Culture-free genome-wide locus sequence typing (GLST) provides new perspectives on Trypanosoma cruzi dispersal and infection complexity


Autoři: Philipp Schwabl aff001;  Jalil Maiguashca Sánchez aff002;  Jaime A. Costales aff002;  Sofía Ocaña-Mayorga aff002;  Maikell Segovia aff003;  Hernán J. Carrasco aff003;  Carolina Hernández aff004;  Juan David Ramírez aff004;  Michael D. Lewis aff005;  Mario J. Grijalva aff002;  Martin S. Llewellyn aff001
Působiště autorů: Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow, United Kingdom aff001;  Centro de Investigación para la Salud en América Latina, Pontificia Universidad Católica del Ecuador, Quito, Ecuador aff002;  Laboratorio de Biología Molecular de Protozoarios, Instituto de Medicina Tropical, Universidad Central de Venezuela, Caracas, Venezuela aff003;  Grupo de Investigaciones Microbiológicas-UR (GIMUR), Departamento de Biología, Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, Colombia aff004;  London School of Hygiene & Tropical Medicine, Keppel Street, London, United Kingdom aff005;  Infectious and Tropical Disease Institute, Biomedical Sciences Department, Heritage College of Osteopathic Medicine, Ohio University, Athens, OH, United States of America aff006
Vyšlo v časopise: Culture-free genome-wide locus sequence typing (GLST) provides new perspectives on Trypanosoma cruzi dispersal and infection complexity. PLoS Genet 16(12): e1009170. doi:10.1371/journal.pgen.1009170
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009170

Souhrn

Analysis of genetic polymorphism is a powerful tool for epidemiological surveillance and research. Powerful inference from pathogen genetic variation, however, is often restrained by limited access to representative target DNA, especially in the study of obligate parasitic species for which ex vivo culture is resource-intensive or bias-prone. Modern sequence capture methods enable pathogen genetic variation to be analyzed directly from host/vector material but are often too complex and expensive for resource-poor settings where infectious diseases prevail. This study proposes a simple, cost-effective ‘genome-wide locus sequence typing’ (GLST) tool based on massive parallel amplification of information hotspots throughout the target pathogen genome. The multiplexed polymerase chain reaction amplifies hundreds of different, user-defined genetic targets in a single reaction tube, and subsequent agarose gel-based clean-up and barcoding completes library preparation at under 4 USD per sample. Our study generates a flexible GLST primer panel design workflow for Trypanosoma cruzi, the parasitic agent of Chagas disease. We successfully apply our 203-target GLST panel to direct, culture-free metagenomic extracts from triatomine vectors containing a minimum of 3.69 pg/μl T. cruzi DNA and further elaborate on method performance by sequencing GLST libraries from T. cruzi reference clones representing discrete typing units (DTUs) TcI, TcIII, TcIV, TcV and TcVI. The 780 SNP sites we identify in the sample set repeatably distinguish parasites infecting sympatric vectors and detect correlations between genetic and geographic distances at regional (< 150 km) as well as continental scales. The markers also clearly separate TcI, TcIII, TcIV and TcV + TcVI and appear to distinguish multiclonal infections within TcI. We discuss the advantages, limitations and prospects of our method across a spectrum of epidemiological research.

Klíčová slova:

Cloning – DNA cloning – Heterozygosity – Polymerase chain reaction – Satellite DNA – Single nucleotide polymorphisms – Trypanosoma cruzi – Variant genotypes


Zdroje

1. Schwabl P, Imamura H, Van den Broeck F, Costales JA, Maiguashca-Sánchez J, Miles MA, et al. Meiotic sex in Chagas disease parasite Trypanosoma cruzi. Nat Commun. 2019;10(1):3972. doi: 10.1038/s41467-019-11771-z 31481692

2. Guerra-Assunção JA, Crampin AC, Houben RMGJ, Mzembe T, Mallard K, Coll F, et al. Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife. 2015;4:e05166. doi: 10.7554/eLife.05166 25732036

