Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague

PLoS Neglected Tropical Diseases

Volumn 11, Issue 9, 2017, Pages

  Vogler, Amy J ^a   Andrianaivoarimanana, Voahangy ^b   Telfer, Sandra ^c   Hall, Carina M ^a   Sahl, Jason W ^a   Hepp, Crystal M ^a   Centner, Heather ^a   Andersen, Genevieve ^a   Birdsell, Dawn N ^a   Rahalison, Lila ^b   Nottingham, Roxanne ^a   Keim, Paul ^a,d   Wagner, David M ^a   Rajerison, Minoarisoa ^b  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENETIC VARIABILITY; GENOTYPE; MADAGASCAR; NONHUMAN; PHYLOGENY; PHYLOGEOGRAPHY; PLAGUE; SEASONAL VARIATION; VIRUS TRANSMISSION; WHOLE GENOME SEQUENCING; YERSINIA PESTIS; BACTERIAL GENOME; CLASSIFICATION; DNA SEQUENCE; ENDEMIC DISEASE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SPATIOTEMPORAL ANALYSIS;

ENDEMIC DISEASES; GENOME, BACTERIAL; GENOTYPE; HUMANS; MADAGASCAR; PHYLOGEOGRAPHY; PLAGUE; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; SPATIO-TEMPORAL ANALYSIS; YERSINIA PESTIS;

EID: 85030428307     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0005887     Document Type: Article

References (55)

