. Aleutian disease of mink. Adv. Immunol. 29, 261–286 (1980).
pubmed: 6251709
doi: 10.1016/S0065-2776(08)60046-2
Alexandersen, S. et al. Acute interstitial pneumonia in mink kits inoculated with defined isolates of Aleutian mink disease parvovirus. Vet. Pathol. 31, 216–228 (1994).
pubmed: 8203085
doi: 10.1177/030098589403100209
Nituch, L. A., Bowman, J., Wilson, P. & Schulte-Hostedde, A. I. Molecular epidemiology of Aleutian disease virus in free-ranging domestic, hybrid, and wild mink. Evol. Appl. 5, 330–340 (2012).
pubmed: 25568054
pmcid: 3353359
doi: 10.1111/j.1752-4571.2011.00224.x
Knuuttila, A., Uzcátegui, N., Kankkonen, J., Vapalahti, O. & Kinnunen, P. Molecular epidemiology of Aleutian mink disease virus in Finland. Vet. Microbiol. 133, 229–238 (2009).
pubmed: 18799272
doi: 10.1016/j.vetmic.2008.07.003
Canuti, M., Whitney, H. G. & Lang, A. S. Amdoparvoviruses in small mammals: Expanding our understanding of parvovirus diversity, distribution, and pathology. Front. Microbiol. 6, 1–9 (2015).
doi: 10.3389/fmicb.2015.01119
Kanno, H., Wolfinbarger, J. B. & Bloom, M. E. Aleutian mink disease parvovirus infection of mink macrophages and human macrophage cell line U937: Demonstration of antibody-dependent enhancement of infection. J. Virol. 67, 7017–7024 (1993).
pubmed: 8230426
pmcid: 238162
doi: 10.1128/jvi.67.12.7017-7024.1993
Canuti, M. et al. Driving forces behind the evolution of the Aleutian mink disease parvovirus in the context of intensive farming. Virus Evol. 2, 1–17 (2016).
doi: 10.1093/ve/vew004
Olofsson, A. et al. Unusual, high genetic diversity of Aleutian mink disease virus. J. Clin. Microbiol. 37, 4145–4149 (1999).
pubmed: 10565948
pmcid: 85904
doi: 10.1128/JCM.37.12.4145-4149.1999
Leimann, A., Knuuttila, A., Maran, T., Vapalahti, O. & Saarma, U. Molecular epidemiology of Aleutian mink disease virus (AMDV) in Estonia, and a global phylogeny of AMDV. Virus Res. 199, 56–61 (2015).
pubmed: 25616049
doi: 10.1016/j.virusres.2015.01.011
Ryt-Hansen, P. et al. Outbreak tracking of Aleutian mink disease virus (AMDV) using partial NS1 gene sequencing. Virol. J. 14, 119 (2017).
pubmed: 28637462
pmcid: 5480136
doi: 10.1186/s12985-017-0786-5
Christensen, L. S., Gram-Hansen, L., Chriél, M. & Jensen, T. H. Diversity and stability of Aleutian mink disease virus during bottleneck transitions resulting from eradication in domestic mink in Denmark. Vet. Microbiol. 149, 64–71 (2011).
pubmed: 21112164
doi: 10.1016/j.vetmic.2010.10.016
Cho, H. J. & Greenfield, J. Eradication of Aleutian disease of mink by eliminating positive counterimmunoelectrophoresis test reactors. J. Clin. Microbiol. 7, 18–22 (1978).
pubmed: 203601
pmcid: 274849
doi: 10.1128/jcm.7.1.18-22.1978
Prieto, A. et al. Molecular epidemiology of Aleutian mink disease virus causing outbreaks in mink farms from Southwestern Europe: A retrospective study from 2012 to 2019. J. Vet. Sci. 21, 1–13 (2020).
doi: 10.4142/jvs.2020.21.e65
Hagberg, E. E., Pedersen, A. G., Larsen, L. E. & Krarup, A. Evolutionary analysis of whole-genome sequences confirms inter-farm transmission of Aleutian mink disease virus. J. Gen. Virol. 98, 1360–1371 (2017).