3. Hall MD, Holden MT, Srisomang P, Mahavanakul W, Wuthiekanun V, Limmathurotsakul D, et al. Improved characterisation of MRSA transmission using within-host bacterial sequence diversity. eLife. 2019;8:e46402. doi: 10.7554/eLife.46402 31591959

4. Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC. Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science. 2001;294(5540):161–5. doi: 10.1126/science.1061888 11588262

5. Wu Z, Periaswamy B, Sahin O, Yaeger M, Plummer P, Zhai W, et al. Point mutations in the major outer membrane protein drive hypervirulence of a rapidly expanding clone of Campylobacter jejuni. Proc Natl Acad Sci U S A. 2016;113(38):10690–5. doi: 10.1073/pnas.1605869113 27601641

6. Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet. 2015;47(3):226–34. doi: 10.1038/ng.3189 25599401

7. Auburn S, Benavente ED, Miotto O, Pearson RD, Amato R, Grigg MJ, et al. Genomic analysis of a pre-elimination Malaysian Plasmodium vivax population reveals selective pressures and changing transmission dynamics. Nat Commun. 2018;9:2585. doi: 10.1038/s41467-018-04965-4 29968722

8. Teixeira DG, Monteiro GRG, Martins DRA, Fernandes MZ, Macedo-Silva V, Ansaldi M, et al. Comparative analyses of whole genome sequences of Leishmania infantum isolates from humans and dogs in northeastern Brazil. Int J Parasitol. 2017;47(10–11):655–65. doi: 10.1016/j.ijpara.2017.04.004 28606698

9. Devera R, Fernandes O, Coura JR. Should Trypanosoma cruzi be called “cruzi” complex? a review of the parasite diversity and the potential of selecting population after in vitro culturing and mice infection. Mem Inst Oswaldo Cruz. 2003;98(1):1–12. doi: 10.1590/s0074-02762003000100001 12700855

10. Alves AM, De Almeida DF, von Krüger WM. Changes in Trypanosoma cruzi kinetoplast DNA minicircles induced by environmental conditions and subcloning. J Eukaryot Microbiol. 1994;41(4):415–9. doi: 10.1111/j.1550-7408.1994.tb06099.x 8087110

11. Dvorak J, Hartman D, Miles M. Trypanosoma cruzi: Correlation of growth kinetics to zymodeme type in clones derived from various sources. J Eukaryot Microbiol. 2007;27:472–4.

12. Deane MP, Jansen AM, Mangia RHR, Gonçalves AM, Morel CM. Are our laboratory “strains” representative samples of Trypanosoma cruzi populations that circulate in nature? Mem Inst Oswaldo Cruz. 1984;79(1):19–24.

13. Lima FM, Souza RT, Santori FR, Santos MF, Cortez DR, Barros RM, et al. Interclonal variations in the molecular karyotype of Trypanosoma cruzi: chromosome rearrangements in a single cell-derived clone of the G strain. PLoS One. 2013;8(5):e63738. doi: 10.1371/journal.pone.0063738 23667668

14. Reis-Cunha JL, Baptista RP, Rodrigues-Luiz GF, Coqueiro-dos-Santos A, Valdivia HO, de Almeida LV, et al. Whole genome sequencing of Trypanosoma cruzi field isolates reveals extensive genomic variability and complex aneuploidy patterns within TcII DTU. BMC Genomics. 2018;19(1):816. doi: 10.1186/s12864-018-5198-4 30424726

15. Messenger LA, Miles MA, Bern C. Between a bug and a hard place: Trypanosoma cruzi genetic diversity and the clinical outcomes of Chagas disease. Expert Rev Anti Infect Ther. 2015;13(8):995–1029. doi: 10.1586/14787210.2015.1056158 26162928

