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Volume 26, Number 8—August 2020
Research

Population Genomic Structure and Recent Evolution of Plasmodium knowlesi, Peninsular Malaysia

Suzanne E. Hocking, Paul C.S. Divis, Khamisah A. Kadir, Balbir Singh, and David J. ConwayComments to Author 
Author affiliations: London School of Hygiene and Tropical Medicine Department of Infection Biology, London, UK (S.E. Hocking, D.J. Conway); Universiti Sarawak Malaysia Malaria Research Centre, Kota Samarahan, Malaysia (P.C.S. Divis, K.A. Kadir, B. Singh, D.J. Conway)

Main Article

Figure 2

Genomewide analysis of diversity in Plasmodium knowlesi clinical samples from Peninsular Malaysia compared with samples from elsewhere. A) Neighbor-joining tree based on a pairwise genetic distance matrix between individual P. knowlesi infection samples for the 28 new clinical samples from Peninsular Malaysia (shown in red), 5 previously sequenced laboratory isolates (shown in orange), most of which were originally isolated from Peninsular Malaysia many years ago (15), and 74 samples from Malays

Figure 2. Genomewide analysis of diversity in Plasmodium knowlesi clinical samples from Peninsular Malaysia compared with samples from elsewhere. A) Neighbor-joining tree based on a pairwise genetic distance matrix between individual P. knowlesi infection samples for the 28 new clinical samples from Peninsular Malaysia (shown in red), 5 previously sequenced laboratory isolates (shown in orange), most of which were originally isolated from Peninsular Malaysia many years ago (15), and 74 samples from Malaysian Borneo that grouped into separate subpopulation clusters (cluster 1 shown in blue, cluster 2 in green) (15,16,23). All the clinical isolate samples from Peninsular Malaysia grouped into cluster 3 together with the laboratory isolates. The distance matrix is based on the proportion of all single-nucleotide polymorphisms (SNPs) showing differences between each infection sample (scale bar shows branch length for 0.5% of SNPs differing); most reads within each infection sample determine the allele scored for each SNP. B) Genomewide scan of nucleotide diversity (π) for P. knowlesi among the clinical isolates in Peninsular Malaysia (cluster 3, shown in red), compared with diversity observed in the subpopulations in Malaysian Borneo (clusters 1 and 2). The sliding window plot shows values of nucleotide diversity for nonoverlapping windows of 50 kb in each of the 14 chromosomes.