pubmed: 28612703
doi: 10.1099/jgv.0.000777
Farid, A. H. Aleutian mink disease virus in furbearing mammals in Nova Scotia, Canada. Acta Vet. Scand. 55, 10 (2013).
pubmed: 23394546
pmcid: 3602201
doi: 10.1186/1751-0147-55-10
Duffy, S., Shackelton, L. A. & Holmes, E. C. Rates of evolutionary change in viruses: Patterns and determinants. Nat. Rev. Genet. 9, 267–276 (2008).
pubmed: 18319742
doi: 10.1038/nrg2323
Tucciarone, C. M. et al. Molecular insight into Italian canine parvovirus heterogeneity and comparison with the worldwide scenario. Infect. Genet. Evol. 66, 171–179 (2018).
pubmed: 30257188
doi: 10.1016/j.meegid.2018.09.021
Franzo, G., Tucciarone, C. M., Cecchinato, M. & Drigo, M. Canine parvovirus type 2 (CPV-2) and Feline panleukopenia virus (FPV) codon bias analysis reveals a progressive adaptation to the new niche after the host jump. Mol. Phylogenet. Evol. 114, 82–92 (2017).
pubmed: 28603036
doi: 10.1016/j.ympev.2017.05.019
Gottschalck, E., Alexandersen, S., Storgaard, T., Bloom, M. E. & Aasted, B. Sequence comparison of the non-structural genes of four different types of Aleutian mink disease parvovirus indicates an unusual degree of variability. Adv. Virol. 138, 213–231 (1994).
Kosakovsky Pond, S. L., Poon, A. F. Y., Leigh Brown, A. J. & Frost, S. D. W. A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza a virus. Mol. Biol. Evol. 25, 1809–1824 (2008).
pubmed: 18511426
pmcid: 2515872
doi: 10.1093/molbev/msn123
Bonesi, L. & Palazon, S. The American mink in Europe: Status, impacts, and control. Biol. Conserv. 134, 470–483 (2007).
doi: 10.1016/j.biocon.2006.09.006
Wildhagen, A. Present distribution of North American mink in Norway. J. Mammal. 37, 116 (1956).
doi: 10.2307/1375544
Gerell, R. Dispersal and acclimatization of the mink (Mustela vison Schreb.) in Sweden. (1967).
Prieto, A. et al. Distribution of Aleutian mink disease virus contamination in the environment of infected mink farms. Vet. Microbiol. 204, 59–63 (2017).
pubmed: 28532807
doi: 10.1016/j.vetmic.2017.04.013
Mañas, S. et al. Aleutian mink disease parvovirus in wild riparian carnivores in Spain. J. Wildl. Dis. 37, 138–144 (2001).
pubmed: 11272488
doi: 10.7589/0090-3558-37.1.138
Nelson, M. I. et al. Global migration of influenza A viruses in swine. Nat. Commun. 6, 6696 (2015).
pubmed: 25813399
doi: 10.1038/ncomms7696
Leng, X. et al. Genetic diversity and phylogenetic analysis of Aleutian mink disease virus isolates in north-east China. Adv. Virol. 163, 1241–1251 (2018).
Franzo, G. et al. Free to circulate: An update on the epidemiological dynamics of porcine circovirus 2 (PCV-2) in Italy reveals the role of local spreading, wild populations, and Foreign countries. Pathogens 9, 221 (2020).
pmcid: 7157736
doi: 10.3390/pathogens9030221
Franzo, G. et al. 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 12, e0184401 (2017).
pubmed: 28880958
pmcid: 5589226
doi: 10.1371/journal.pone.0184401
Franzo, G., Cortey, M., Segalés, J., Hughes, J. & Drigo, M. Phylodynamic analysis of porcine circovirus type 2 reveals global waves of emerging genotypes and the circulation of recombinant forms. Mol. Phylogenet. Evol. 100, 269–280 (2016).
pubmed: 27114187
doi: 10.1016/j.ympev.2016.04.028
Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, 1–5 (2015).