16. Cuypers B, Domagalska MA, Meysman P, Muylder G de, Vanaerschot M, Imamura H, et al. Multiplexed dpliced-leader sequencing: a high-throughput, selective method for RNA-seq in trypanosomatids. Sci Rep. 2017;7(1):1–11. doi: 10.1038/s41598-016-0028-x 28127051

17. Kumar N, Creasy T, Sun Y, Flowers M, Tallon LJ, Dunning Hotopp JC. Efficient subtraction of insect rRNA prior to transcriptome analysis of Wolbachia-Drosophila lateral gene transfer. BMC Res Notes. 2012;5:230. doi: 10.1186/1756-0500-5-230 22583543

18. Oyola SO, Gu Y, Manske M, Otto TD, O’Brien J, Alcock D, et al. Efficient depletion of host DNA contamination in malaria clinical sequencing. J Clin Microbiol. 2013;51(3):745–51. doi: 10.1128/JCM.02507-12 23224084

19. Feehery GR, Yigit E, Oyola SO, Langhorst BW, Schmidt VT, Stewart FJ, et al. A method for selectively enriching microbial DNA from contaminating vertebrate host DNA. PLoS One. 2013;8(10):e76096. doi: 10.1371/journal.pone.0076096 24204593

20. Domagalska MA, Imamura H, Sanders M, Broeck FV den, Bhattarai NR, Vanaerschot M, et al. Genomes of intracellular Leishmania parasites directly sequenced from patients. bioRxiv. 2019;676163.

21. Melnikov A, Galinsky K, Rogov P, Fennell T, Van Tyne D, Russ C, et al. Hybrid selection for sequencing pathogen genomes from clinical samples. Genome Biol. 2011;12(8):R73. doi: 10.1186/gb-2011-12-8-r73 21835008

22. Schuenemann VJ, Singh P, Mendum TA, Krause-Kyora B, Jäger G, Bos KI, et al. Genome-wide comparison of medieval and modern Mycobacterium leprae. Science. 2013;341(6142):179–83. doi: 10.1126/science.1238286 23765279

23. Metsky HC, Matranga CB, Wohl S, Schaffner SF, Freije CA, Winnicki SM, et al. Zika virus evolution and spread in the Americas. Nature. 2017;546(7658):411–5. doi: 10.1038/nature22402 28538734

24. Cowell AN, Loy DE, Sundararaman SA, Valdivia H, Fisch K, Lescano AG, et al. Selective whole-genome amplification is a robust method that enables scalable whole-genome sequencing of Plasmodium vivax from unprocessed clinical samples. mBio. 2017;8(1):e02257–16. doi: 10.1128/mBio.02257-16 28174312

25. Hintzsche JD, Robinson WA, Tan AC. A survey of computational tools to analyze and interpret whole exome sequencing data. Int J Genomics. 2016;2016:7983236. doi: 10.1155/2016/7983236 28070503

26. Gampawar P, Saba Y, Werner U, Schmidt R, Müller-Myhsok B, Schmidt H. Evaluation of the performance of AmpliSeq and SureSelect exome sequencing libraries for Ion Proton. Front Genet. 2019;10:856. doi: 10.3389/fgene.2019.00856 31608108

27. Nag S, Dalgaard MD, Kofoed P-E, Ursing J, Crespo M, Andersen LO, et al. High throughput resistance profiling of Plasmodium falciparum infections based on custom dual indexing and Illumina next generation sequencing-technology. Sci Rep. 2017;7(1):2398. doi: 10.1038/s41598-017-02724-x 28546554

28. Balkenhol N, Cushman S, Storfer A, Waits L. Landscape Genetics: Concepts, Methods, Applications. John Wiley & Sons; 2015. 292 p.