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References
  1. Liu  W, Li  Y, Learn  GH, Rudicell  RS, Robertson  JD, Keele  BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420–5. DOIPubMedGoogle Scholar
  2. Loy  DE, Plenderleith  LJ, Sundararaman  SA, Liu  W, Gruszczyk  J, Chen  YJ, et al. Evolutionary history of human Plasmodium vivax revealed by genome-wide analyses of related ape parasites. Proc Natl Acad Sci U S A. 2018;115:E8450–9. DOIPubMedGoogle Scholar
  3. Rutledge  GG, Böhme  U, Sanders  M, Reid  AJ, Cotton  JA, Maiga-Ascofare  O, et al. Plasmodium malariae and P. ovale genomes provide insights into malaria parasite evolution. Nature. 2017;542:101–4. DOIPubMedGoogle Scholar
  4. WHO. World malaria report 2018 [cited 2019 Jun 13]. https://www.who.int/malaria/publications/world-malaria-report-2018
  5. Cox-Singh  J, Davis  TM, Lee  KS, Shamsul  SS, Matusop  A, Ratnam  S, et al. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis. 2008;46:165–71. DOIPubMedGoogle Scholar
  6. Singh  B, Kim Sung  L, Matusop  A, Radhakrishnan  A, Shamsul  SS, Cox-Singh  J, et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004;363:1017–24. DOIPubMedGoogle Scholar
  7. Shearer  FM, Huang  Z, Weiss  DJ, Wiebe  A, Gibson  HS, Battle  KE, et al. Estimating geographical variation in the risk of zoonotic Plasmodium knowlesi infection in countries eliminating malaria. PLoS Negl Trop Dis. 2016;10:e0004915. DOIPubMedGoogle Scholar
  8. Singh  B, Daneshvar  C. Human infections and detection of Plasmodium knowlesi. Clin Microbiol Rev. 2013;26:165–84. DOIPubMedGoogle Scholar
  9. William  T, Jelip  J, Menon  J, Anderios  F, Mohammad  R, Awang Mohammad  TA, et al. Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi. Malar J. 2014;13:390. DOIPubMedGoogle Scholar
  10. Cooper  DJ, Rajahram  GS, William  T, Jelip  J, Mohammad  R, Benedict  J, et al. Plasmodium knowlesi malaria in Sabah, Malaysia, 2015–2017: ongoing increase in incidence despite near-elimination of the human-only Plasmodium species. Clin Infect Dis. 2020;70:361–7.PubMedGoogle Scholar
  11. Lapp  SA, Geraldo  JA, Chien  JT, Ay  F, Pakala  SB, Batugedara  G, et al. MaHPIC consortium. PacBiol assembly of a Plasmodium knowlesi genome sequence with Hi-C correction and manual annotation of the SICAvar gene family. Parasitology. 2018;145:71–84. DOIPubMedGoogle Scholar
  12. Pain  A, Böhme  U, Berry  AE, Mungall  K, Finn  RD, Jackson  AP, et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature. 2008;455:799–803. DOIPubMedGoogle Scholar
  13. Divis  PC, Lin  LC, Rovie-Ryan  JJ, Kadir  KA, Anderios  F, Hisam  S, et al. Three divergent subpopulations of the malaria parasite Plasmodium knowlesi. Emerg Infect Dis. 2017;23:616–24. DOIPubMedGoogle Scholar
  14. Divis  PC, Singh  B, Anderios  F, Hisam  S, Matusop  A, Kocken  CH, et al. Admixture in humans of two divergent Plasmodium knowlesi populations associated with different macaque host species. PLoS Pathog. 2015;11:e1004888. DOIPubMedGoogle Scholar
  15. Assefa  S, Lim  C, Preston  MD, Duffy  CW, Nair  MB, Adroub  SA, et al. Population genomic structure and adaptation in the zoonotic malaria parasite Plasmodium knowlesi. Proc Natl Acad Sci U S A. 2015;112:13027–32. DOIPubMedGoogle Scholar
  16. Divis  PCS, Duffy  CW, Kadir  KA, Singh  B, Conway  DJ. Genome-wide mosaicism in divergence between zoonotic malaria parasite subpopulations with separate sympatric transmission cycles. Mol Ecol. 2018;27:860–70. DOIPubMedGoogle Scholar
  17. Yusof  R, Ahmed  MA, Jelip  J, Ngian  HU, Mustakim  S, Hussin  HM, et al. Phylogeographic evidence for 2 genetically distinct zoonotic Plasmodium knowlesi parasites, Malaysia. Emerg Infect Dis. 2016;22:1371–80. DOIPubMedGoogle Scholar
  18. Coatney  GR, Collins  WE, McWilson  W, Contacos  PG. The primate malarias. Atlanta: US Department of Health and Human Services; 1971.
  19. Moon  RW, Hall  J, Rangkuti  F, Ho  YS, Almond  N, Mitchell  GH, et al. Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proc Natl Acad Sci U S A. 2013;110:531–6. DOIPubMedGoogle Scholar
  20. Lim  C, Hansen  E, DeSimone  TM, Moreno  Y, Junker  K, Bei  A, et al. Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans. Nat Commun. 2013;4:1638. DOIPubMedGoogle Scholar
