Multigenomic Delineation of Plasmodium Species of the Laverania Subgenus Infecting Wild-Living Chimpanzees and Gorillas.
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, Plasmodium 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 polymerase chain reaction 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, Plasmodium gaboni, and Plasmodium billcollinsi only infect chimpanzees, whereas Plasmodium praefalciparum, Plasmodium adleri, and Pladmodium blacklocki only infect gorillas. The new sequence data also confirm the P. praefalciparum origin of human P. falciparum.
Department of Medicine, Perelman School of Medicine, University of Pennsylvania.
Weimin
W
Liu
Department of Medicine, Perelman School of Medicine, University of Pennsylvania Department of Microbiology, Perelman School of Medicine, University of Pennsylvania.
Sesh A
SA
Sundararaman
Department of Medicine, Perelman School of Medicine, University of Pennsylvania Department of Microbiology, Perelman School of Medicine, University of Pennsylvania.
Dorothy E
DE
Loy
Department of Medicine, Perelman School of Medicine, University of Pennsylvania.
Gerald H
GH
Learn
Department of Medicine, Perelman School of Medicine, University of Pennsylvania.
Yingying
Y
Li
Institute of Evolutionary Biology, and Centre for Immunity, Infection and Evolution, University of Edinburgh, United Kingdom.
Lindsey J
LJ
Plenderleith
Faculty of Sciences, University of Kisangani, Democratic Republic of the Congo.
Jean-Bosco N
JB
Ndjango
Sanaga-Yong Chimpanzee Rescue Center, IDA-Africa, Portland, Oregon.
Sheri
S
Speede
Tchimpounga Chimpanzee Rehabilitation Center, Pointe-Noire, Republic of the Congo.
Rebeca
R
Atencia
Tchimpounga Chimpanzee Rehabilitation Center, Pointe-Noire, Republic of the Congo Africa Programmes, Jane Goodall Institute, Vienna, Virginia.
Debby
D
Cox
Department of Medicine, Perelman School of Medicine, University of Pennsylvania Department of Microbiology, Perelman School of Medicine, University of Pennsylvania.
George M
GM
Shaw
UMI 233, Institut de Recherche pour le Développement (IRD), INSERM U1175, and University of Montpellier, France.
Ahidjo
A
Ayouba
UMI 233, Institut de Recherche pour le Développement (IRD), INSERM U1175, and University of Montpellier, France.
Martine
M
Peeters
Malaria Programme, Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, UK.
Julian C
JC
Rayner
Department of Medicine, Perelman School of Medicine, University of Pennsylvania Department of Microbiology, Perelman School of Medicine, University of Pennsylvania.
Beatrice H
BH
Hahn
Institute of Evolutionary Biology, and Centre for Immunity, Infection and Evolution, University of Edinburgh, United Kingdom paul.sharp@ed.ac.uk.
Paul M
PM
Sharp
D000349:Africa; D000818:Animals; D004272:DNA, Mitochondrial / Q000235:genetics; D019143:Evolution, Molecular; D005243:Feces / Q000469:parasitology; D006071:Gorilla gorilla / Q000235:genetics / Q000469:parasitology; D006801:Humans; D016778:Malaria, Falciparum / Q000145:classification / Q000235:genetics* / Q000469:parasitology; D002679:Pan troglodytes / Q000235:genetics / Q000469:parasitology; D010802:Phylogeny; D010963:Plasmodium falciparum / Q000145:classification / Q000235:genetics* / Q000472:pathogenicity; D017422:Sequence Analysis, DNA
D004272:DNA, Mitochondrial
Laverania; P. falciparum; Plasmodium parasites infecting chimpanzees and gorillas; cryptic Plasmodium species; single genome sequencing