African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum

Abstract

Plasmodium reichenowi, a chimpanzee parasite, was until very recently the only known close relative of Plasmodium falciparum, the most virulent agent of human malaria. Recently, Plasmodium gaboni, another closely related chimpanzee parasite, was discovered, suggesting that the diversity of Plasmodium circulating in great apes in Africa might have been underestimated. It was also recently shown that P. reichenowi is a geographically widespread and genetically diverse chimpanzee parasite and that the world diversity of P. falciparum is fully included within the much broader genetic diversity of P. reichenowi. The evidence indicates that all extant populations of P. falciparum originated from P. reichenowi, likely by a single transfer from chimpanzees. In this work, we have studied the diversity of Plasmodium species infecting chimpanzees and gorillas in Central Africa (Cameroon and Gabon) from both wild-living and captive animals. The studies in wild apes used noninvasive sampling methods. We confirm the presence of P. reichenowi and P. gaboni in wild chimpanzees. Moreover, our results reveal the existence of an unexpected genetic diversity of Plasmodium lineages circulating in gorillas. We show that gorillas are naturally infected by two related lineages of parasites that have not been described previously, herein referred to as Plasmodium GorA and P. GorB, but also by P. falciparum, a species previously considered as strictly human specific. The continuously increasing contacts between humans and primate populations raise concerns about further reciprocal host transfers of these pathogens.

Fig. 1.

Phylogenetic relationships among Plasmodium species. (A) Before: Cytochrome b phylogeny based on gene sequences available before 2009. Only two species, P. falciparum, parasitic to humans, and P. reichenowi, parasitic to chimpanzees, were known within the clade that includes humans and the great apes (above). (B) This study: Phylogeny that includes the sequences obtained in our study. Three additional species are shown: P. gaboni, which infects chimpanzees (5), and P. GorA and P. GorB, which infect gorillas. Moreover, P. falciparum is shown to infect gorillas in addition to humans. The phylograms were constructed using a maximum-likelihood method from partial Cyt b sequence data (704 nucleotides). Bootstrap values are shown for the nodes inside the African great apes/human clade. (Scale bar, 0.03 substitutions per site.) cpm: Cheek-Push monkeys.

Fig. 2.

Location of the wild chimpanzee and gorilla populations in Cameroon. The Sanaga River defines the boundary between P. t. troglodytes in the south and P. t. vellerosus in the north. G. g. gorilla is found in the south of Cameroon and G. g. diehli in the northwest of Cameroon at the border with Nigeria. BQ, CP, DP, MB, MF, MG, MP, TK: Sites of chimpanzee and gorilla feces collection (more details in Table S1).

Fig. 3.

Phylogeny of Plasmodium species including our samples and those from Rich et al. (4), i.e., “reichenowi_isolate.” This phylogram was constructed using maximum likelihood from partial Cyt b sequence data (i.e., 350 nucleotides shared between the two studies). Bootstrap values were obtained using 100 iterations. (Scale bar, 0.05 substitutions per site.) P. reichenowi* corresponds to the reference GenBank sequence (Table S2).