The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching
Tobias Mourier,
Denise Anete Madureira de Alvarenga,
Abhinav Kaushik,
Anielle de Pina-Costa,
Olga Douvropoulou,
Qingtian Guan,
Francisco J. Guzmán-Vega,
Sarah Forrester,
Filipe Vieira Santos de Abreu,
Cesare Bianco Júnior,
Julio Cesar de Souza Junior,
Silvia Bahadian Moreira,
Zelinda Maria Braga Hirano,
Alcides Pissinatti,
Maria de Fátima Ferreira-da-Cruz,
Ricardo Lourenço de Oliveira,
Stefan T. Arold,
Daniel C. Jeffares,
Patrícia Brasil,
Cristiana Ferreira Alves de Brito,
Richard Culleton,
Cláudio Tadeu Daniel-Ribeiro,
Arnab Pain
Affiliations
Tobias Mourier
Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Denise Anete Madureira de Alvarenga
Grupo de Pesquisa em Biologia Molecular e Imunologia da Malária, Instituto René Rachou, Fundação Oswaldo Cruz (Fiocruz)
Abhinav Kaushik
Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Anielle de Pina-Costa
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Olga Douvropoulou
Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Qingtian Guan
Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Francisco J. Guzmán-Vega
Computational Bioscience Research Center, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Sarah Forrester
Department of Biology and York Biomedical Research Institute, University of York
Filipe Vieira Santos de Abreu
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Cesare Bianco Júnior
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Julio Cesar de Souza Junior
Universidade Regional de Blumenau (FURB), Centro de Pesquisas Biológicas de Indaial (CEPESBI)/ Projeto bugio
Silvia Bahadian Moreira
Centro de Primatologia do Rio de Janeiro (CPRJ/Inea)
Zelinda Maria Braga Hirano
Universidade Regional de Blumenau (FURB), Centro de Pesquisas Biológicas de Indaial (CEPESBI)/ Projeto bugio
Alcides Pissinatti
Centro de Primatologia do Rio de Janeiro (CPRJ/Inea)
Maria de Fátima Ferreira-da-Cruz
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Ricardo Lourenço de Oliveira
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Stefan T. Arold
Computational Bioscience Research Center, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Daniel C. Jeffares
Department of Biology and York Biomedical Research Institute, University of York
Patrícia Brasil
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Cristiana Ferreira Alves de Brito
Grupo de Pesquisa em Biologia Molecular e Imunologia da Malária, Instituto René Rachou, Fundação Oswaldo Cruz (Fiocruz)
Richard Culleton
Division of Molecular Parasitology, Proteo-Science Center, Ehime University
Cláudio Tadeu Daniel-Ribeiro
Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz
Arnab Pain
Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
Abstract Background Plasmodium simium, a malaria parasite of non-human primates (NHP), was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. Results Phylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy-binding protein 1 (DBP1) and reticulocyte-binding protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. Conclusions Analysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.