Plasmodium simium: birth and evolution of a zoonotic malaria parasite species

Plasmodium simium, a parasite of platyrrhine monkeys, is known to cause human malaria outbreaks in Southeast Brazil. It has been hypothesized that, upon the introduction of Plasmodium vivax into the Americas at the time of the European colonization, the human parasite adapted to neotropical anopheli...

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Main Authors: Nathalia Rammé M. de Albuquerque, Winni A. Ladeia, Ryan J. Scalsky, Ankit Dwivedi, Thomas C. Stabler, Priscila T. Rodrigues, Thaís C. de Oliveira, Joana C. Silva, Marcelo U. Ferreira
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Language:English
Published: Cambridge University Press
Series:Parasitology
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Online Access:https://www.cambridge.org/core/product/identifier/S0031182025100310/type/journal_article
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author Nathalia Rammé M. de Albuquerque
Winni A. Ladeia
Ryan J. Scalsky
Ankit Dwivedi
Thomas C. Stabler
Priscila T. Rodrigues
Thaís C. de Oliveira
Joana C. Silva
Marcelo U. Ferreira
author_facet Nathalia Rammé M. de Albuquerque
Winni A. Ladeia
Ryan J. Scalsky
Ankit Dwivedi
Thomas C. Stabler
Priscila T. Rodrigues
Thaís C. de Oliveira
Joana C. Silva
Marcelo U. Ferreira
author_sort Nathalia Rammé M. de Albuquerque
collection DOAJ
description Plasmodium simium, a parasite of platyrrhine monkeys, is known to cause human malaria outbreaks in Southeast Brazil. It has been hypothesized that, upon the introduction of Plasmodium vivax into the Americas at the time of the European colonization, the human parasite adapted to neotropical anophelines of the Kerteszia subgenus and to local monkeys, along the Atlantic coast of Brazil, to give rise to a sister species, P. simium. Here, to obtain new insights into the origins and adaptation of P. simium to new hosts, we analysed whole-genome sequence (WGS) data from 31 P. simium isolates together with a global sequence dataset of 1086 P. vivax isolates. Population genomic analyses revealed that P. simium comprises a discrete parasite lineage with greatest genetic similarity to P. vivax populations from Latin America – especially those from the Amazon Basin of Brazil – and to ancient European P. vivax isolates, consistent with Brazil as the most likely birthplace of the species. We show that P. simium displays half the amount of nucleotide diversity of P. vivax from Latin America, as expected from its recent origin. We identified pairs of sympatric P. simium isolates from monkeys and from humans as closely related as meiotic half-siblings, revealing ongoing zoonotic transmission of P. simium. Most critically, we show that P. simium currently causes most, and possibly all, malarial infections usually attributed to P. vivax along the Serra do Mar Mountain Range of Southeast Brazil.
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spelling doaj-art-db4d7c09037949c4aa434d4e5a37cf722025-08-20T02:46:01ZengCambridge University PressParasitology0031-18201469-816111210.1017/S0031182025100310Plasmodium simium: birth and evolution of a zoonotic malaria parasite speciesNathalia Rammé M. de Albuquerque0https://orcid.org/0000-0001-7198-8026Winni A. Ladeia1Ryan J. Scalsky2Ankit Dwivedi3Thomas C. Stabler4Priscila T. Rodrigues5Thaís C. de Oliveira6https://orcid.org/0000-0002-9959-0690Joana C. Silva7Marcelo U. Ferreira8Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil Department of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USADepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, BrazilDepartment of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USADepartment of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USADepartment of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, SwitzerlandDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil Brazilian Center for Research in Energy and Materials, Campinas, SP, BrazilDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil Department of Translational Medicine, School of Medical Sciences, University of Campinas, Campinas, SP, BrazilDepartment of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, USA Global Health and Tropical Medicine (GHTM), Associate Laboratory in Translation and Innovation Towards Global Health (LA-REAL), Institute of Hygiene and Tropical Medicine, NOVA University of Lisbon, Lisbon, PortugalDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil Global Health and Tropical Medicine (GHTM), Associate Laboratory in Translation and Innovation Towards Global Health (LA-REAL), Institute of Hygiene and Tropical Medicine, NOVA University of Lisbon, Lisbon, PortugalPlasmodium simium, a parasite of platyrrhine monkeys, is known to cause human malaria outbreaks in Southeast Brazil. It has been hypothesized that, upon the introduction of Plasmodium vivax into the Americas at the time of the European colonization, the human parasite adapted to neotropical anophelines of the Kerteszia subgenus and to local monkeys, along the Atlantic coast of Brazil, to give rise to a sister species, P. simium. Here, to obtain new insights into the origins and adaptation of P. simium to new hosts, we analysed whole-genome sequence (WGS) data from 31 P. simium isolates together with a global sequence dataset of 1086 P. vivax isolates. Population genomic analyses revealed that P. simium comprises a discrete parasite lineage with greatest genetic similarity to P. vivax populations from Latin America – especially those from the Amazon Basin of Brazil – and to ancient European P. vivax isolates, consistent with Brazil as the most likely birthplace of the species. We show that P. simium displays half the amount of nucleotide diversity of P. vivax from Latin America, as expected from its recent origin. We identified pairs of sympatric P. simium isolates from monkeys and from humans as closely related as meiotic half-siblings, revealing ongoing zoonotic transmission of P. simium. Most critically, we show that P. simium currently causes most, and possibly all, malarial infections usually attributed to P. vivax along the Serra do Mar Mountain Range of Southeast Brazil.https://www.cambridge.org/core/product/identifier/S0031182025100310/type/journal_articleAtlantic forestBrazilMalariaPlasmodium simiumPlasmodium vivaxpopulation genomicszoonosis
spellingShingle Nathalia Rammé M. de Albuquerque
Winni A. Ladeia
Ryan J. Scalsky
Ankit Dwivedi
Thomas C. Stabler
Priscila T. Rodrigues
Thaís C. de Oliveira
Joana C. Silva
Marcelo U. Ferreira
Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
Parasitology
Atlantic forest
Brazil
Malaria
Plasmodium simium
Plasmodium vivax
population genomics
zoonosis
title Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
title_full Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
title_fullStr Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
title_full_unstemmed Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
title_short Plasmodium simium: birth and evolution of a zoonotic malaria parasite species
title_sort plasmodium simium birth and evolution of a zoonotic malaria parasite species
topic Atlantic forest
Brazil
Malaria
Plasmodium simium
Plasmodium vivax
population genomics
zoonosis
url https://www.cambridge.org/core/product/identifier/S0031182025100310/type/journal_article
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