Zoonotic origin of the human malaria parasite Plasmodium malariae from African apes

Lindsey J. Plenderleith (), Weimin Liu, Yingying Li, Dorothy E. Loy, Ewan Mollison, Jesse Connell, Ahidjo Ayouba, Amandine Esteban, Martine Peeters, Crickette M. Sanz, David B. Morgan, Nathan D. Wolfe, Markus Ulrich, Andreas Sachse, Sébastien Calvignac-Spencer, Fabian H. Leendertz, George M. Shaw, Beatrice H. Hahn and Paul M. Sharp ()
Additional contact information
Lindsey J. Plenderleith: Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh
Weimin Liu: University of Pennsylvania
Yingying Li: University of Pennsylvania
Dorothy E. Loy: University of Pennsylvania
Ewan Mollison: Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh
Jesse Connell: University of Pennsylvania
Ahidjo Ayouba: University of Montpellier, INSERM
Amandine Esteban: University of Montpellier, INSERM
Martine Peeters: University of Montpellier, INSERM
Crickette M. Sanz: Washington University in St. Louis
David B. Morgan: Wildlife Conservation Society, Congo Program, BP
Nathan D. Wolfe: Metabiota Inc
Markus Ulrich: Robert Koch Institute
Andreas Sachse: Robert Koch Institute
Sébastien Calvignac-Spencer: Robert Koch Institute
Fabian H. Leendertz: Robert Koch Institute
George M. Shaw: University of Pennsylvania
Beatrice H. Hahn: University of Pennsylvania
Paul M. Sharp: Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh

Nature Communications, 2022, vol. 13, issue 1, 1-12

Abstract: Abstract The human parasite Plasmodium malariae has relatives infecting African apes (Plasmodium rodhaini) and New World monkeys (Plasmodium brasilianum), but its origins remain unknown. Using a novel approach to characterise P. malariae-related sequences in wild and captive African apes, we found that this group comprises three distinct lineages, one of which represents a previously unknown, highly divergent species infecting chimpanzees, bonobos and gorillas across central Africa. A second ape-derived lineage is much more closely related to the third, human-infective lineage P. malariae, but exhibits little evidence of genetic exchange with it, and so likely represents a separate species. Moreover, the levels and nature of genetic polymorphisms in P. malariae indicate that it resulted from the zoonotic transmission of an African ape parasite, reminiscent of the origin of P. falciparum. In contrast, P. brasilianum falls within the radiation of human P. malariae, and thus reflects a recent anthroponosis.

Date: 2022
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DOI: 10.1038/s41467-022-29306-4

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