  21. Moon  RW, Sharaf  H, Hastings  CH, Ho  YS, Nair  MB, Rchiad  Z, et al. Normocyte-binding protein required for human erythrocyte invasion by the zoonotic malaria parasite Plasmodium knowlesi. Proc Natl Acad Sci U S A. 2016;113:7231–6. DOIPubMedGoogle Scholar
  22. Lee  KS, Divis  PC, Zakaria  SK, Matusop  A, Julin  RA, Conway  DJ, et al. Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog. 2011;7:e1002015. DOIPubMedGoogle Scholar
  23. Pinheiro  MM, Ahmed  MA, Millar  SB, Sanderson  T, Otto  TD, Lu  WC, et al. Plasmodium knowlesi genome sequences from clinical isolates reveal extensive genomic dimorphism. PLoS One. 2015;10:e0121303. DOIPubMedGoogle Scholar
  24. Duffy  CW, Amambua-Ngwa  A, Ahouidi  AD, Diakite  M, Awandare  GA, Ba  H, et al. Multi-population genomic analysis of malaria parasites indicates local selection and differentiation at the gdv1 locus regulating sexual development. Sci Rep. 2018;8:15763. DOIPubMedGoogle Scholar
  25. Jombart  T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5. DOIPubMedGoogle Scholar
  26. Paradis  E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26:419–20. DOIPubMedGoogle Scholar
  27. Pfeifer  B, Wittelsbürger  U, Ramos-Onsins  SE, Lercher  MJ. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol. 2014;31:1929–36. DOIPubMedGoogle Scholar
  28. Gautier  M, Vitalis  R. rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics. 2012;28:1176–7. DOIPubMedGoogle Scholar
  29. Sallum  MA, Peyton  EL, Wilkerson  RC. Six new species of the Anopheles leucosphyrus group, reinterpretation of An. elegans and vector implications. Med Vet Entomol. 2005;19:158–99. DOIPubMedGoogle Scholar
  30. Vythilingam  I, Wong  ML, Wan-Yussof  WS. Current status of Plasmodium knowlesi vectors: a public health concern? Parasitology. 2018;145:32–40. DOIPubMedGoogle Scholar
  31. Moyes  CL, Shearer  FM, Huang  Z, Wiebe  A, Gibson  HS, Nijman  V, et al. Predicting the geographical distributions of the macaque hosts and mosquito vectors of Plasmodium knowlesi malaria in forested and non-forested areas. Parasit Vectors. 2016;9:242. DOIPubMedGoogle Scholar
  32. Sinka  ME, Bangs  MJ, Manguin  S, Chareonviriyaphap  T, Patil  AP, Temperley  WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011;4:89. DOIPubMedGoogle Scholar
  33. Jiram  AI, Vythilingam  I, NoorAzian  YM, Yusof  YM, Azahari  AH, Fong  MY. Entomologic investigation of Plasmodium knowlesi vectors in Kuala Lipis, Pahang, Malaysia. Malar J. 2012;11:213. DOIPubMedGoogle Scholar
  34. Vythilingam  I, Lim  YA, Venugopalan  B, Ngui  R, Leong  CS, Wong  ML, et al. Plasmodium knowlesi malaria an emerging public health problem in Hulu Selangor, Selangor, Malaysia (2009-2013): epidemiologic and entomologic analysis. Parasit Vectors. 2014;7:436. DOIPubMedGoogle Scholar
  35. Vythilingam  I, Noorazian  YM, Huat  TC, Jiram  AI, Yusri  YM, Azahari  AH, et al. Plasmodium knowlesi in humans, macaques and mosquitoes in peninsular Malaysia. Parasit Vectors. 2008;1:26. DOIPubMedGoogle Scholar
  36. Wong  ML, Ahmed  MA, Sulaiman  WYW, Manin  BO, Leong  CS, Quan  FS, et al. Genetic diversity of zoonotic malaria parasites from mosquito vector and vertebrate hosts. Infect Genet Evol. 2019;73:26–32. DOIPubMedGoogle Scholar
  37. Anthony  TG, Conway  DJ, Cox-Singh  J, Matusop  A, Ratnam  S, Shamsul  S, et al. Fragmented population structure of plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005;191:1558–64. DOIPubMedGoogle Scholar
  38. 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. DOIPubMedGoogle Scholar
  39. Miotto  O, Almagro-Garcia  J, Manske  M, Macinnis  B, Campino  S, Rockett  KA, et al. Multiple populations of artemisinin-resistant Plasmodium falciparum in Cambodia. Nat Genet. 2013;45:648–55. DOIPubMedGoogle Scholar
  40. Herdiana  H, Irnawati  I, Coutrier  FN, Munthe  A, Mardiati  M, Yuniarti  T, et al. Two clusters of Plasmodium knowlesi cases in a malaria elimination area, Sabang Municipality, Aceh, Indonesia. Malar J. 2018;17:186. DOIPubMedGoogle Scholar
  41. Imwong  M, Madmanee  W, Suwannasin  K, Kunasol  C, Peto  TJ, Tripura  R, et al. Asymptomatic natural human infections with the simian malaria parasites Plasmodium cynomolgi and Plasmodium knowlesi. J Infect Dis. 2019;219:695–702. DOIPubMedGoogle Scholar

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