29. Momčilović S, Cantacessi C, Arsić-Arsenijević V, Otranto D, Tasić-Otašević S. Rapid diagnosis of parasitic diseases: current scenario and future needs. Clin Microbiol Infect. 2019;25(3):290–309. doi: 10.1016/j.cmi.2018.04.028 29730224

30. Arias A, Watson SJ, Asogun D, Tobin EA, Lu J, Phan MVT, et al. Rapid outbreak sequencing of Ebola virus in Sierra Leone identifies transmission chains linked to sporadic cases. Virus Evol. 2016;2(1):vew016. doi: 10.1093/ve/vew016 28694998

31. Park J, Shin SY, Kim K, Park K, Shin S, Ihm C. Determining genotypic drug resistance by ion semiconductor sequencing with the Ion AmpliSeqTM TB Panel in multidrug-resistant Mycobacterium tuberculosis isolates. Ann Lab Med. 2018;38(4):316–23. doi: 10.3343/alm.2018.38.4.316 29611381

32. Ferrario C, Milani C, Mancabelli L, Lugli GA, Turroni F, Duranti S, et al. A genome-based identification approach for members of the genus Bifidobacterium. FEMS Microbiol Ecol. 2015;91(3):fiv009. doi: 10.1093/femsec/fiv009 25764568

33. Makowsky R, Lhaki P, Wiener HW, Bhatta MP, Cullen M, Johnson DC, et al. Genomic diversity and phylogenetic relationships of human papillomavirus 16 (HPV16) in Nepal. Infect Genet Evol. 2016;46:7–11. doi: 10.1016/j.meegid.2016.10.004 27725301

34. Schwabl P. Genomics and spatial surveillance of Chagas disease and American visceral leishmaniasis. University of Glasgow (doctoral thesis). 2020. Available from: http://theses.gla.ac.uk/81448/1/2020schwablphd.pdf

35. Brenière SF, Waleckx E, Barnabé C. Over six thousand Trypanosoma cruzi strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Negl Trop Dis. 2016;10(8):e0004792. doi: 10.1371/journal.pntd.0004792 27571035

36. Monteiro WM, Magalhães LKC, de Sá ARN, Gomes ML, Toledo MJ de O, Borges L, et al. Trypanosoma cruzi IV causing outbreaks of acute Chagas disease and infections by different haplotypes in the Western Brazilian Amazonia. PloS One. 2012;7(7):e41284. doi: 10.1371/journal.pone.0041284 22848457

37. Ramírez JD, Montilla M, Cucunubá ZM, Floréz AC, Zambrano P, Guhl F. Molecular epidemiology of human oral Chagas disease outbreaks in Colombia. PLoS Negl Trop Dis. 2013;7(2):e2041. doi: 10.1371/journal.pntd.0002041 23437405

38. Flores-López CA, Machado CA. Analyses of 32 loci clarify phylogenetic relationships among Trypanosoma cruzi lineages and support a single hybridization prior to human contact. PLoS Negl Trop Dis. 2011;5(8):e1272. doi: 10.1371/journal.pntd.0001272 21829751

39. Grijalva MJ, Suarez-Davalos V, Villacis AG, Ocaña-Mayorga S, Dangles O. Ecological factors related to the widespread distribution of sylvatic Rhodnius ecuadoriensis populations in southern Ecuador. Parasit Vectors. 2012;5:17. doi: 10.1186/1756-3305-5-17 22243930

40. Nascimento JD, Rosa JA da, Salgado-Roa FC, Hernández C, Pardo-Diaz C, Alevi KCC, et al. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One. 2019;14(2):e0211285. doi: 10.1371/journal.pone.0211285 30730919

41. Velásquez-Ortiz N, Hernández C, Herrera G, Cruz-Saavedra L, Higuera A, Arias-Giraldo LM, et al. Trypanosoma cruzi infection, discrete typing units and feeding sources among Psammolestes arthuri (Reduviidae: Triatominae) collected in eastern Colombia. Parasit Vectors. 2019;12(1):157. doi: 10.1186/s13071-019-3422-y 30961657

