Genomic diversity in Onchocerca volvulus and its Wolbachia endosymbiont

Nature Microbiology

Volumn 2, Issue , 2016, Pages

  Choi, Young Jun ^a   Tyagi, Rahul ^a   McNulty, Samantha N ^a   Rosa, Bruce A ^a   Ozersky, Philip ^a   Martin, John ^a   Hallsworth Pepin, Kymberlie ^a   Unnasch, Thomas R ^b   Norice, Carmelle T ^c   Nutman, Thomas B ^c   Weil, Gary J ^a   Fischer, Peter U ^a   Mitreva, Makedonka ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ANIMAL; CLASSIFICATION; ECUADOR; GENE FLOW; GENETIC VARIATION; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; MICROBIOLOGY; ONCHOCERCA VOLVULUS; PHYLOGEOGRAPHY; UGANDA; WOLBACHIA;

AFRICA, WESTERN; ANIMALS; ECUADOR; GENE FLOW; GENETIC VARIATION; GENOTYPE; ONCHOCERCA VOLVULUS; PHYLOGEOGRAPHY; UGANDA; WOLBACHIA;

EID: 84996490437     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.207     Document Type: Article

References (74)

1. Dunn, C. et al. The contributions of onchocerciasis control and elimination programs toward the achievement of the millennium development goals. PLoS Negl. Trop. Dis. 9, e0003703 (2015).
2. Crump, A., Morel, C. M. & Omura, S. The onchocerciasis chronicle: from the beginning to the end? Trends Parasitol. 28, 280-288 (2012).
3. Cupp, E.W., Sauerbrey,M. & Richards, F. Elimination of human onchocerciasis: history of progress and current feasibility using ivermectin (Mectizan®) monotherapy. Acta Trop. 120(Suppl. 1), S100-S108 (2011).
4. Coffeng, L. E. et al. African programme for onchocerciasis control 1995-2015: updated health impact estimates based on new disability weights. PLoS Negl. Trop. Dis. 8, e2759 (2014).
5. Progress towards eliminating onchocerciasis in the WHO region of the americas: verification by WHO of elimination of transmission in Colombia. Wkly Epidemiol. Rec. 88, 381-385 (2013).
6. Elimination of onchocerciasis in the WHO region of the Americas: Ecuador's progress towards verification of elimination. Wkly Epidemiol. Rec. 89, 401-405 (2014).
7. Mackenzie, C. D., Homeida, M. M., Hopkins, A. D. & Lawrence, J. C. Elimination of onchocerciasis from Africa: possible? Trends Parasitol. 28, 16-22 (2012).
8. Centers for Disease Control and Prevention. Progress toward elimination of onchocerciasis in the Americas - 1993-2012. MMWR Morb. Mortal. Wkly. Rep. 62, 405-408 (2013).
9. WHO. African Programme for Onchocerciasis Control: progress report, 2013-2014. Wkly Epidemiol. Rec. 89, 545-560 (2014).
10. Osei-Atweneboana, M. Y., Eng, J. K. L., Boakye, D. A., Gyapong, J. O. & Prichard, R. K. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 369, 2021-2029 (2007).
11. Dadzie, K. Y., Remme, J., Baker, R. H., Rolland, A. & Thylefors, B. Ocular onchocerciasis and intensity of infection in the community. III. West African rainforest foci of the vector Simulium sanctipauli. Trop. Med. Parasitol. 41, 376-382 (1990).
12. Remme, J., Dadzie, K. Y., Rolland, A. & Thylefors, B. Ocular onchocerciasis and intensity of infection in the community. I. West African savanna. Trop. Med. Parasitol. 40, 340-347 (1989).
13. Botto, C., Escalante, A., Arango, M. & Yarzabal, L. Morphological differences between Venezuelan and African microfilariae of Onchocerca volvulus. J. Helminthol. 62, 345-351 (1988).
14. Eichner, M. & Renz, A. Differential length of Onchocerca volvulus infective larvae from the Cameroon rain forest and savanna. Trop. Med. Parasitol. 41, 29-32 (1990).
15. Vuong, P. N. et al. Forest and savanna onchocerciasis: comparative morphometric histopathology of skin lesions. Trop. Med. Parasitol. 39, 105-110 (1988).
16. Duke, B. O., Lewis, D. J. & Moore, P. J. Onchocerca-Simulium complexes. I. Transmission of forest and Sudan-savanna strains of Onchocerca volvulus, from Cameroon, by Simulium damnosum from various West African bioclimatic zones. Ann. Trop. Med. Parasitol. 60, 318-326 (1966).