doi: 10.1093/ve/vev003
Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D. W. GARD: A genetic algorithm for recombination detection. Bioinformatics 22, 3096–3098 (2006).
pubmed: 17110367
doi: 10.1093/bioinformatics/btl474
Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, W232–W235 (2016).
pubmed: 27084950
pmcid: 4987875
doi: 10.1093/nar/gkw256
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. 2, vew007 (2016).
pubmed: 27774300
pmcid: 4989882
doi: 10.1093/ve/vew007
Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).
pubmed: 17996036
pmcid: 2247476
doi: 10.1186/1471-2148-7-214
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. JModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).
pubmed: 22847109
pmcid: 4594756
doi: 10.1038/nmeth.2109
Drummond, A. J., Ho, S. Y. W. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
pubmed: 16683862
pmcid: 1395354
doi: 10.1371/journal.pbio.0040088
Baele, G. et al. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29, 2157–2167 (2012).
pubmed: 22403239
pmcid: 3424409
doi: 10.1093/molbev/mss084
Gill, M. S. et al. Improving Bayesian population dynamics inference: A coalescent-based model for multiple loci. Mol. Biol. Evol. 30, 713–724 (2013).
pubmed: 23180580
doi: 10.1093/molbev/mss265
Lemey, P., Rambaut, A., Drummond, A. J. & Suchard, M. A. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520 (2009).
pubmed: 19779555
pmcid: 2740835
doi: 10.1371/journal.pcbi.1000520
Bielejec, F. et al. Sprea D3: Interactive visualization of spatiotemporal history and trait evolutionary processes. Mol. Biol. Evol. 33, 2167–2169 (2016).
pubmed: 27189542
pmcid: 6398721
doi: 10.1093/molbev/msw082
Vaughan, T. G., Kühnert, D., Popinga, A., Welch, D. & Drummond, A. J. Efficient Bayesian inference under the structured coalescent. Bioinformatics 30, 2272–2279 (2014).
pubmed: 24753484
pmcid: 4207426
doi: 10.1093/bioinformatics/btu201
De Maio, N., Wu, C.-H., O’Reilly, K. M. & Wilson, D. New routes to phylogeography: A Bayesian structured coalescent approximation. PLoS Genet. 11, e1005421 (2015).
pubmed: 26267488
pmcid: 4534465
doi: 10.1371/journal.pgen.1005421
Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).
pubmed: 30958812
pmcid: 6472827
doi: 10.1371/journal.pcbi.1006650
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. 22, 1208–1222 (2005).
pubmed: 15703242
doi: 10.1093/molbev/msi105
Murrell, B. et al. FUBAR: A fast, unconstrained bayesian AppRoximation for inferring selection. Mol. Biol. Evol. 30, 1196–1205 (2013).
pubmed: 23420840
pmcid: 3670733
doi: 10.1093/molbev/mst030
Murrell, B. et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8, e1002764 (2012).
pubmed: 22807683
pmcid: 3395634
doi: 10.1371/journal.pgen.1002764
Kosakovsky Pond, S. L., Frost, S. D. W. & Muse, S. V. HyPhy: Hypothesis testing using phylogenies. Bioinformatics 21, 676–679 (2005).
doi: 10.1093/bioinformatics/bti079
Murrell, B., de Oliveira, T., Seebregts, C., Kosakovsky Pond, S. L. & Scheffler, K. Modeling HIV-1 drug resistance as episodic directional selection. PLoS Comput. Biol. 8, e1002507 (2012).
pubmed: 22589711
pmcid: 3349733
doi: 10.1371/journal.pcbi.1002507
Kelley, L. A. & Sternberg, M. J. E. Protein structure prediction on the web: A case study using the phyre server. Nat. Protoc. 4, 363–373 (2009).
pubmed: 19247286
doi: 10.1038/nprot.2009.2
Pettersen, E. F. et al. UCSF Chimera—A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Ginestet, C. ggplot2: Elegant graphics for data analysis. J. R. Stat. Soc. A. Stat. Soc. 174, 245–246 (2011).
doi: 10.1111/j.1467-985X.2010.00676_9.x