Zika virus evolution and spread in the Americas

Nature

Volumn 546, Issue 7658, 2017, Pages 411-415

  Metsky, Hayden C ^a,b   Matranga, Christian B ^a   Wohl, Shirlee ^a,c   Schaffner, Stephen F ^a,c,d   Freije, Catherine A ^a,c   Winnicki, Sarah M ^a   West, Kendra ^a   Qu, James ^a   Baniecki, Mary Lynn ^a   Gladden Young, Adrianne ^a   Lin, Aaron E ^a,c   Tomkins Tinch, Christopher H ^a   Ye, Simon H ^a,e   Park, Daniel J ^a   Luo, Cynthia Y ^a,c   Barnes, Kayla G ^a,c,d   Shah, Rickey R ^a,c   Chak, Bridget ^a,c   Barbosa Lima, Giselle ^f   Delatorre, Edson ^g   Vieira, Yasmine R ^f   Paul, Lauren M ^h   Tan, Amanda L ^h   Barcellona, Carolyn M ^h   Porcelli, Mario C ⁱ   Vasquez, Chalmers ⁱ   Cannons, Andrew C ^j   Cone, Marshall R ^j   Hogan, Kelly N ^j   Kopp, Edgar W ^j   Anzinger, Joshua J ^k   Garcia, Kimberly F ^l   Parham, Leda A ^l   Ramírez, Rosa M Gélvez ^m   Montoya, Maria C Miranda ^m   Rojas, Diana P ⁿ   Brown, Catherine M ^o   Hennigan, Scott ^o   Sabina, Brandon ^o   Scotland, Sarah ^o   Gangavarapu, Karthik ^p   Grubaugh, Nathan D ^p   Oliveira, Glenn ^q   Robles Sikisaka, Refugio ^p   Rambaut, Andrew ^r,s   Gehrke, Lee ^t,u   Smole, Sandra ^o   Halloran, M Elizabeth ^v,w   Villar, Luis ^m   Mattar, Salim ^x   Lorenzana, Ivette ^l   Cerbino Neto, Jose ^d   Valim, Clarissa ^d,y   Degrave, Wim ^g   Bozza, Patricia T ^g   Gnirke, Andreas ^a   Andersen, Kristian G ^p,q   Isern, Sharon ^h   Michael, Scott F ^h   Bozza, Fernando A ^f,z   Souza, Thiago M L ^g   Bosch, Irene ^t   Yozwiak, Nathan L ^a,c   Macinnis, Bronwyn L ^a,d   Sabeti, Pardis C ^a,c,d,aa   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b USA   (United States)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f Funda??o Oswaldo Cruz   (Brazil)

^g INSTITUTO OSWALDO CRUZ   (Brazil)

^h FLORIDA GULF COAST UNIVERSITY   (United States)

ⁱ Miami Dade County   (United States)

^j FLORIDA DEPARTMENT OF HEALTH   (United States)

^k UNIVERSITY OF THE WEST INDIES   (Jamaica)

^l NATIONAL AUTONOMOUS UNIVERSITY OF HONDURAS   (Honduras)

^m UNIVERSIDAD INDUSTRIAL DE SANTANDER   (Colombia)

ⁿ UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^o MASSACHUSETTS DEPARTMENT OF PUBLIC HEALTH   (United States)

^p SCRIPPS RESEARCH INSTITUTE   (United States)

^q SCRIPPS TRANSLATIONAL SCIENCE INSTITUTE   (United States)

^r UNIVERSITY OF EDINBURGH   (United Kingdom)

^s NATIONAL INSTITUTES OF HEALTH   (United States)

^t Massachusetts Institute of Technology Cambridge   (United States)

^u HARVARD MEDICAL SCHOOL   (United States)

^v Fred Hutchinson Cancer Research Center   (United States)

^w UNIVERSITY OF WASHINGTON   (United States)

^x UNIVERSIDAD DE CÓRDOBA   (Colombia)

^y MICHIGAN STATE UNIVERSITY   (United States)

^z D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

^aa HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOGRAPHY; DISEASE SPREAD; EPIDEMIC; EVOLUTIONARY BIOLOGY; GENOME; GENOMICS; MOSQUITO; PHYLOGENETICS; POPULATION OUTBREAK; VIRUS;

ARTICLE; CONTROLLED STUDY; EPIDEMIC; EVOLUTION; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; GENETIC VARIATION; GEOGRAPHIC DISTRIBUTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; ZIKA FEVER; ZIKA VIRUS; ANIMAL; BRAZIL; CLASSIFICATION; COLOMBIA; GENETICS; GEOGRAPHIC MAPPING; HEALTH SURVEY; HONDURAS; HUMAN; ISOLATION AND PURIFICATION; METAGENOME; MOLECULAR EPIDEMIOLOGY; MOSQUITO; MOSQUITO VECTOR; MUTATION; PATHOGENICITY; PHYLOGENY; PUERTO RICO; STATISTICS AND NUMERICAL DATA; TRANSMISSION; UNITED STATES; VIROLOGY; VIRUS GENOME; ZIKA VIRUS INFECTION;