17. Omar, M. S., Prost, A. & Marshall, T. F. Histochemical enzyme variation in Onchocerca volvulus microfilariae from rain-forest and Sudan-savanna areas of the Onchocerciasis Control Programme in West Africa. Bull. World Health Organ. 60, 933-944 (1982).
18. Flockhart, H. A., Cibulskis, R. E., Karam, M. & Albiez, E. J. Onchocerca volvulus: enzyme polymorphism in relation to the differentiation of forest and savannah strains of this parasite. Trans. R. Soc. Trop. Med. Hyg. 80, 285-292 (1986).
19. Higazi, T. B. et al. Wolbachia endosymbiont levels in severe and mild strains of Onchocerca volvulus. Mol. Biochem. Parasitol. 141, 109-112 (2005).
20. Zimmerman, P. A. et al. Onchocerca volvulus DNA probe classification correlates with epidemiologic patterns of blindness. J. Infect. Dis. 165, 964-968 (1992).
21. Fischer, P., Bamuhiiga, J., Kilian, A. H. & Buttner, D.W. Strain differentiation of Onchocerca volvulus from Uganda using DNA probes. Parasitology 112(Pt 4), 401-408 (1996).
22. Higazi, T. B. et al. Onchocerca volvulus: genetic diversity of parasite isolates from Sudan. Exp. Parasitol. 97, 24-34 (2001).
23. Morales-Hojas, R., Cheke, R. A. & Post, R. J. A preliminary analysis of the population genetics and molecular phylogenetics of Onchocerca volvulus (Nematoda: Filarioidea) using nuclear ribosomal second internal transcribed spacer sequences. Mem. Inst. Oswaldo Cruz 102, 879-882 (2007).
24. Keddie, E. M. et al. Onchocerca volvulus: limited heterogeneity in the nuclear and mitochondrial genomes. Exp. Parasitol. 93, 198-206 (1999).
25. Gallin, M. et al. Epidemiological studies of onchocerciasis in southern Benin. Trop. Med. Parasitol. 44, 69-74 (1993).
26. Nutman, T. B., Parredes, W., Kubofcik, J. & Guderian, R. H. Polymerase chain reaction-based assessment after macrofilaricidal therapy in Onchocerca volvulus infection. J. Infect. Dis. 173, 773-776 (1996).
27. Cotton, J. A. et al. The genome of Onchocerca volvulus, agent of river blindness. Nat. Microbiol. 2, 16216 (2016).
28. Post, R. The chromosomes of the Filariae. Filaria J. 4, 10 (2005).
29. Andersen, E. C. et al. Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat. Genet. 44, 285-290 (2012).
30. Cutter, A. D. Integrating phylogenetics, phylogeography and population genetics through genomes and evolutionary theory. Mol. Phylogenet. Evol. 69, 1172-1185 (2013).
31. Johnson, N. A. & Lachance, J. The genetics of sex chromosomes: evolution and implications for hybrid incompatibility. Ann. NY Acad. Sci. 1256, E1-E22 (2012).
32. Zimmerman, P. A. et al. Migration of a novel DQA1∗ allele (DQA1∗0502) from African origin to North and South America. Hum. Immunol. 42, 233-240 (1995).
33. Pezzi, P. J. P. & Trebeschi, P. in Coleccion Antropolgia Aplicada no 10 (eds Pezzi, P. J. P., Nunez, G. C. & Minda, P.) U.P.S. 12-98 (Quito, 1996).
34. Boakye, D. A., Back, C., Fiasorgbor, G. K., Sib, A. P. & Coulibaly, Y. Sibling species distributions of the Simulium damnosum complex in the west African Onchocerciasis Control Programme area during the decade 1984-93, following intensive larviciding since 1974. Med. Vet. Entomol. 12, 345-358 (1998).
35. Wilson, M. D. et al. Deforestation and the spatio-temporal distribution of savannah and forest members of the Simulium damnosum complex in southern Ghana and south-western Togo. Trans. R. Soc. Trop. Med. Hyg. 96, 632-639 (2002).
36. Baker, R. H. et al. Progress in controlling the reinvasion of windborne vectors into the western area of the Onchocerciasis Control Programme in West Africa. Philos. Trans. R. Soc. Lond. B 328, 731-747, discussion 747-750 (1990).
37. Duke, B. O. Geographical aspects of onchocerciasis. Ann. Soc. Belge. Med. Trop. 61, 179-186 (1981).
38. Basáñez, M.-G., Churcher, T. S. & Grillet, M. E. Onchocerca-Simulium interactions and the population and evolutionary biology of Onchocerca volvulus. Adv. Parasitol. 68, 263-313 (2009).
39. Thomas, J. H. & Robertson, H. M. The Caenorhabditis chemoreceptor gene families. BMC Biol. 6, 42 (2008).
