Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria

Nature Communications

Volumn 7, Issue , 2016, Pages

  Sundararaman, Sesh A ^a   Plenderleith, Lindsey J ^b   Liu, Weimin ^a   Loy, Dorothy E ^a   Learn, Gerald H ^a   Li, Yingying ^a   Shaw, Katharina S ^a   Ayouba, Ahidjo ^c   Peeters, Martine ^c   Speede, Sheri ^d   Shaw, George M ^a   Bushman, Frederic D ^a   Brisson, Dustin ^a   Rayner, Julian C ^e   Sharp, Paul M ^b   Hahn, Beatrice H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITÉ DE MONTPELLIER   (France)

^d IDA Africa   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME; CRYPSIS; DNA FINGERPRINTING; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; GENETIC ANALYSIS; GENOME; MALARIA; PARASITE; PRIMATE; PROTOZOAN;

CHIMPANZEE; CHROMOSOME 4; ERYTHROCYTE; GENE AMPLIFICATION; GENOME; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; HUMAN VERSUS NONHUMAN DATA; MATING; MULTIGENE FAMILY; PATHOGENESIS; PLASMODIUM; PRECURSOR; SPECIES; ANIMAL; EVOLUTION; GENETIC VARIATION; GENETICS; MALARIA FALCIPARUM; MOLECULAR EVOLUTION; PAN TROGLODYTES; PARASITOLOGY; PHYLOGENY; PLASMODIUM FALCIPARUM; REAL TIME POLYMERASE CHAIN REACTION;

PAN; PLASMODIUM FALCIPARUM; PLASMODIUM REICHENOWI;

ANIMALS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, PROTOZOAN; HUMANS; MALARIA, FALCIPARUM; MULTIGENE FAMILY; PAN TROGLODYTES; PHYLOGENY; PLASMODIUM; PLASMODIUM FALCIPARUM; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84961613394     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11078     Document Type: Article

References (70)