42. Caicedo-Garzón V, Salgado-Roa FC, Sánchez-Herrera M, Hernández C, Arias-Giraldo LM, García L, et al. Genetic diversification of Panstrongylus geniculatus (Reduviidae: Triatominae) in northern South America. PLoS One. 2019;14(10):e0223963. doi: 10.1371/journal.pone.0223963 31622439

43. Carrasco HJ, Torrellas A, García C, Segovia M, Feliciangeli MD. Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (Metropolitan District) and neighboring states, Venezuela. Int J Parasitol. 2005;35(13):1379–84. doi: 10.1016/j.ijpara.2005.05.003 16019006

44. Carrasco HJ, Segovia M, Llewellyn MS, Morocoima A, Urdaneta-Morales S, Martínez C, et al. Geographical distribution of Trypanosoma cruzi genotypes in Venezuela. PLoS Negl Trop Dis. 2012;6(6):e1707. doi: 10.1371/journal.pntd.0001707 22745843

45. Nakad Bechara CC, Londoño JC, Segovia M, Sanchez MAL, Martínez PCE, Rodríguez RMM, Carrasco HJ. Genetic variability of Panstrongylus geniculatus (Reduviidae: Triatominae) in the Metropolitan District of Caracas, Venezuela. Infect Genet Evol. 2018;66:236–44. doi: 10.1016/j.meegid.2018.09.011 30240833

46. Messenger LA, Yeo M, Lewis MD, Llewellyn MS, Miles MA. Molecular genotyping of Trypanosoma cruzi for lineage assignment and population genetics. Methods Mol Biol. 2015;1201:297–337. doi: 10.1007/978-1-4939-1438-8_19 25388123

47. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. doi: 10.1093/bioinformatics/btp324 19451168

48. 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

49. Derrien T, Estellé J, Marco Sola S, Knowles DG, Raineri E, Guigó R, et al. Fast computation and applications of genome mappability. PLoS One. 2012;7(1):e3037. doi: 10.1371/journal.pone.0030377 22276185

50. Franzén O, Talavera-López C, Ochaya S, Butler CE, Messenger LA, Lewis MD, et al. Comparative genomic analysis of human infective Trypanosoma cruzi lineages with the bat-restricted subspecies T. cruzi marinkellei. BMC Genomics. 2012;13:531. doi: 10.1186/1471-2164-13-531 23035642

51. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–89. doi: 10.1101/gr.1224503 12952885

52. Talavera-Lopez C, Messenger LA, Lewis MD, Yeo M, Reis-Cunha JL, Bartholomeu DC, et al. Repeat-driven generation of antigenic diversity in a major human pathogen, Trypanosoma cruzi. bioRxiv. 2018;283531.

53. You FM, Huo N, Gu YQ, Luo M-C, Ma Y, Hane D, et al. BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics. 2008;9:253. doi: 10.1186/1471-2105-9-253 18510760

54. Kaplinski L, Andreson R, Puurand T, Remm M. MultiPLX: automatic grouping and evaluation of PCR primers. Bioinformatics. 2005;21(8):17012. doi: 10.1093/bioinformatics/bti219 15598831

55. Sonnhammer EL, Hollich V. Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinformatics. 2005;6:108. doi: 10.1186/1471-2105-6-108 15857510

56. Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20(2):289–90. doi: 10.1093/bioinformatics/btg412 14734327

57. R: The R Project for Statistical Computing. Available from: https://www.r-project.org/

58. Cummings KL, Tarleton RL. Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol Biochem Parasitol. 2003;129(1):53–9. doi: 10.1016/s0166-6851(03)00093-8 12798506

59. Access Array System for Illumina Sequencing Systems. Available from: https://docplayer.net/78505463-Access-array-system-for-illumina-sequencing-systems.html

60. Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PloS One. 2011;6(3):e17288. doi: 10.1371/journal.pone.0017288 21408061

61. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. doi: 10.1093/bioinformatics/btr330 21653522

62. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37–48. doi: 10.1093/oxfordjournals.molbev.a026036 10331250