40. Stallings, T., Cupp, M. S. & Cupp, E.W. Orientation of Onchocerca lienalis stiles (Filarioidea: Onchocercidae) microfilariae to black fly saliva. J. Med. Entomol. 39, 908-914 (2002).
41. Chang, C.-C. & Lin, C.-J. LIBSVM: a library for support vector machines. ACM Trans. Intelligent Syst. Technol. 2, 27 (2011).
42. Taylor, M. J., Voronin, D., Johnston, K. L. & Ford, L. Wolbachia filarial interactions. Cell. Microbiol. 15, 520-526 (2013).
43. McGarry, H. F., Egerton, G. L. & Taylor, M. J. Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol. Biochem. Parasitol. 135, 57-67 (2004).
44. Zimmerman, P. A., Katholi, C. R., Wooten, M. C., Lang-Unnasch, N. & Unnasch, T. R. Recent evolutionary history of American Onchocerca volvulus, based on analysis of a tandemly repeated DNA sequence family. Mol. Biol. Evol. 11, 384-392 (1994).
45. Toews, D. P. & Brelsford, A. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21, 3907-3930 (2012).
46. Ballard, J. W. & Whitlock, M. C. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729-744 (2004).
47. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
48. Cheke, R. A. & Garms, R. Indices of onchocerciasis transmission by different members of the Simulium damnosum complex conflict with the paradigm of forest and savanna parasite strains. Acta Trop. 125, 43-52 (2013).
49. Dodt, M., Roehr, J. T., Ahmed, R. & Dieterich, C. Flexbar - flexible barcode and adapter processing for next-generation sequencing platforms. MDPI Biol. 1, 895-905 (2012).
50. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
51. McKenna, A. et al. The genome analysis toolkit: a mapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
52. Cingolani, P. 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 (Austin) 6, 80-92 (2012).
53. Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
54. Purcell, S. et al. PLINK. A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).
55. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 (1989).
56. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).
57. Wang, D., Zhang, Y., Zhang, Z., Zhu, J. & Yu, J. Kaks-Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8, 77-80 (2010).
58. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065-1093 (2012).
59. Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).
60. Beissinger, T. M., Rosa, G. J. M., Kaeppler, S. M., Gianola, D. & de Leon, N. Defining window-boundaries for genomic analyses using smoothing spline techniques. Genet. Sel. Evol. 47, 30 (2015).
61. Prüfer, K. et al. FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinformatics 8, 41 (2007).
62. Dunning Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753-1756 (2007).
63. Pulido-Tamayo, S. et al. Frequency-based haplotype reconstruction from deep sequencing data of bacterial populations. Nucleic Acids Res. 43, e105 (2015).
64. Li, M. et al. Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am. J. Hum. Genet. 87, 237-249 (2010).
65. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120 (1980).
66. Massey, F. J. Jr The Kolmogorov-Smirnov test for goodness of fit. J. Am. Stat. Assoc. 46, 68-78 (1951).
67. Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479-491 (1992).
68. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
69. Bandelt, H. J., Forster, P. & Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37-48 (1999).
70. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
71. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).
72. Stamatakis, A., Hoover, P. & Rougemont, J. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 57, 758-771 (2008).
73. Legendre, P., Desdevises, Y. & Bazin, E. A statistical test for host-parasite coevolution. Syst. Biol. 51, 217-234 (2002).
74. Oton, E. V., Quince, C., Nicol, G. W., Prosser, J. I. & Gubry-Rangin, C. Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota. ISME J. 10, 85-96 (2016).