Chimpanzee Malaria Parasites Related to Plasmodium ovale in Africa

Abstract

Since the 1970's, the diversity of Plasmodium parasites in African great apes has been neglected. Surprisingly, P. reichenowi, a chimpanzee parasite, is the only such parasite to have been molecularly characterized. This parasite is closely phylogenetically related to P. falciparum, the principal cause of the greatest malaria burden in humans. Studies of malaria parasites from anthropoid primates may provide relevant phylogenetic information, improving our understanding of the origin and evolutionary history of human malaria species. In this study, we screened 130 DNA samples from chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) from Cameroon for Plasmodium infection, using cytochrome b molecular tools. Two chimpanzees from the subspecies Pan t. troglodytes presented single infections with Plasmodium strains molecularly related to the human malaria parasite P. ovale. These chimpanzee parasites and 13 human strains of P. ovale originated from a various sites in Africa and Asia were characterized using cytochrome b and cytochrome c oxidase 1 mitochondrial partial genes and nuclear ldh partial gene. Consistent with previous findings, two genetically distinct types of P. ovale, classical and variant, were observed in the human population from a variety of geographical locations. One chimpanzee Plasmodium strain was genetically identical, on all three markers tested, to variant P. ovale type. The other chimpanzee Plasmodium strain was different from P. ovale strains isolated from humans. This study provides the first evidence of possibility of natural cross-species exchange of P. ovale between humans and chimpanzees of the subspecies Pan t. troglodytes.

African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus

“…The other chimpanzee samples are very different from those in the ape cluster. Two samples (CPZcam89 and CPZcam91) are P. ovale; these are the same samples already reported (23). Another sample (CPZcam83) is similar to P. malariae.…”

“…Krief et al (30) found four bonobos also infected with P. falciparum and one bonobo infected with P. malariae. In addition, three chimpanzees are shown in Table 1 to be infected with P. ovale; one of the chimpanzees, CPZcam63, in a mixed infection (with P. reichenowi) and two more, CPZcam89 and CPZcam91, previously reported by Duval et al (23). Of these two chimpanzees, CPZcam 89 was infected with "classic" P. ovale.…”

“…Of these two chimpanzees, CPZcam 89 was infected with "classic" P. ovale. The parasites from CPZcam91 are more similar to the "variant" P. ovale strain, although somewhat different from it, which might suggest the presence of a distinct strain of P. ovale (23).…”

“…Duval et al (23) screened DNA isolated from blood samples in captivity from 113 chimpanzees and 17 gorillas from Cameroon, initially kept as pets for variable time periods and then brought to local zoos or sanctuaries or confiscated by the Ministry of Environment and Forestry. Two chimpanzees from the subspecies Pan troglodytes troglodytes presented with single infections of Plasmodium ovale, molecularly characterized by means of partial fragments from three genes, the mitochondrial genes cytochrome b and cytochrome c oxidase and the nuclear gene lactate dehydrogenase.…”

Clues to Evolution of the SERA Multigene Family in the Genus Plasmodium

“…The host range or host specificity of Plasmodium is believed to be restricted, although, primate malaria parasites generally infect multiple hosts. For example, it has been reported that, P. knowlesi and P. cynomolgi have the ability to infect a wide variety of macaques and human (Coatney et al, 1971); additionally, two human parasites P. malariae and P. ovale have been detected in chimpanzees (Hayakawa et al, 2009;Duval et al, 2009). It may be probable that duplications of Group IV SERA genes that occurred frequently in both primate parasite lineages may be associated with host range expansions.…”