Pervasive within-host recombination and epistasis as major determinants of the molecular evolution of the foot-and-mouth disease virus capsid

English version

Autoři: Luca Ferretti ^aff001; Eva Pérez-Martín ^aff001; Fuquan Zhang ^aff001; François Maree ^aff003; Lin-Mari de Klerk-Lorist ^aff003; Louis van Schalkwykc ^aff003; Nicholas D. Juleff ^aff001; Bryan Charleston ^aff001; Paolo Ribeca ^aff001
Působiště autorů: The Pirbright Institute, Woking, Surrey, United Kingdom ^aff001; Current address: Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom ^aff002; South Africa Department of Microbiology and Plant Pathology, University of Pretoria, Pretoria, South Africa ^aff003; Onderstepoort Veterinary Institute-Transboundary Animal Diseases Programme (OVI-TADP), Onderstepoort, Gauteng, South Africa ^aff004
Vyšlo v časopise: Pervasive within-host recombination and epistasis as major determinants of the molecular evolution of the foot-and-mouth disease virus capsid. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008235
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008235

Souhrn

Although recombination is known to occur in foot-and-mouth disease virus (FMDV), it is considered only a minor determinant of virus sequence diversity. Analysis at phylogenetic scales shows inter-serotypic recombination events are rare, whereby recombination occurs almost exclusively in non-structural proteins. In this study we have estimated recombination rates within a natural host in an experimental setting. African buffaloes were inoculated with a SAT-1 FMDV strain containing two major viral sub-populations differing in their capsid sequence. This population structure enabled the detection of extensive within-host recombination in the genomic region coding for structural proteins and allowed recombination rates between the two sub-populations to be estimated. Quite surprisingly, the effective recombination rate in VP1 during the acute infection phase turns out to be about 0.1 per base per year, i.e. comparable to the mutation/substitution rate. Using a high-resolution map of effective within-host recombination in the capsid-coding region, we identified a linkage disequilibrium pattern in VP1 that is consistent with a mosaic structure with two main genetic blocks. Positive epistatic interactions between co-evolved variants appear to be present both within and between blocks. These interactions are due to intra-host selection both at the RNA and protein level. Overall our findings show that during FMDV co-infections by closely related strains, capsid-coding genes recombine within the host at a much higher rate than expected, despite the presence of strong constraints dictated by the capsid structure. Although these intra-host results are not immediately translatable to a phylogenetic setting, recombination and epistasis must play a major and so far underappreciated role in the molecular evolution of the virus at all scales.

Klíčová slova:

Alleles – DNA recombination – Epistasis – Foot and mouth disease – Linkage disequilibrium – Recombinant proteins – Viral packaging – Buffaloes

Zdroje

1. Alexandersen S, Zhang Z, Donaldson A, Garland A. The pathogenesis and diagnosis of foot-and-mouth disease. Journal of comparative pathology. 2003;129(1):1–36. doi: 10.1016/s0021-9975(03)00041-0 12859905

2. Maree F, de Klerk-Lorist LM, Gubbins S, Zhang F, Seago J, Pérez-Martín E, et al. Differential persistence of foot-and-mouth disease virus in African buffalo is related to virus virulence. Journal of virology. 2016;90(10):5132–5140. doi: 10.1128/JVI.00166-16 26962214

3. Mason PW, Grubman MJ, Baxt B. Molecular basis of pathogenesis of FMDV. Virus research. 2003;91(1):9–32. doi: 10.1016/s0168-1702(02)00257-5 12527435

4. Belsham GJ, Charleston B, Jackson T, Paton DJ. Foot-and-Mouth Disease. eLS. 2009;.

5. Domingo E, Holland J. RNA virus mutations and fitness for survival. Annual Reviews in Microbiology. 1997;51(1):151–178. doi: 10.1146/annurev.micro.51.1.151

6. Knowles N, Samuel A. Molecular epidemiology of foot-and-mouth disease virus. Virus research. 2003;91(1):65–80. doi: 10.1016/s0168-1702(02)00260-5 12527438