CARIBBEAN ISLANDS; COLOMBIA; HONDURAS; NORTH AMERICA; PUERTO RICO; SOUTH AMERICA; UNITED STATES;

ZIKA VIRUS;

ANIMALS; BRAZIL; COLOMBIA; CULICIDAE; DISEASE OUTBREAKS; GENOME, VIRAL; GEOGRAPHIC MAPPING; HONDURAS; HUMANS; METAGENOME; MOLECULAR EPIDEMIOLOGY; MOSQUITO VECTORS; MUTATION; PHYLOGENY; PUBLIC HEALTH SURVEILLANCE; PUERTO RICO; UNITED STATES; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85019697447     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22402     Document Type: Article

References (68)

1. World Health Organization. Zika situation report: Zika virus, Microcephaly and Guillain-Barré syndrome. http://who.int/emergencies/zika-virus/situationreport/2-february-2017/en/(2017).
2. Reynolds, M. R. et al. Vital signs: update on Zika virus-associated birth defects and evaluation of all U.S. infants with congenital Zika virus exposure-U.S. Zika pregnancy registry, 2016. MMWR Morb. Mortal. Wkly. Rep. 66, 366-373 (2017).
3. de Vigilância em Saúde, S. Protocolo de Vigilância e Resposta à Ocorrência de Microcefalia (Ministério da Saúde Brasília, 2016).
4. Schieffelin, J. S. et al. Clinical illness and outcomes in patients with Ebola in Sierra Leone. N. Engl. J. Med. 371, 2092-2100 (2014).
5. Sardi, S. I. et al. Coinfections of Zika and chikungunya viruses in Bahia, Brazil, identified by metagenomic next-generation sequencing. J. Clin. Microbiol. 54, 2348-2353 (2016).
6. Martina, B. E. E., Koraka, P. & Osterhaus, A. D. M. E. Dengue virus pathogenesis: an integrated view. Clin. Microbiol. Rev. 22, 564-581 (2009).
7. Fauci, A. S. & Morens, D. M. Zika virus in the Americas-yet another Arbovirus threat. N. Engl. J. Med. 374, 601-604 (2016).
8. Quick, J. et al. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples. Nat. Protocols http://dx.doi.org/10.1038/nprot.2017.066 (2017).
9. Matranga, C. B. et al. Enhanced methods for unbiased deep sequencing of Lassa and Ebola RNA viruses from clinical and biological samples. Genome Biol. 15, 519 (2014).
10. Faria, N. R. et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature http://dx.doi.org/10.1038/nature22401 (2017).
11. Grubaugh, N. D. et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature http://dx.doi.org/10.1038/nature22400 (2017).
12. Faria, N. R. et al. Zika virus in the Americas: early epidemiological and genetic findings. Science 352, 345-349 (2016).
13. Sall, A. A. et al. Yellow fever virus exhibits slower evolutionary dynamics than dengue virus. J. Virol. 84, 765-772 (2010).
14. Centers for Disease Control and Prevention. First case of Zika virus reported in Puerto Rico. https://www.cdc.gov/media/releases/2015/s1231-zika.html (2015).
15. Pan American Health Organization. Zika: Epidemiological Report Honduras. http://www2.paho.org/hq/index.php?option=com-docman&task=doc-view&gid=35137&Itemid=270 (2017).
16. Pan American Health Organization. Epidemiological Update: Zika Virus Infection. http://www2.paho.org/hq/index.php?option=com-docman&task=doc-view&gid=32021&Itemid=270 (2015).
17. Pan American Health Organization. Zika: Epidemiological Report Dominican Republic. http://www2.paho.org/hq/index.php?option=com-ocman&task=doc-iew&gid=35103&Itemid=270 (2017).
18. Nunes, M. R. T. et al. Emergence and potential for spread of chikungunya virus in Brazil. BMC Med. 13, 102 (2015).
19. Tsetsarkin, K. A., Vanlandingham, D. L., McGee, C. E. & Higgs, S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3, e201 (2007).
20. Piantadosi, A. et al. HIV-1 evolution in gag and env is highly correlated but exhibits different relationships with viral load and the immune response. AIDS 23, 579-587 (2009).
21. Villabona-Arenas, C. J. et al. Dengue virus type 3 adaptive changes during epidemics in São Jose de Rio Preto, Brazil, 2006-2007. PLoS One 8, e63496 (2013).
22. Brinton, M. A. & Basu, M. Functions of the 3′ and 5′ genome RNA regions of members of the genus Flavivirus. Virus Res. 206, 108-119 (2015).
23. Duchêne, S., Ho, S. Y. W. & Holmes, E. C. Declining transition/transversion ratios through time reveal limitations to the accuracy of nucleotide substitution models. BMC Evol. Biol. 15, 36 (2015).
24. Corman, V. M. et al. Clinical comparison, standardization and optimization of Zika virus molecular detection. Bull. World Health Organ. (2016).
25. Gire, S. K. et al. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345, 1369-1372 (2014).
26. Pyke, A. T. et al. Imported zika virus infection from the Cook islands into Australia, 2014. PLoS Curr. http://dx.doi.org/10.1371/currents. outbreaks.4635a54dbffba2156fb2fd76dc49f65e (2014).