63. Leigh JW and Bryant D. PopART: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–16.

64. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81(3):559–75. doi: 10.1086/519795 17701901

65. Ritland K. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Evolution. 1990;44(5):1230–41. doi: 10.1111/j.1558-5646.1990.tb05227.x 28563887

66. Wigginton JE, Cutler DJ, Abecasis GR. A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet. 2005;76(5):887–93. doi: 10.1086/429864 15789306

67. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10(3):564–7. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

68. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. Available from: https://CRAN.R-project.org/package=vegan

69. Šavrič B, Jenny B, Jenny H. Projection wizard–an online map projection selection tool. Cartogr J. 2016;53(2):177–85.

70. Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations. Evol Int J Org Evol. 1993;47(1):264–79. doi: 10.1111/j.1558-5646.1993.tb01215.x 28568097

71. Zumaya-Estrada FA, Messenger LA, Lopez-Ordonez T, Lewis MD, Flores-Lopez CA, Martínez-Ibarra AJ, et al. North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasit Vectors. 2012;5:226. doi: 10.1186/1756-3305-5-226 23050833

72. Ocaña-Mayorga S, Llewellyn MS, Costales JA, Miles MA, Grijalva MJ. Sex, subdivision, and domestic dispersal of Trypanosoma cruzi lineage I in southern Ecuador. PLoS Negl Trop Dis. 2010;4(12):e915. doi: 10.1371/journal.pntd.0000915 21179502

73. Messenger LA, Garcia L, Vanhove M, Huaranca C, Bustamante M, Torrico M, et al. Ecological host fitting of Trypanosoma cruzi TcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal. Mol Ecol. 2015;24(10):2406–22. doi: 10.1111/mec.13186 25847086

74. Ramírez JD, Guhl F, Messenger LA, Lewis MD, Montilla M, Cucunuba Z, et al. Contemporary cryptic sexuality in Trypanosoma cruzi. Mol Ecol. 2012;21(17):4216–26. doi: 10.1111/j.1365-294X.2012.05699.x 22774844

75. Llewellyn MS, Lewis MD, Acosta N, Yeo M, Carrasco HJ, Segovia M, et al. Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent Chagas disease. PLoS Negl Trop Dis. 2009;3(9):e510. doi: 10.1371/journal.pntd.0000510 19721699

76. Roman F, Xavier S das C, Messenger LA, Pavan MG, Miles MA, Jansen AM, et al. Dissecting the phyloepidemiology of Trypanosoma cruzi I (TcI) in Brazil by the use of high resolution genetic markers. PLoS Negl Trop Dis. 2018;12(5):e0006466. doi: 10.1371/journal.pntd.0006466 29782493

77. Barnabe C, Buitrago R, Bremond P, Aliaga C, Salas R, Vidaurre P, et al. Putative panmixia in restricted populations of Trypanosoma cruzi isolated from wild Triatoma infestans in Bolivia. PloS One. 2013;8(11):e82269. doi: 10.1371/journal.pone.0082269 24312410

78. Llewellyn MS. The molecular epidemiology of Trypanosoma cruzi infection in wild and domestic transmission cycles with special emphasis on multilocus microsatellite analysis. London School of Hygiene & Tropical Medicine (doctoral thesis). 2008. Available from: https://researchonline.lshtm.ac.uk/id/eprint/4652860/

79. Lewis MD, Llewellyn MS, Yeo M, Acosta N, Gaunt MW, Miles MA. Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids. PLoS Negl Trop Dis. 2011; 5(10):e1363. doi: 10.1371/journal.pntd.0001363 22022633

80. Shibata H, Rai SK, Satoh M, Murakoso K, Sumi K, Uga S, et al. The use of PCR in detecting toxoplasma parasites in the blood and brains of mice experimentally infected with Toxoplasma gondii. Kansenshogaku Zasshi. 1995;69(2):158–63. doi: 10.11150/kansenshogakuzasshi1970.69.158 7745290