7. Paton DJ, Sumption KJ, Charleston B. Options for control of foot-and-mouth disease: knowledge, capability and policy. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364(1530):2657–2667. doi: 10.1098/rstb.2009.0100

8. Gebauer F, De La Torre J, Gomes I, Mateu M, Barahona H, Tiraboschi B, et al. Rapid selection of genetic and antigenic variants of foot-and-mouth disease virus during persistence in cattle. Journal of virology. 1988;62(6):2041–2049. 2835508

9. Lauring AS, Andino R. Quasispecies theory and the behavior of RNA viruses. PLoS pathogens. 2010;6(7):e1001005. doi: 10.1371/journal.ppat.1001005 20661479

10. Domingo E, Sheldon J, Perales C. Viral quasispecies evolution. Microbiology and Molecular Biology Reviews. 2012;76(2):159–216. doi: 10.1128/MMBR.05023-11 22688811

11. King AM. Genetic recombination in positive strand RNA viruses. In: RNA Genetics, Volume II, Retroviruses, viroids, and RNA recombination. CRC Press Albany, NY; 1988. p. 149–165.

12. Carrillo C, Tulman E, Delhon G, Lu Z, Carreno A, Vagnozzi A, et al. Comparative genomics of foot-and-mouth disease virus. Journal of virology. 2005;79(10):6487–6504. doi: 10.1128/JVI.79.10.6487-6504.2005 15858032

13. Lewis-Rogers N, McClellan DA, Crandall KA. The evolution of foot-and-mouth disease virus: impacts of recombination and selection. Infection, Genetics and Evolution. 2008;8(6):786–798. doi: 10.1016/j.meegid.2008.07.009 18718559

14. McCahon D, Slade W, Priston R, Lake J. An extended genetic recombination map for foot-and-mouth disease virus. Journal of General Virology. 1977;35(3):555–565. doi: 10.1099/0022-1317-35-3-555 196035

15. King A, Slade W, Newman J, McCahon D. Temperature-sensitive mutants of foot-and-mouth disease virus with altered structural polypeptides. II. Comparison of recombination and biochemical maps. Journal of virology. 1980;34(1):67–72. 6246263

16. Tosh C, Hemadri D, Sanyal A. Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. Journal of general virology. 2002;83(10):2455–2460. doi: 10.1099/0022-1317-83-10-2455 12237427

17. Tosh C, Sanyal A, Hemadri D. Genetic and antigenic analysis of a recombinant foot-and-mouth disease virus. Current Science. 2002; p. 1016–1019.

18. Heath L, Van Der Walt E, Varsani A, Martin DP. Recombination patterns in aphthoviruses mirror those found in other picornaviruses. Journal of Virology. 2006;80(23):11827–11832. doi: 10.1128/JVI.01100-06 16971423

19. Jackson A, O’neill H, Maree F, Blignaut B, Carrillo C, Rodriguez L, et al. Mosaic structure of foot-and-mouth disease virus genomes. Journal of General Virology. 2007;88(2):487–492. doi: 10.1099/vir.0.82555-0 17251567

20. Worobey M, Holmes EC. Evolutionary aspects of recombination in RNA viruses. Journal of General Virology. 1999;80(10):2535–2543. doi: 10.1099/0022-1317-80-10-2535 10573145

21. Shriner D, Rodrigo AG, Nickle DC, Mullins JI. Pervasive genomic recombination of HIV-1 in vivo. Genetics. 2004;167(4):1573–1583. doi: 10.1534/genetics.103.023382 15342499

22. Froissart R, Roze D, Uzest M, Galibert L, Blanc S, Michalakis Y. Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS biology. 2005;3(3):e89. doi: 10.1371/journal.pbio.0030089 15737066

23. Neher RA, Leitner T. Recombination rate and selection strength in HIV intra-patient evolution. PLoS computational biology. 2010;6(1):e1000660. doi: 10.1371/journal.pcbi.1000660 20126527

24. Batorsky R, Kearney MF, Palmer SE, Maldarelli F, Rouzine IM, Coffin JM. Estimate of effective recombination rate and average selection coefficient for HIV in chronic infection. Proceedings of the National Academy of Sciences. 2011;108(14):5661–5666. doi: 10.1073/pnas.1102036108

