Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus

ABSTRACT Plasmodium falciparum, the major cause of malaria morbidity and mortality in humans, has been shown to have emerged after cross-species transmission of one of six host-specific parasites (subgenus Laverania) infecting wild chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla)...

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Autores principales:	Lindsey J. Plenderleith, Weimin Liu, Oscar A. MacLean, Yingying Li, Dorothy E. Loy, Sesh A. Sundararaman, Frederic Bibollet-Ruche, Gerald H. Learn, Beatrice H. Hahn, Paul M. Sharp
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Laverania Plasmodium falciparum RH5 basigin chimpanzee gorilla Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/72968de674554b908ed14642623310d4
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spelling	oai:doaj.org-article:72968de674554b908ed14642623310d42021-11-15T15:53:26ZAdaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus10.1128/mBio.02237-172150-7511https://doaj.org/article/72968de674554b908ed14642623310d42018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02237-17https://doaj.org/toc/2150-7511ABSTRACT Plasmodium falciparum, the major cause of malaria morbidity and mortality in humans, has been shown to have emerged after cross-species transmission of one of six host-specific parasites (subgenus Laverania) infecting wild chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla). Binding of the parasite-encoded ligand RH5 to the host protein basigin is essential for erythrocyte invasion and has been implicated in host specificity. A recent study claimed to have found two amino acid changes in RH5 that “drove the host shift leading to the emergence of P. falciparum as a human pathogen.” However, the ape Laverania data available at that time, which included only a single distantly related chimpanzee parasite sequence, were inadequate to justify any such conclusion. Here, we have investigated Laverania Rh5 gene evolution using sequences from all six ape parasite species. Searching for gene-wide episodic selection across the entire Laverania phylogeny, we found eight codons to be under positive selection, including three that correspond to contact residues known to form hydrogen bonds between P. falciparum RH5 and human basigin. One of these sites (residue 197) has changed subsequent to the transmission from apes to humans that gave rise to P. falciparum, suggesting a possible role in the adaptation of the gorilla parasite to the human host. We also found evidence that the patterns of nucleotide polymorphisms in P. falciparum are not typical of Laverania species and likely reflect the recent demographic history of the human parasite. IMPORTANCE A number of closely related, host-specific malaria parasites infecting wild chimpanzees and gorillas have recently been described. The most important cause of human malaria, Plasmodium falciparum, is now known to have resulted from a cross-species transmission of one of the gorilla parasites. Overcoming species-specific interactions between a parasite ligand, RH5, and its receptor on host cells, basigin, was likely an important step in the origin of the human parasite. We have investigated the evolution of the Rh5 gene and found evidence of adaptive changes during the diversification of the ape parasite species at sites that are known to form bonds with human basigin. One of these changes occurred at the origin of P. falciparum, implicating it as an important adaptation to the human host.Lindsey J. PlenderleithWeimin LiuOscar A. MacLeanYingying LiDorothy E. LoySesh A. SundararamanFrederic Bibollet-RucheGerald H. LearnBeatrice H. HahnPaul M. SharpAmerican Society for MicrobiologyarticleLaveraniaPlasmodium falciparumRH5basiginchimpanzeegorillaMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Laverania Plasmodium falciparum RH5 basigin chimpanzee gorilla Microbiology QR1-502
spellingShingle	Laverania Plasmodium falciparum RH5 basigin chimpanzee gorilla Microbiology QR1-502 Lindsey J. Plenderleith Weimin Liu Oscar A. MacLean Yingying Li Dorothy E. Loy Sesh A. Sundararaman Frederic Bibollet-Ruche Gerald H. Learn Beatrice H. Hahn Paul M. Sharp Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
description	ABSTRACT Plasmodium falciparum, the major cause of malaria morbidity and mortality in humans, has been shown to have emerged after cross-species transmission of one of six host-specific parasites (subgenus Laverania) infecting wild chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla). Binding of the parasite-encoded ligand RH5 to the host protein basigin is essential for erythrocyte invasion and has been implicated in host specificity. A recent study claimed to have found two amino acid changes in RH5 that “drove the host shift leading to the emergence of P. falciparum as a human pathogen.” However, the ape Laverania data available at that time, which included only a single distantly related chimpanzee parasite sequence, were inadequate to justify any such conclusion. Here, we have investigated Laverania Rh5 gene evolution using sequences from all six ape parasite species. Searching for gene-wide episodic selection across the entire Laverania phylogeny, we found eight codons to be under positive selection, including three that correspond to contact residues known to form hydrogen bonds between P. falciparum RH5 and human basigin. One of these sites (residue 197) has changed subsequent to the transmission from apes to humans that gave rise to P. falciparum, suggesting a possible role in the adaptation of the gorilla parasite to the human host. We also found evidence that the patterns of nucleotide polymorphisms in P. falciparum are not typical of Laverania species and likely reflect the recent demographic history of the human parasite. IMPORTANCE A number of closely related, host-specific malaria parasites infecting wild chimpanzees and gorillas have recently been described. The most important cause of human malaria, Plasmodium falciparum, is now known to have resulted from a cross-species transmission of one of the gorilla parasites. Overcoming species-specific interactions between a parasite ligand, RH5, and its receptor on host cells, basigin, was likely an important step in the origin of the human parasite. We have investigated the evolution of the Rh5 gene and found evidence of adaptive changes during the diversification of the ape parasite species at sites that are known to form bonds with human basigin. One of these changes occurred at the origin of P. falciparum, implicating it as an important adaptation to the human host.
format	article
author	Lindsey J. Plenderleith Weimin Liu Oscar A. MacLean Yingying Li Dorothy E. Loy Sesh A. Sundararaman Frederic Bibollet-Ruche Gerald H. Learn Beatrice H. Hahn Paul M. Sharp
author_facet	Lindsey J. Plenderleith Weimin Liu Oscar A. MacLean Yingying Li Dorothy E. Loy Sesh A. Sundararaman Frederic Bibollet-Ruche Gerald H. Learn Beatrice H. Hahn Paul M. Sharp
author_sort	Lindsey J. Plenderleith
title	Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
title_short	Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
title_full	Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
title_fullStr	Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
title_full_unstemmed	Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus
title_sort	adaptive evolution of rh5 in ape <italic toggle="yes">plasmodium</italic> species of the <italic toggle="yes">laverania</italic> subgenus
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/72968de674554b908ed14642623310d4
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Adaptive Evolution of RH5 in Ape <italic toggle="yes">Plasmodium</italic> species of the <italic toggle="yes">Laverania</italic> Subgenus

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