Plasmodium simium: Population Genomics Reveals the Origin of a Reverse Zoonosis.

Thaís C de Oliveira, Priscila T Rodrigues, Angela M Early, Ana Maria R C Duarte, Julyana C Buery, Marina G Bueno, José L Catão-Dias, Crispim Cerutti, Luísa D P Rona, Daniel E Neafsey, Marcelo U Ferreira
Author Information
  1. Thaís C de Oliveira: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
  2. Priscila T Rodrigues: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
  3. Angela M Early: Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.
  4. Ana Maria R C Duarte: Laboratory of Biochemistry and Molecular Biology, Superintendency for the Control of Endemics (SUCEN), State Secretary of Health, São Paulo, Brazil.
  5. Julyana C Buery: Department of Social Medicine, Center for Health Sciences, Federal University of Espírito Santo, Vitória, Brazil.
  6. Marina G Bueno: Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil.
  7. José L Catão-Dias: Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil.
  8. Crispim Cerutti: Department of Social Medicine, Center for Health Sciences, Federal University of Espírito Santo, Vitória, Brazil.
  9. Luísa D P Rona: Department of Cell Biology, Embryology, and Genetics, Federal University of Santa Catarina, Florianópolis, Brazil.
  10. Daniel E Neafsey: Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.
  11. Marcelo U Ferreira: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. ORCID

Abstract

BACKGROUND: The population history of Plasmodium simium, which causes malaria in sylvatic Neotropical monkeys and humans along the Atlantic Coast of Brazil, remains disputed. Genetically diverse P vivax populations from various sources, including the lineages that founded the species P simium, are thought to have arrived in the Americas in separate migratory waves.
METHODS: We use population genomic approaches to investigate the origin and evolution of P simium.
RESULTS: We find a minimal genome-level differentiation between P simium and present-day New World P vivax isolates, consistent with their common geographic origin and subsequent divergence on this continent. The meagre genetic diversity in P simium samples from humans and monkeys implies a recent transfer from humans to non-human primates - a unique example of malaria as a reverse zoonosis of public health significance. Likely genomic signatures of P simium adaptation to new hosts include the deletion of >40% of a key erythrocyte invasion ligand, PvRBP2a, which may have favored more efficient simian host cell infection.
CONCLUSIONS: New World P vivax lineages that switched from humans to platyrrhine monkeys founded the P simium population that infects nonhuman primates and feeds sustained human malaria transmission in the outskirts of major cities.

Keywords

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Grants

  1. /Wellcome Trust
  2. U19 AI110818/NIAID NIH HHS
  3. 207486/Z/17/Z/Wellcome Trust

MeSH Term

Animals
Bacterial Zoonoses
Brazil
Haplorhini
Malaria
Metagenomics
Monkey Diseases
Plasmodium
Plasmodium vivax
Polymerase Chain Reaction
Polymorphism, Single Nucleotide

Word Cloud

Created with Highcharts 10.0.0PsimiummonkeyshumanspopulationPlasmodiummalariavivaxNeotropicallineagesfoundedgenomicoriginNewWorldprimatesreversezoonosisBACKGROUND:historycausessylvaticalongAtlanticCoastBrazilremainsdisputedGeneticallydiversepopulationsvarioussourcesincludingspeciesthoughtarrivedAmericasseparatemigratorywavesMETHODS:useapproachesinvestigateevolutionRESULTS:findminimalgenome-leveldifferentiationpresent-dayisolatesconsistentcommongeographicsubsequentdivergencecontinentmeagregeneticdiversitysamplesimpliesrecenttransfernon-human-uniqueexamplepublichealthsignificanceLikelysignaturesadaptationnewhostsincludedeletion>40%keyerythrocyteinvasionligandPvRBP2amayfavoredefficientsimianhostcellinfectionCONCLUSIONS:switchedplatyrrhineinfectsnonhumanfeedssustainedhumantransmissionoutskirtsmajorcitiessimium:PopulationGenomicsRevealsOriginReverseZoonosis

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