1. Bray, R. S. The malaria parasites of anthropoid apes. J. Parasitol. 49, 888-891 (1963).
2. Escalante, A. A. & Ayala, F. J. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc. Natl Acad. Sci. USA 91, 11373-11377 (1994).
3. Ollomo, B. et al. A new malaria agent in African hominids. PLoS Pathog. 5, e1000446 (2009).
4. Rich, S. M. et al. The origin of malignant malaria. Proc. Natl Acad. Sci. USA 106, 14902-14907 (2009).
5. Prugnolle, F. et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc. Natl Acad. Sci. USA 107, 1458-1463 (2010).
6. Duval, L. et al. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc. Natl Acad. Sci. USA 107, 10561-10566 (2010).
7. Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420-425 (2010).
8. Miller, L. H., Baruch, D. I., Marsh, K. & Doumbo, O. K. The pathogenic basis of malaria. Nature 415, 673-679 (2002).
9. Rayner, J. C., Liu, W., Peeters, M., Sharp, P. M. & Hahn, B. H. A plethora of Plasmodium species in wild apes: a source of human infection? Trends Parasitol. 27, 222-229 (2011).
10. Larremore, D. B. et al. Ape parasite origins of human malaria virulence genes. Nat. Commun. 6, 8368 (2015).
11. Gardner, M. J. et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511 (2002).
12. Otto, T. D. et al. Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat. Commun. 5, 4754 (2014).
13. Pain, A. et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455, 799-803 (2008).
14. Carlton, J. M. et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455, 757-763 (2008).
15. Tachibana, S. I. et al. Plasmodium cynomolgi genome sequences provide insight into Plasmodium vivax and the monkey malaria clade. Nat. Genet. 44, 1051-1055 (2012).
16. Collins, W. E., Skinner, J. C., Pappaioanou, M., Broderson, J. R. & Mehaffey, P. The sporogonic cycle of Plasmodium reichenowi. J. Parasitol. 72, 292-298 (1986).
17. Paez, J. G. et al. Genome coverage and sequence fidelity of Phi29 polymerasebased multiple strand displacement whole genome amplification. Nucleic Acids Res. 32, e71-e71 (2004).
18. Blanco, L. et al. Highly efficient DNA synthesis by the phage Phi29 DNA polymerase. Symmetrical mode of DNA replication. J. Biol. Chem. 264, 8935-8940 (1989).
19. Leichty, A. R. & Brisson, D. Selective whole genome amplification for resequencing target microbial species from complex natural samples. Genetics 198, 473-481 (2014).
20. Oyola, S. O. et al. Efficient depletion of host DNA contamination in malaria clinical sequencing. J. Clin. Microbiol. 51, 745-751 (2013).
21. Swain, M. T. et al. A post-assembly genome-improvement toolkit (PAGIT) to obtain annotated genomes from contigs. Nat. Protoc. 7, 1260-1284 (2012).
22. Schneider, A. G. & Mercereau-Puijalon, O. A new Apicomplexa-specific protein kinase family: multiple members in Plasmodium falciparum, all with an export signature. BMC Genomics 6, 30 (2005).
23. Rovira-Graells, N. et al. Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res. 22, 925-938 (2012).
24. Spillman, N. J., Beck, J. R. & Goldberg, D. E. Protein export into malaria parasite-infected erythrocytes: mechanisms and functional consequences. Annu. Rev. Biochem. 84, 813-841 (2015).
25. Nunes, M. C., Okada, M., Scheidig-Benatar, C., Cooke, B. M. & Scherf, A. Plasmodium falciparum FIKK kinase members target distinct components of the erythrocyte membrane. PLoS ONE 5, e11747 (2010).
26. Bozdech, Z. et al. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc. Natl Acad. Sci. USA 105, 16290-16295 (2008).
27. Crosnier, C. et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480, 534-537 (2011).
28. Reddy, K. S. et al. Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proc. Natl Acad. Sci. USA 112, 1179-1184 (2015).
29. Hester, J. et al. De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes. PLoS Negl. Trop. Dis. 7, e2569 (2013).
30. Loy, D. E. et al. Genome sequencing of Plasmodium falciparum from infected Anopheles mosquitoes, in ASTMH 63rd Annual Meeting. November 3-6, 2015. New Orleans, LA, USA.
31. Rich, S. M., Licht, M. C., Hudson, R. R. & Ayala, F. J. Malaria's eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. Natl Acad. Sci. USA 95, 4425-4430 (1998).
32. Hartl, D. L. The origin of malaria: mixed messages from genetic diversity. Nat. Rev. Microbiol. 2, 15-22 (2004).
33. Chang, H. H. et al. Malaria life cycle intensifies both natural selection and random genetic drift. Proc. Natl Acad. Sci. USA 110, 20129-20134 (2013).
34. Chang, H. H. & Hartl, D. L. Recurrent bottlenecks in the malaria life cycle obscure signals of positive selection. Parasitology 142, S98-S107 (2015).
