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Single-cell analyses of polyclonal Plasmodium vivax infections and their consequences on parasite transmission

Author

Listed:
  • Brittany Hazzard

    (University of Maryland School of Medicine)

  • Juliana M. Sá

    (National Institutes of Health)

  • Haikel N. Bogale

    (University of Maryland School of Medicine)

  • Tales V. Pascini

    (National Institutes of Health)

  • Angela C. Ellis

    (National Institutes of Health)

  • Shuchi Amin

    (National Institutes of Health)

  • Jennifer S. Armistead

    (National Institutes of Health
    University of South Florida)

  • John H. Adams

    (University of South Florida)

  • Thomas E. Wellems

    (National Institutes of Health)

  • David Serre

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

Abstract

Most Plasmodium vivax infections contain genetically distinct parasites, but the consequences of this polyclonality on the development of asexual parasites, their sexual differentiation, and their transmission remain unknown. We describe infections of Saimiri monkeys with two strains of P. vivax and the analyses of 80,024 parasites characterized by single cell RNA sequencing and individually genotyped. In our model, consecutive inoculations fail to establish polyclonal infections. By contrast, simultaneous inoculations of two strains lead to sustained polyclonal infections, although without detectable differences in parasite regulation or sexual commitment. Analyses of sporozoites dissected from mosquitoes fed on coinfected monkeys show that all genotypes are successfully transmitted to mosquitoes. However, after sporozoite inoculation, not all genotypes contribute to the subsequent blood infections, highlighting an important bottleneck during pre-erythrocytic development. Overall, these studies provide new insights on the mechanisms regulating the establishment of polyclonal P. vivax infections and their consequences for disease transmission.

Suggested Citation

  • Brittany Hazzard & Juliana M. Sá & Haikel N. Bogale & Tales V. Pascini & Angela C. Ellis & Shuchi Amin & Jennifer S. Armistead & John H. Adams & Thomas E. Wellems & David Serre, 2024. "Single-cell analyses of polyclonal Plasmodium vivax infections and their consequences on parasite transmission," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51949-8
    DOI: 10.1038/s41467-024-51949-8
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    1. Adam Kim & Jean Popovici & Didier Menard & David Serre, 2019. "Plasmodium vivax transcriptomes reveal stage-specific chloroquine response and differential regulation of male and female gametocytes," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    2. Asaf Poran & Christopher Nötzel & Omar Aly & Nuria Mencia-Trinchant & Chantal T. Harris & Monica L. Guzman & Duane C. Hassane & Olivier Elemento & Björn F. C. Kafsack, 2017. "Single-cell RNA sequencing reveals a signature of sexual commitment in malaria parasites," Nature, Nature, vol. 551(7678), pages 95-99, November.
    3. Jane M. Carlton & John H. Adams & Joana C. Silva & Shelby L. Bidwell & Hernan Lorenzi & Elisabet Caler & Jonathan Crabtree & Samuel V. Angiuoli & Emilio F. Merino & Paolo Amedeo & Qin Cheng & Richard , 2008. "Comparative genomics of the neglected human malaria parasite Plasmodium vivax," Nature, Nature, vol. 455(7214), pages 757-763, October.
    4. Hernando A. del Portillo & Carmen Fernandez-Becerra & Sharen Bowman & Karen Oliver & Martin Preuss & Cecilia P. Sanchez & Nick K. Schneider & Juan M. Villalobos & Marie-Adele Rajandream & David Harris, 2001. "A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax," Nature, Nature, vol. 410(6830), pages 839-842, April.
    5. Juliana M. Sá & Sarah R. Kaslow & Roberto R. Moraes Barros & Nicholas F. Brazeau & Christian M. Parobek & Dingyin Tao & Rebecca E. Salzman & Tyler J. Gibson & Soundarapandian Velmurugan & Michael A. K, 2019. "Plasmodium vivax chloroquine resistance links to pvcrt transcription in a genetic cross," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    6. Camilla Luiza-Batista & Sabine Thiberge & Malika Serra-Hassoun & Flore Nardella & Aurélie Claës & Vanessa C. Nicolete & Pierre-Henri Commère & Liliana Mancio-Silva & Marcelo U. Ferreira & Artur Scherf, 2022. "Humanized mice for investigating sustained Plasmodium vivax blood-stage infections and transmission," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    7. Abhinav Sinha & Katie R. Hughes & Katarzyna K. Modrzynska & Thomas D. Otto & Claudia Pfander & Nicholas J. Dickens & Agnieszka A. Religa & Ellen Bushell & Anne L. Graham & Rachael Cameron & Bjorn F. C, 2014. "A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium," Nature, Nature, vol. 507(7491), pages 253-257, March.
    8. Eliana Real & Virginia M. Howick & Farah A. Dahalan & Kathrin Witmer & Juliana Cudini & Clare Andradi-Brown & Joshua Blight & Mira S. Davidson & Sunil Kumar Dogga & Adam J. Reid & Jake Baum & Mara K. , 2021. "A single-cell atlas of Plasmodium falciparum transmission through the mosquito," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
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