Malarial parasite diversity in chimpanzees

The value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens

M. Andreína Pacheco, Michael Cranfield, Kenneth Cameron, Ananias A. Escalante

Research output: Contribution to journalArticle

44 Citations (Scopus)

Abstract

Background: Plasmodium falciparum shares its most recent common ancestor with parasites found in African apes; these species constitute the so-called Laverania clade. In this investigation, the evolutionary history of Plasmodium lineages found in chimpanzees (Pan troglodytes) was explored. Methods. Here, the remainders of 74 blood samples collected as part of the chimpanzees' routine health examinations were studied. For all positive samples with parasite lineages belonging to the Laverania clade, the complete mitochondrial genome (mtDNA), the gene encoding dihydrofolate reductase-thymidylate synthase (dhfr-ts), the chloroquine resistance transporter (Pfcrt), the circumsporozoite protein (csp), merozoite surface protein 2 (msp2), and the DBL-1 domain from var2CSA were amplified, cloned, and sequenced. Other Plasmodium species were included in the mtDNA, dhfr-ts, and csp analyses. Phylogenetic and evolutionary genetic analyses were performed, including molecular clock analyses on the mtDNA. Results/Conclusions. Nine chimpanzees were malaria positive (12.2%); four of those infections were identified as P. falciparum, two as a Plasmodium reichenowi-like parasite or Plasmodium sp., one as Plasmodium gaboni, and two as Plasmodium malariae. All P. falciparum isolates were resistant to chloroquine indicating that the chimpanzees acquired such infections from humans in recent times. Such findings, however, are not sufficient for implicating chimpanzees as an animal reservoir for P. falciparum. Timing estimates support that the Laverania clade has co-existed with hominids for a long-period of time. The proposed species P. gaboni, Plasmodium billbrayi, and Plasmodium billcollinsi are monophyletic groups supporting that they are indeed different species. An expanded CSP phylogeny is presented, including all the Laverania species and other malarial parasites. Contrasting with other Plasmodium, the Laverania csp exhibits great conservation at the central tandem repeat region. Msp2 and var2CSA, however, show extended recent polymorphism in P. falciparum that likely originated after the P. reichenowi-P. falciparum split. The accumulation of such diversity may indicate adaptation to the human host. These examples support the notion that comparative approaches among P. falciparum and its related species will be of great value in understanding the evolution of proteins that are important in parasite invasion of the human red blood cell, as well as those involved in malaria pathogenesis.

Original languageEnglish (US)
Article number328
JournalMalaria Journal
Volume12
Issue number1
DOIs
StatePublished - 2013

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Plasmodium
Pan troglodytes
Plasmodium falciparum
Parasites
Antigens
Mitochondrial DNA
Hominidae
Chloroquine
Malaria
Plasmodium malariae
Merozoites
Proteins
Tandem Repeat Sequences
Mitochondrial Genome
Phylogeny
Infection
Membrane Proteins
Erythrocytes
History
Health

Keywords

  • Antigen
  • Chimpanzee
  • Circumsporozoite protein
  • Co-evolution
  • Dihydrofolate reductase-thymidylate synthase
  • Malaria
  • Merozoite surface protein 2
  • Mitochondrion genome
  • Pan troglodytes
  • Parasite evolution
  • Plasmodium
  • Plasmodium falciparum
  • Plasmodium phylogeny
  • Var2CSA

ASJC Scopus subject areas

  • Infectious Diseases
  • Parasitology

Cite this

Malarial parasite diversity in chimpanzees : The value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. / Pacheco, M. Andreína; Cranfield, Michael; Cameron, Kenneth; Escalante, Ananias A.

In: Malaria Journal, Vol. 12, No. 1, 328, 2013.

Research output: Contribution to journalArticle

Pacheco, M. Andreína ; Cranfield, Michael ; Cameron, Kenneth ; Escalante, Ananias A. / Malarial parasite diversity in chimpanzees : The value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. In: Malaria Journal. 2013 ; Vol. 12, No. 1.
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AB - Background: Plasmodium falciparum shares its most recent common ancestor with parasites found in African apes; these species constitute the so-called Laverania clade. In this investigation, the evolutionary history of Plasmodium lineages found in chimpanzees (Pan troglodytes) was explored. Methods. Here, the remainders of 74 blood samples collected as part of the chimpanzees' routine health examinations were studied. For all positive samples with parasite lineages belonging to the Laverania clade, the complete mitochondrial genome (mtDNA), the gene encoding dihydrofolate reductase-thymidylate synthase (dhfr-ts), the chloroquine resistance transporter (Pfcrt), the circumsporozoite protein (csp), merozoite surface protein 2 (msp2), and the DBL-1 domain from var2CSA were amplified, cloned, and sequenced. Other Plasmodium species were included in the mtDNA, dhfr-ts, and csp analyses. Phylogenetic and evolutionary genetic analyses were performed, including molecular clock analyses on the mtDNA. Results/Conclusions. Nine chimpanzees were malaria positive (12.2%); four of those infections were identified as P. falciparum, two as a Plasmodium reichenowi-like parasite or Plasmodium sp., one as Plasmodium gaboni, and two as Plasmodium malariae. All P. falciparum isolates were resistant to chloroquine indicating that the chimpanzees acquired such infections from humans in recent times. Such findings, however, are not sufficient for implicating chimpanzees as an animal reservoir for P. falciparum. Timing estimates support that the Laverania clade has co-existed with hominids for a long-period of time. The proposed species P. gaboni, Plasmodium billbrayi, and Plasmodium billcollinsi are monophyletic groups supporting that they are indeed different species. An expanded CSP phylogeny is presented, including all the Laverania species and other malarial parasites. Contrasting with other Plasmodium, the Laverania csp exhibits great conservation at the central tandem repeat region. Msp2 and var2CSA, however, show extended recent polymorphism in P. falciparum that likely originated after the P. reichenowi-P. falciparum split. The accumulation of such diversity may indicate adaptation to the human host. These examples support the notion that comparative approaches among P. falciparum and its related species will be of great value in understanding the evolution of proteins that are important in parasite invasion of the human red blood cell, as well as those involved in malaria pathogenesis.

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KW - Mitochondrion genome

KW - Pan troglodytes

KW - Parasite evolution

KW - Plasmodium

KW - Plasmodium falciparum

KW - Plasmodium phylogeny

KW - Var2CSA

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