25. Paton DJ, Gubbins S, King DP. Understanding the transmission of foot-and-mouth disease virus at different scales. Current opinion in virology. 2018;28 : 85–91. doi: 10.1016/j.coviro.2017.11.013 29245054

26. Cortey M, Ferretti L, Pérez-Martín E, Zhang F, de Klerk-Lorist LM, Scott K, et al. Persistent infection of African buffalo (Syncerus caffer) with Foot-and-Mouth Disease Virus: limited viral evolution and no evidence of antibody neutralization escape. Journal of Virology. 2019; doi: 10.1128/JVI.00563-19 31092573

27. Hartl DL, Clark AG, Clark AG. Principles of population genetics. vol. 116. Sinauer associates Sunderland; 1997.

28. Franklin I, Lewontin R. Is the gene the unit of selection? Genetics. 1970;65(4):707–734. 5518513

29. Cottam EM, Haydon DT, Paton DJ, Gloster J, Wilesmith JW, Ferris NP, et al. Molecular epidemiology of the foot-and-mouth disease virus outbreak in the United Kingdom in 2001. Journal of Virology. 2006;80(22):11274–11282. doi: 10.1128/JVI.01236-06 16971422

30. Wright CF, Knowles NJ, Di Nardo A, Paton DJ, Haydon DT, King DP. Reconstructing the origin and transmission dynamics of the 1967–68 foot-and-mouth disease epidemic in the United Kingdom. Infection, Genetics and Evolution. 2013;20 : 230–238. doi: 10.1016/j.meegid.2013.09.009 24035793

31. Runckel C, Westesson O, Andino R, DeRisi JL. Identification and manipulation of the molecular determinants influencing poliovirus recombination. PLoS pathogens. 2013;9(2):e1003164. doi: 10.1371/journal.ppat.1003164 23408891

32. Neher RA, Shraiman BI. Competition between recombination and epistasis can cause a transition from allele to genotype selection. Proceedings of the National Academy of Sciences. 2009;106(16):6866–6871. doi: 10.1073/pnas.0812560106

33. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T. Identification of direct residue contacts in protein–protein interaction by message passing. Proceedings of the National Academy of Sciences. 2009;106(1):67–72. doi: 10.1073/pnas.0805923106

34. Baldassi C, Zamparo M, Feinauer C, Procaccini A, Zecchina R, Weigt M, et al. Fast and accurate multivariate Gaussian modeling of protein families: predicting residue contacts and protein-interaction partners. PloS one. 2014;9(3):e92721. doi: 10.1371/journal.pone.0092721 24663061

35. Xiao Y, Dolan PT, Goldstein EF, Li M, Farkov M, Brodsky L, et al. Poliovirus intrahost evolution is required to overcome tissue-specific innate immune responses. Nature communications. 2017;8(1):375. doi: 10.1038/s41467-017-00354-5 28851882

36. Charpentier C, Nora T, Tenaillon O, Clavel F, Hance AJ. Extensive recombination among human immunodeficiency virus type 1 quasispecies makes an important contribution to viral diversity in individual patients. Journal of virology. 2006;80(5):2472–2482. doi: 10.1128/JVI.80.5.2472-2482.2006 16474154

37. Simon-Loriere E, Holmes EC. Why do RNA viruses recombine? Nature Reviews Microbiology. 2011;9(8):617. doi: 10.1038/nrmicro2614 21725337

38. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of computational biology. 2012;19(5):455–477. doi: 10.1089/cmb.2012.0021 22506599

39. Marco-Sola S, Sammeth M, Guigó R, Ribeca P. The GEM mapper: fast, accurate and versatile alignment by filtration. Nature methods. 2012;9(12):1185. doi: 10.1038/nmeth.2221 23103880

40. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular systems biology. 2011;7(1):539. doi: 10.1038/msb.2011.75 21988835

41. Raineri E, Ferretti L, Esteve-Codina A, Nevado B, Heath S, Pérez-Enciso M. SNP calling by sequencing pooled samples. BMC bioinformatics. 2012;13(1):239. doi: 10.1186/1471-2105-13-239 22992255