81. Yang H, Golenberg EM, Shoshani J. Proboscidean DNA from museum and fossil specimens: an assessment of ancient DNA extraction and amplification techniques. Biochem Genet. 1997;35(5):165–79. doi: 10.1023/a:1021902125382 9332711

82. Ramos RAN, Ramos CAN, Santos EMS, de Araújo FR, de Carvalho GA, Faustino MAG, et al. Quantification of Leishmania infantum DNA in the bone marrow, lymph node and spleen of dogs. Rev Bras Parasitol Vet. 2013;22(3):346–50. doi: 10.1590/S1984-29612013000300005 24142164

83. Schubert G, Stockhausen M, Hoffmann C, Merkel K, Vigilant L, Leendertz F, et al. Targeted detection of mammalian species using carrion fly–derived DNA. Mol Ecol Resour. 2015;15(2):285–94. doi: 10.1111/1755-0998.12306 25042567

84. Côté NML, Daligault J, Pruvost M, Bennett EA, Gorgé O, Guimaraes S, et al. A new high-throughput approach to genotype ancient human gastrointestinal parasites. PLoS One. 2016. 11(1):e0146230. doi: 10.1371/journal.pone.0146230 26752051

85. Cencig S, Coltel N, Truyens C, Carlier Y. Parasitic loads in tissues of mice infected with Trypanosoma cruzi and treated with AmBisome. PLoS Negl Trop Dis. 2011;5(6):e1216. doi: 10.1371/journal.pntd.0001216 21738811

86. Thompson CT, Dvorak JA. Quantitation of total DNA per cell in an exponentially growing population using the diphenylamine reaction and flow cytometry. Anal Biochem. 1989; 177(2):353–7. doi: 10.1016/0003-2697(89)90065-1 2658678

87. Reithinger R, Lambson BE, Barker DC, Davies CR. Use of PCR to detect Leishmania (Viannia) spp. in dog blood and bone marrow. 2000;38(2):748–51. doi: 10.1128/JCM.38.2.748-751.2000 10655379

88. Wen C, Wu L, Qin Y, Van Nostrand JD, Ning D, Sun B, et al. Evaluation of the reproducibility of amplicon sequencing with Illumina MiSeq platform. PLoS One.2017;12(4):e0176716. doi: 10.1371/journal.pone.0176716 28453559

89. Storfer A, Patton A, Fraik AK. Navigating the interface between landscape genetics and landscape genomics. Front Genet. 2018;13;9:68. doi: 10.3389/fgene.2018.00068 29593776

90. Erben ED. High-throughput methods for dissection of trypanosome gene regulatory networks. Curr Genomics. 2018;19(2):78–86. doi: 10.2174/1389202918666170815125336 29491736

91. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012;6(2):80–92. doi: 10.4161/fly.19695 22728672

92. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841–2. doi: 10.1093/bioinformatics/btq033 20110278

93. Aurrecoechea C, Barreto A, Basenko EY, Brestelli J, Brunk BP, Cade C, et al. EuPathDB: the eukaryotic pathogen genomics database resource. Nucleic Acids Res. 2017;45(database issue):D581–D591. doi: 10.1093/nar/gkw1105 27903906

94. Linck E, Battey CJ. Minor allele frequency thresholds strongly affect population structure inference with genomic data sets. Mol Ecol Resour. 2019;19(3):639–47. doi: 10.1111/1755-0998.12995 30659755

95. Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M. Robust demographic inference from genomic and SNP data. PLoS Genet. 2013;9(10):e1003905. doi: 10.1371/journal.pgen.1003905 24204310

96. Bryant D, Bouckaert R, Felsenstein J, Rosenberg NA, RoyChoudhury A. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol Biol Evol. 2012;29(8):1917–32. doi: 10.1093/molbev/mss086 22422763

97. Landguth EL, Bearlin A, Day CC, Dunham J. CDMetaPOP: an individual-based, eco-evolutionary model for spatially explicit simulation of landscape demogenetics. Methods Ecol Evol. 2017;8(1):4–11.

98. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59. 10835412

99. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered. 2004;95(6):536–9. doi: 10.1093/jhered/esh074 15475402

100. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol. 2013;30(5):1224–8. doi: 10.1093/molbev/mst028 23408797

101. Anderson EC, Thompson EA. A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002;160(3):1217–29. 11901135

102. Graffelman J, Jain D, Weir B. A genome-wide study of Hardy–Weinberg equilibrium with next generation sequence data. Hum Genet. 2017;136(6):727–41. doi: 10.1007/s00439-017-1786-7 28374190

103. Sefid Dashti MJ, Gamieldien J. A practical guide to filtering and prioritizing genetic variants. BioTechniques. 2017;62(1):18–30. doi: 10.2144/000114492 28118812

104. Etherington TR. Python based GIS tools for landscape–genetics: visualising genetic relatedness and measuring landscape connectivity. Methods Ecol Evol. 2011;2:52–5.

105. Carrasco HJ, Segovia M, Londoño JC, Ortegoza J, Rodríguez M, Martínez CE. Panstrongylus geniculatus and four other species of triatomine bug involved in the Trypanosoma cruzi enzootic cycle: high risk factors for Chagas’ disease transmission in the Metropolitan District of Caracas, Venezuela. Parasit Vectors. 2014;7:602. doi: 10.1186/s13071-014-0602-7 25532708

106. Zingales B. Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Trop. 2018;184:38–52. doi: 10.1016/j.actatropica.2017.09.017 28941731

107. Nunes Maria Carmo Pereira, Beaton Andrea, Acquatella Harry, Bern Caryn, Bolger Ann F., Echeverría Luis E., et al. Chagas cardiomyopathy: an update of current clinical knowledge and management: a scientific statement from the American Heart Association. Circulation. 2018;138(12):e169–209. doi: 10.1161/CIR.0000000000000599 30354432

108. Llewellyn MS, Rivett-Carnac JB, Fitzpatrick S, Lewis MD, Yeo M, Gaunt MW, et al. Extraordinary Trypanosoma cruzi diversity within single mammalian reservoir hosts implies a mechanism of diversifying selection. Int J Parasitol. 2011;41(6–10):609–14. doi: 10.1016/j.ijpara.2010.12.004 21232539

109. Valadares HMS, Pimenta JR, Segatto M, Veloso VM, Gomes ML, Chiari E, et al. Unequivocal identification of subpopulations in putative multiclonal Trypanosoma cruzi strains by FACs single cell sorting and genotyping. PLoS Negl Trop Dis. 2012;6(7):e1722. doi: 10.1371/journal.pntd.0001722 22802979

110. Pronovost H, Peterson AC, Chavez BG, Blum MJ, Dumonteil E, Herrera CP. Deep sequencing reveals multiclonality and new discrete typing units of Trypanosoma cruzi in rodents from the southern United States. J Microbiol Immunol Infect. 2018;S1684-1182(18)30097–5. doi: 10.1016/j.jmii.2018.12.004 30709717

111. Yeo M, Lewis MD, Carrasco HJ, Acosta N, Llewellyn M, da Silva Valente SA, et al. Resolution of multiclonal infections of Trypanosoma cruzi from naturally infected triatomine bugs and from experimentally infected mice by direct plating on a sensitive solid medium. Int J Parasitol. 2007;37(1):111–20. doi: 10.1016/j.ijpara.2006.08.002 17052720

112. Baptista RP, Reis-Cunha JL, DeBarry JD, Chiari E, Kissinger JC, Bartholomeu DC, et al. Assembly of highly repetitive genomes using short reads: the genome of discrete typing unit III Trypanosoma cruzi strain 231. Microb Genomics. 2018;4(4):e000156. doi: 10.1099/mgen.0.000156 29442617


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