1. Rasmussen S, Allentoft ME, Nielsen K, Orlando L, Sikora M, Sjögren KG, et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell. 2015;163(3):571–82. doi: 10.1016/j.cell.2015.10.009 26496604;.
2. Perry RD, Fetherston JD, Yersinia pestis-etiologic agent of plague. Clinical microbiology reviews. 1997;10(1):35–66. Epub 1997/01/01. 8993858.
3. Cui Y, Yu C, Yan Y, Li D, Li Y, Jombart T, et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(2):577–82. Epub 2012/12/29. doi: 10.1073/pnas.1205750110 23271803;.
4. Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P, Wagner DM, et al. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat Genet. 2010;42(12):1140–3. Epub 2010/11/03. doi: 10.1038/ng.705 21037571.
5. Keim PS, Wagner DM, Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases. Nat Rev Microbiol. 2009;7(11):813–21. Epub 2009/10/13. doi: 10.1038/nrmicro2219 19820723.
6. Biggins DE, Kosoy MY, Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. J Mammal. 2001;82(4):906–16.
7. Cully JF, Jr.Williams ES, Interspecific comparisons of sylvatic plague in prairie dogs. J Mammal. 2001;82(4):894–905.
8. Andrianaivoarimanana V, Kreppel K, Elissa N, Duplantier JM, Carniel E, Rajerison M, et al. Understanding the persistence of plague foci in Madagascar. PLoS neglected tropical diseases. 2013;7(11):e2382. doi: 10.1371/journal.pntd.0002382 24244760;.
9. Chanteau S, Ratsifasoamanana L, Rasoamanana B, Rahalison L, Randriambelosoa J, Roux J, et al. Plague, a reemerging disease in Madagascar. Emerg Infect Dis. 1998;4(1):101–4. Epub 1998/03/21. doi: 10.3201/eid0401.980114 9452403.
10. Duplantier JM, The black rat's role in spreading human plague in Madagascar. L'Institut de recherche pour le développement Scientific Bulletin. 2001;131:1–3.
11. Duplantier JM, Rakotondravony D, Singleton G, Hinds L, Leirs H, Zhang Z, The rodent problem in Madagascar: agricultural pest and threat to human health. In: Ecologically-based management of rodent pests. Canberra: Australian Centre for International Agricultural Research; 1999. p. 441–59.
12. Brygoo ER, Epidémiologie de la peste à Madagascar. Arch Inst Pasteur Madagascar. 1966;35:9–147.
13. Boisier P, Rahalison L, Rasolomaharo M, Ratsitorahina M, Mahafaly M, Razafimahefa M, et al. Epidemiologic features of four successive annual outbreaks of bubonic plague in Mahajanga, Madagascar. Emerg Infect Dis. 2002;8(3):311–6. Epub 2002/04/03. doi: 10.3201/eid0803.010250 11927030.
14. Boisier P, Rasolomaharo M, Ranaivoson G, Rasoamanana B, Rakoto L, Andrianirina Z, et al. Urban epidemic of bubonic plague in Majunga, Madagascar: epidemiological aspects. Trop Med Int Health. 1997;2(5):422–7. Epub 1997/05/01. 9217697.
15. Laventure S, Andrianaja V, Rasoamanana B, Epidémie de peste à Majunga en 1991. Rapport de mission de l’Institut Pasteur de Madagascar1991. 1991:1–26.
16. Rasolomaharo M, Rasoamanana B, Andrianirina Z, Buchy P, Rakotoarimanana N, Chanteau S, Plague in Majunga, Madagascar. Lancet. 1995;346(8984):1234. Epub 1995/11/04. 7475693.
17. Riehm JM, Projahn M, Vogler AJ, Rajerison M, Andersen G, Hall CM, et al. Diverse Genotypes of Yersinia pestis Caused Plague in Madagascar in 2007. PLoS neglected tropical diseases. 2015;9(6):e0003844. doi: 10.1371/journal.pntd.0003844 26069964;.
18. Vogler AJ, Chan F, Nottingham R, Andersen G, Drees K, Beckstrom-Sternberg SM, et al. A decade of plague in Mahajanga, Madagascar: insights into the global maritime spread of pandemic plague. mBio. 2013;4(1):e00623–12. Epub 2013/02/14. doi: 10.1128/mBio.00623-12 23404402;.
19. Vogler AJ, Chan F, Wagner DM, Roumagnac P, Lee J, Nera R, et al. Phylogeography and Molecular Epidemiology of Yersinia pestis in Madagascar. PLoS neglected tropical diseases. 2011;5(9):e1319. Epub 2011/09/21. doi: 10.1371/journal.pntd.0001319 21931876;.
20. Girard JM, Wagner DM, Vogler AJ, Keys C, Allender CJ, Drickamer LC, et al. Differential plague-transmission dynamics determine Yersinia pestis population genetic structure on local, regional, and global scales. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(22):8408–13. Epub 2004/06/03. doi: 10.1073/pnas.0401561101 15173603.
21. Pearson T, Okinaka RT, Foster JT, Keim P, Phylogenetic understanding of clonal populations in an era of whole genome sequencing. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2009;9(5):1010–9. Epub 2009/05/30. doi: 10.1016/j.meegid.2009.05.014 19477301.
22. Sahl JW, Gillece JD, Schupp JM, Waddell VG, Driebe EM, Engelthaler DM, et al. Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter. PLoS One. 2013;8(1):e54287. doi: 10.1371/journal.pone.0054287 23365658;.
23. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio.GN]; 2013.
24. Parkhill J, Wren BW, Thomson NR, Titball RW, Holden MT, Prentice MB, et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature. 2001;413(6855):523–7. Epub 2001/10/05. doi: 10.1038/35097083 11586360.
25. Wright MS, Haft DH, Harkins DM, Perez F, Hujer KM, Bajaksouzian S, et al. New insights into dissemination and variation of the health care-associated pathogen Acinetobacter baumannii from genomic analysis. mBio. 2014;5(1):e00963–13. doi: 10.1128/mBio.00963-13 24449752;.
26. Delcher AL, Salzberg SL, Phillippy AM, Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics. 2003;Chapter 10:Unit 10 3. doi: 10.1002/0471250953.bi1003s00 18428693.
27. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943;.
28. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43(5):491–8. doi: 10.1038/ng.806 21478889;.
29. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–303. doi: 10.1101/gr.107524.110 20644199;.
30. Sahl JW, Lemmer D, Travis J, Schupp J, Gillece J, Aziz M, et al. The Northern Arizona SNP Pipeline (NASP): accurate, flexible, and rapid identification of SNPs in WGS datasets. bioRxiv. 2016. doi: 10.1101/037267
31. Koressaar T, Remm M, Enhancements and modifications of primer design program Primer3. Bioinformatics. 2007;23(10):1289–91. doi: 10.1093/bioinformatics/btm091 17379693.
32. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic acids research. 2012;40(15):e115. doi: 10.1093/nar/gks596 22730293;.
33. Colman RE, Schupp JM, Hicks ND, Smith DE, Buchhagen JL, Valafar F, et al. Detection of Low-Level Mixed-Population Drug Resistance in Mycobacterium tuberculosis Using High Fidelity Amplicon Sequencing. PLoS One. 2015;10(5):e0126626. doi: 10.1371/journal.pone.0126626 25970423;.
34. Bowers JR, Lemmer D, Sahl JW, Pearson T, Driebe EM, Wojack B, et al. KlebSeq, a Diagnostic Tool for Surveillance, Detection, and Monitoring of Klebsiella pneumoniae. Journal of clinical microbiology. 2016;54(10):2582–96. doi: 10.1128/JCM.00927-16 27510832;.
35. Kumar S, Tamura K, Jakobsen IB, Nei M, MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001;17(12):1244–5. Epub 2001/12/26. 11751241.
36. Rambaut A, Lam TT, Max Carvalho L, Pybus OG, Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2(1):vew007. doi: 10.1093/ve/vew007 27774300;.
37. Drummond AJ, Suchard MA, Xie D, Rambaut A, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–73. doi: 10.1093/molbev/mss075 22367748;.
38. Akaike H, New Look at Statistical-Model Identification. Ieee T Automat Contr. 1974;Ac19(6):716–23. doi: 10.1109/Tac.1974.1100705
39. Burnham KP, Anderson DR, Multimodel inference—understanding AIC and BIC in model selection. Sociol Method Res. 2004;33(2):261–304. doi: 10.1177/0049124104268644
40. Gelman A, Meng XL, Simulating normalizing constants: From importance sampling to bridge sampling to path sampling. Stat Sci. 1998;13(2):163–85.
41. Xie WG, Lewis PO, Fan Y, Kuo L, Chen MH, Improving Marginal Likelihood Estimation for Bayesian Phylogenetic Model Selection. Syst Biol. 2011;60(2):150–60. doi: 10.1093/sysbio/syq085 21187451
42. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV, Improving the Accuracy of Demographic and Molecular Clock Model Comparison While Accommodating Phylogenetic Uncertainty. Molecular Biology and Evolution. 2012;29(9):2157–67. doi: 10.1093/molbev/mss084 22403239
43. Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P, Accurate Model Selection of Relaxed Molecular Clocks in Bayesian Phylogenetics. Molecular Biology and Evolution. 2013;30(2):239–43. doi: 10.1093/molbev/mss243 23090976
44. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A, Relaxed phylogenetics and dating with confidence. Plos Biol. 2006;4(5):699–710. doi: 10.1371/journal.pbio.0040088 16683862
45. Minin VN, Bloomquist EW, Suchard MA, Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Molecular Biology and Evolution. 2008;25(7):1459–71. doi: 10.1093/molbev/msn090 18408232
46. Rambaut A, Suchard MA, Xie D, Drummond AJ. Tracer v1.6 http://beast.bio.ed.ac.uk/Tracer. 2014.
47. FigTree http://tree.bio.ed.ac.uk/software/figtree.
48. Rahelinirina S, Duplantier JM, Ratovonjato J, Ramilijaona O, Ratsimba M, Rahalison L, Study on the movement of Rattus rattus and evaluation of the plague dispersion in Madagascar. Vector Borne Zoonotic Dis. 2010;10(1):77–84. Epub 2010/02/18. doi: 10.1089/vbz.2009.0019 20158335.
49. World Health Organization (WHO)Plague around the world, 2010–2015. Wkly Epidemiol Rec. 2016;91(8):89–93. Epub 2016/03/01. 26922822.
50. Chanteau S, Ratsitorahina M, Rahalison L, Rasoamanana B, Chan F, Boisier P, et al. Current epidemiology of human plague in Madagascar. Microbes and infection / Institut Pasteur. 2000;2(1):25–31. Epub 2000/03/16. 10717537.
51. Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, Ratsifasoamanana L, et al. Epidemiological trends for human plague in Madagascar during the second half of the 20th century: a survey of 20,900 notified cases. Trop Med Int Health. 2006;11(8):1228–37. Epub 2006/08/15. doi: 10.1111/j.1365-3156.2006.01677.x 16903886.
52. Eisen RJ, Griffith KS, Borchert JN, MacMillan K, Apangu T, Owor N, et al. Assessing human risk of exposure to plague bacteria in northwestern Uganda based on remotely sensed predictors. Am J Trop Med Hyg. 2010;82(5):904–11. doi: 10.4269/ajtmh.2010.09-0737 20439974;.
53. Duplantier JM, Duchemin JB, Chanteau S, Carniel E, From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res. 2005;36(3):437–53. Epub 2005/04/23. doi: 10.1051/vetres:2005007 15845233.
54. Rahalison L, Ranjalahy M, Duplantier JM, Duchemin JB, Ravelosaona J, Ratsifasoamanana L, et al. Susceptibility to plague of the rodents in Antananarivo, Madagascar. Adv Exp Med Biol. 2003;529:439–42. Epub 2003/05/22. doi: 10.1007/0-306-48416-1_87 12756805.
55. Brouat C, Rahelinirina S, Loiseau A, Rahalison L, Rajerison M, Laffly D, et al. Plague circulation and population genetics of the reservoir Rattus rattus: the influence of topographic relief on the distribution of the disease within the Madagascan focus. PLoS neglected tropical diseases. 2013;7(6):e2266. doi: 10.1371/journal.pntd.0002266 23755317;.