The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching.


Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
01 10 2021
Historique:
received: 03 06 2021
accepted: 03 09 2021
entrez: 1 10 2021
pubmed: 2 10 2021
medline: 2 2 2022
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 34592986
doi: 10.1186/s12915-021-01139-5
pii: 10.1186/s12915-021-01139-5
pmc: PMC8485552
doi:

Substances chimiques

Carrier Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

219

Subventions

Organisme : Wellcome Seed Award in Science
ID : 208965/Z/17/Z

Informations de copyright

© 2021. The Author(s).

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Auteurs

Tobias Mourier (T)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Denise Anete Madureira de Alvarenga (DAM)

Grupo de Pesquisa em Biologia Molecular e Imunologia da Malária, Instituto René Rachou, Fundação Oswaldo Cruz (Fiocruz), Belo Horizonte, MG, 30190-009, Brazil.

Abhinav Kaushik (A)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Anielle de Pina-Costa (A)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Pesquisa Clínica em Doenças Febris Agudas, Instituto Nacional de Infectologia Evandro Chagas, Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Centro Universitário Serra dos Órgãos (UNIFESO), Teresópolis, RJ, 25964-004, Brazil.

Olga Douvropoulou (O)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Qingtian Guan (Q)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Francisco J Guzmán-Vega (FJ)

Computational Bioscience Research Center, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Sarah Forrester (S)

Department of Biology and York Biomedical Research Institute, University of York, Wentworth Way, York, YO10 5DD, UK.

Filipe Vieira Santos de Abreu (FVS)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz (IOC), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.

Cesare Bianco Júnior (CB)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Pesquisa em Malária, IOC, Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.

Julio Cesar de Souza Junior (JC)

Universidade Regional de Blumenau (FURB), Centro de Pesquisas Biológicas de Indaial (CEPESBI)/ Projeto bugio, Blumenau, Indaial, SC, Brazil.

Silvia Bahadian Moreira (SB)

Centro de Primatologia do Rio de Janeiro (CPRJ/Inea), Guapimirim, RJ, 25940-000, Brazil.

Zelinda Maria Braga Hirano (ZMB)

Universidade Regional de Blumenau (FURB), Centro de Pesquisas Biológicas de Indaial (CEPESBI)/ Projeto bugio, Blumenau, Indaial, SC, Brazil.

Alcides Pissinatti (A)

Centro de Primatologia do Rio de Janeiro (CPRJ/Inea), Guapimirim, RJ, 25940-000, Brazil.

Maria de Fátima Ferreira-da-Cruz (MF)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Pesquisa em Malária, IOC, Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.

Ricardo Lourenço de Oliveira (RL)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz (IOC), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.

Stefan T Arold (ST)

Computational Bioscience Research Center, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.
Centre de Biologie Structurale, CNRS, INSERM, Université de Montpellier, 34090, Montpellier, France.

Daniel C Jeffares (DC)

Department of Biology and York Biomedical Research Institute, University of York, Wentworth Way, York, YO10 5DD, UK.

Patrícia Brasil (P)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.
Laboratório de Pesquisa Clínica em Doenças Febris Agudas, Instituto Nacional de Infectologia Evandro Chagas, Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil.

Cristiana Ferreira Alves de Brito (CFA)

Grupo de Pesquisa em Biologia Molecular e Imunologia da Malária, Instituto René Rachou, Fundação Oswaldo Cruz (Fiocruz), Belo Horizonte, MG, 30190-009, Brazil.

Richard Culleton (R)

Division of Molecular Parasitology, Proteo-Science Center, Ehime University, Toon, Ehime, 791-0295, Japan.

Cláudio Tadeu Daniel-Ribeiro (CT)

Centro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil. malaria@fiocruz.br.
Laboratório de Pesquisa em Malária, IOC, Fiocruz, Rio de Janeiro, RJ, 21040-360, Brazil. malaria@fiocruz.br.

Arnab Pain (A)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia. arnab.pain@kaust.edu.sa.
Global Station for Zoonosis Control, Global Institution for Collaborative Research and Education (GI-CoRE), Hokkaido University, N20 W10 Kita-ku, Sapporo, Japan. arnab.pain@kaust.edu.sa.

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