Multigenomic Delineation of Plasmodium Species of the Laverania Subgenus Infecting Wild-living Chimpanzees and Gorillas

Weimin Liu, Sesh A. Sundararaman, Dorothy E. Loy, Gerald H Learn, Yingying Li, Lindsey J Plenderleith, Jean-Bosco N. Ndjango, Sheri Speede, Rebeca Atencia, Debby Cox, George M. Shaw, Ahidjo Ayouba, Martine Peeters, Julian C. Rayner, Beatrice H Hahn, Paul Sharp

Research output: Contribution to journalArticlepeer-review

Abstract

Plasmodium falciparum, the major cause of malaria morbidity and mortality worldwide, is only distantly related to other human malaria parasites, and has thus been placed in a separate subgenus, termed Laverania. Parasites morphologically similar to P. falciparum have been identified in African apes, but only one other Laverania species, P. reichenowi from chimpanzees, has been formally described. Although recent studies have pointed to the existence of additional Laverania species, their precise number and host associations remain uncertain, primarily because of limited sampling and a paucity of parasite sequences other than from mitochondrial DNA. To address this, we used limiting dilution PCR to amplify additional parasite sequences from a large number of chimpanzee and gorilla blood and fecal samples collected at two sanctuaries and 30 field sites across equatorial Africa. Phylogenetic analyses of more than 2,000 new sequences derived from the mitochondrial, nuclear and apicoplast genomes revealed six divergent and well-supported clades within the Laverania parasite group. Although two of these clades exhibited deep subdivisions in phylogenies estimated from organelle gene sequences, these sublineages were geographically defined and not present in trees from four unlinked nuclear loci. This greatly expanded sequence data set thus confirms six, and not seven or more, ape Laverania species, of which P. reichenowi, P. gaboni, and P. billcollinsi only infect chimpanzees, while P. praefalciparum, P. adleri, P. blacklocki only infect gorillas. The new sequence data also confirm the P. praefalciparum origin of human P. falciparum.
Original languageEnglish
Pages (from-to)1929-1939
Number of pages11
JournalGenome Biology and Evolution
Volume8
Issue number6
Early online date11 Jun 2016
DOIs
Publication statusE-pub ahead of print - 11 Jun 2016

Keywords

  • Laverania
  • Plasmodium parasites infecting chimpanzees and gorillas
  • cryptic Plasmodium species
  • single genome sequencing
  • P. falciparum

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