35. Prado-Martinez, J. et al. Great ape genetic diversity and population history. Nature 499, 471-475 (2013).
36. Nair, S. et al. A selective sweep driven by pyrimethamine treatment in southeast asian malaria parasites. Mol. Biol. Evol. 20, 1526-1536 (2003).
37. Volkman, S. K. et al. A genome-wide map of diversity in Plasmodium falciparum. Nat. Genet. 39, 113-119 (2007).
38. Hughes, A. L. & Verra, F. Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc. Biol. Sci. 268, 1855-1860 (2001).
39. Pacheco, M. A. et al. Timing the origin of human malarias: the lemur puzzle. BMC Evol. Biol. 11, 299 (2011).
40. Neafsey, D. E. et al. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat. Genet. 44, 1046-1050 (2012).
41. Coluzzi, M., Sabatini, A., della Torre, A., Di Deco, M. A. & Petrarca, V. A polytene chromosome analysis of the Anopheles gambiae species complex. Science 298, 1415-1418 (2002).
42. Hedrick, P. W. Population genetics of malaria resistance in humans. Heredity 107, 283-304 (2011).
43. Livingstone, F. B. Anthropological implications of sickle cell gene distribution in West Africa. Am. Anthropol. 60, 533-562 (1958).
44. Carter, R. & Mendis, K. N. Evolutionary and historical aspects of the burden of malaria. Clin. Microbiol. Rev. 15, 564-594 (2002).
45. Paget-McNicol, S. & Saul, A. Mutation rates in the dihydrofolate reductase gene of Plasmodium falciparum. Parasitology 122, 497-505 (2001).
46. Lynch, M. Evolution of the mutation rate. Trends Genet. 26, 345-352 (2010).
47. Bopp, S. E. et al. Mitotic evolution of Plasmodium falciparum shows a stable core genome but recombination in antigen families. PLoS Genet. 9, e1003293 (2013).
48. Sargeant, T. J. et al. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 7, R12 (2006).
49. Kilili, G. K. & LaCount, D. J. An erythrocyte cytoskeleton-binding motif in exported Plasmodium falciparum proteins. Eukaryot. Cell 10, 1439-1447 (2011).
50. Maier, A. G. et al. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134, 48-61 (2008).
51. Tarr, S. J., Moon, R. W., Hardege, I. & Osborne, A. R. A conserved domain targets exported PHISTb family proteins to the periphery of Plasmodium infected erythrocytes. Mol. Biochem. Parasitol. 196, 29-40 (2014).
52. Goel, S. et al. Targeted disruption of a ring-infected erythrocyte surface antigen (RESA)-like export protein gene in Plasmodium falciparum confers stable chondroitin 4-sulfate cytoadherence capacity. J. Biol. Chem. 289, 34408-34421 (2014).
53. Deitsch, K., Driskill, C. & Wellems, T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res. 29, 850-853 (2001).
54. Regev-Rudzki, N. et al. Cell-cell communication between malaria-Infected red blood cells via exosome-like vesicles. Cell 153, 1120-1133 (2013).
55. Wanaguru, M., Liu, W., Hahn, B. H., Rayner, J. C. & Wright, G. J. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc. Natl Acad. Sci. USA 110, 20735-20740 (2013).
56. Sundararaman, S. A. et al. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc. Natl Acad. Sci. USA 110, 7020-7025 (2013).
57. Delicat-Loembet, L. et al. No evidence for ape Plasmodium infections in humans in Gabon. PLoS ONE 10, e0126933 (2015).
58. Molina-Cruz, A. et al. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340, 984-987 (2013).
59. Liu, W. et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).
60. Liu, W. et al. Single genome amplification and direct amplicon sequencing of Plasmodium spp. DNA from ape fecal specimens. Protoc. Exch. http://dx.doi.org/10.1038/nprot.2010.156 (2010).
61. Crusoe, M. R. et al. The khmer software package: enabling efficient nucleotide sequence analysis. F1000Res 4, 900 (2015).
62. Carver, T., Harris, S. R., Berriman, M., Parkhill, J. & McQuillan, J. A. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28, 464-469 (2012).
63. Nadalin, F., Vezzi, F. & Policriti, A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics 13, S8 (2012).
64. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477 (2012).
65. Safonova, Y., Bankevich, A. & Pevzner, P. A. dipSPAdes: assembler for highly polymorphic diploid genomes. J. Comput. Biol. 22, 528-545 (2015).
66. Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19(Suppl 2): ii215-ii225 (2003).
67. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290 (2004).
68. Assefa, S. A. et al. estMOI: estimating multiplicity of infection using parasite deep sequencing data. Bioinformatics 30, 1292-1294 (2014).
69. 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).
70. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772-772 (2012).