27. Lanciotti, R. S. et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 14, 1232-1239 (2008).
28. Faye, O. et al. One-step RT-PCR for detection of Zika virus. J. Clin. Virol. 43, 96-101 (2008).
29. Faye, O. et al. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virol. J. 10, 311 (2013).
30. Balm, M. N. D. et al. A diagnostic polymerase chain reaction assay for Zika virus. J. Med. Virol. 84, 1501-1505 (2012).
31. Tappe, D. et al. First case of laboratory-confirmed Zika virus infection imported into Europe, November 2013. Euro Surveill. 19, 20685 (2014).
32. U.S. Food and Drug Administration. Zika virus response updates from FDA. https://www.fda.gov/EmergencyPreparedness/Counterterrorism/MedicalCountermeasures/MCMIssues/ucm485199.htm#eua (2017).
33. Morlan, J. D., Qu, K. & Sinicropi, D. V. Selective depletion of rRNA enables whole transcriptome profiling of archival fixed tissue. PLoS One 7, e42882 (2012).
34. Worobey, M. et al. 1970s and 'Patient 0' HIV-1 genomes illuminate early HIV/AIDS history in North America. Nature 539, 98-101 (2016).
35. Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 44, D67-D72 (2016).
36. Park, D. J. et al. Ebola virus epidemiology, transmission, and evolution during seven months in Sierra Leone. Cell 161, 1516-1526 (2015).
37. Tomkins-Tinch, C. et al. Broad Institute viral-ngs: v1.13.3. https://github.com/broadinstitute/viral-ngs/releases/tag/v1.13.3 (2016).
38. Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).
39. O'Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733-D745 (2016).
40. Aurrecoechea, C. et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37, D539-D543 (2009).
41. Yarza, P. et al. The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst. Appl. Microbiol. 31, 241-250 (2008).
42. Brister, J. R., Ako-Adjei, D., Bao, Y. & Blinkova, O. NCBI viral genomes resource. Nucleic Acids Res. 43, D571-D577 (2015).
43. NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 44, D7-D19 (2016).
44. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652 (2011).
45. Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152 (2012).
46. Hyatt, D., LoCascio, P. F., Hauser, L. J. & Uberbacher, E. C. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28, 2223-2230 (2012).
47. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016).
48. Cribari-Neto, F. & Zeileis, A. Beta regression in R. J. Stat. Softw. 34, 1-24 (2010).
49. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
50. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
51. Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649 (2012).
52. Henikoff, S. & Henikoff, J. G. Amino acid substitution matrices from protein blocks. Proc. Natl Acad. Sci. USA 89, 10915-10919 (1992).
53. Guindon, S. et al. New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).
54. Rambaut, A. FigTree. Version 1.4.2 (Inst. Evol. Biol., Univ. Edinburgh, 2014).
55. 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).
56. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973 (2012).
57. Shapiro, B. et al. A Bayesian phylogenetic method to estimate unknown sequence ages. Mol. Biol. Evol. 28, 879-887 (2011).
58. Shapiro, B., Rambaut, A. & Drummond, A. J. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol. Biol. Evol. 23, 7-9 (2006).
59. Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185-1192 (2005).
60. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
61. Ferreira, M. A. R. & Suchard, M. A. Bayesian analysis of elapsed times in continuous-time Markov chains. Can. J. Stat. 36, 355-368 (2008).
62. 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).
63. Baele, G., Li, W. L. S., Drummond, A. J., Suchard, M. A. & Lemey, P. Accurate model selection of relaxed molecular clocks in bayesian phylogenetics. Mol. Biol. Evol. 30, 239-243 (2013).
64. Yang, Z. Maximum-likelihood models for combined analyses of multiple sequence data. J. Mol. Evol. 42, 587-596 (1996).
65. Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1-18 (2008).
66. Josse, J. & Husson, F. missMDA: a package for handling missing values in multivariate data analysis. J. Stat. Softw. 70, 1-31 (2016).
67. Gourinat, A.-C., O'Connor, O., Calvez, E., Goarant, C. & Dupont-Rouzeyrol, M. Detection of Zika virus in urine. Emerg. Infect. Dis. J. 21, 84 (2015).
68. Paz-Bailey, G. et al. Persistence of Zika virus in body fluids-preliminary report. N. Engl. J. Med. https://doi.org/10.1056/NEJMoa1613108 (2017).