Origin of the human malaria parasite Plasmodium falciparum in gorillas

Abstract

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here, we used single genome amplification (SGA) strategies to show that wild-living African apes are naturally infected with at least nine Plasmodium species, including one that is the direct precursor of P.falciparum. Among nearly 3,000 ape fecal specimens collected from 57 field sites throughout central Africa, we found Plasmodium spp. infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Panpaniscus). Ape plasmodial infections were highly prevalent, widely distributed, and almost always made up of mixed parasite species. To obtain Plasmodium sequences not confounded by in vitro recombination, we used SGA to amplify fragments of the mitochondrial (956bp of the cytochrome b gene; 3.4kb and 3.3kb half-genome fragments), apicoplast (390bp of the caseinolytic protease C gene) and nuclear (772bp of the lactate dehydrogenase gene) genomes. Among more than 1,100 such sequences from 80 chimpanzee and 55 gorilla samples, we found nine that were related to P. malariae, P. ovale or P. vivax. All others grouped within one of six chimpanzee-or gorilla-specific lineages representing distinct Plasmodium species within the Laverania subgenus. One of these from western gorillas was comprised of parasites that were nearly identical to P. falciparum. In phylogenetic trees of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin, and that all known human strains appear to have resulted from a single cross-species transmission event.

Genome sequences reveal divergence times of malaria parasite lineages

“…In Fig. 4, we represent schematically the portion of Liu et al .’s (2010, p. 422) cytochrome b phylogeny that concerns the subgenus Laverania , to which P. falciparum and P. reichenowi belong. In this rooted phylogenetic tree, P. falciparum and P. reichenowi form part of a clade within Laverania , most members of which are found in Pan (the genus including the two extant chimpanzee species; Fig.…”

“…Indeed ape infections with P. falciparum may be very recent phenomena, occurring only as a result of forest destruction that has brought human and ape populations into greater proximity (Harcourt, 1981; Struhsaker, 1981; Morgan et al 2006). The claim that ape-derived malaria infections may be common in humans (Duval et al 2010; Liu et al 2010) is premature and may have unfortunate consequences for great ape survival. The African great apes are subject to numerous threats (Caldecott and Miles, 2005), and the Western gorilla ( Gorilla gorilla ) is listed as critically endangered (Hopkin, 2007).…”

Biochemical Characterization of the Interaction between the Extracellular Domain of a P. falciparum Invasion Ligand and Its Red Blood Cell Receptor♦

“…parasites to their natural hosts is therefore warranted, and this will be facilitated by the ability to express the entire ectodomain of EBA175 in an active form. This is of topical interest due to the recent discovery of new Plasmodium species that infect gorillas and that are the closest known relatives of P. falciparum (40,41).…”

Wild great apes as sentinels and sources of infectious disease

“…Various malarial parasites infect chimpanzees and gorillas [46][47][48]. Various malarial parasites infect chimpanzees and gorillas [46][47][48].…”

“…This contrasts with frequent reports of great ape SFV and STLV-1 transmission to humans (notably in high-risk populations such as great ape-bitten hunters; reviewed in [50]). Obviously, prevalence is not the only determining parameter, as shown by the example of plasmodia, which are highly prevalent in great apes but were apparently only transmitted once to humans, giving rise to Plasmodium falciparum [47]. For example, transmission of great ape SIVs, which are found at only a low prevalence, with few communities infected [51], to humans appears to be exceptionally rare [8].…”