Single-cell RNA sequencing of Plasmodium vivax sporozoites reveals stage- and species-specific transcriptomic signatures.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
08 2022
Historique:
received: 18 12 2021
accepted: 04 07 2022
revised: 16 08 2022
pubmed: 5 8 2022
medline: 19 8 2022
entrez: 4 8 2022
Statut: epublish

Résumé

Plasmodium vivax sporozoites reside in the salivary glands of a mosquito before infecting a human host and causing malaria. Previous transcriptome-wide studies in populations of these parasite forms were limited in their ability to elucidate cell-to-cell variation, thereby masking cellular states potentially important in understanding malaria transmission outcomes. In this study, we performed transcription profiling on 9,947 P. vivax sporozoites to assess the extent to which they differ at single-cell resolution. We show that sporozoites residing in the mosquito's salivary glands exist in distinct developmental states, as defined by their transcriptomic signatures. Additionally, relative to P. falciparum, P. vivax displays overlapping and unique gene usage patterns, highlighting conserved and species-specific gene programs. Notably, distinguishing P. vivax from P. falciparum were a subset of P. vivax sporozoites expressing genes associated with translational regulation and repression. Finally, our comparison of single-cell transcriptomic data from P. vivax sporozoite and erythrocytic forms reveals gene usage patterns unique to sporozoites. In defining the transcriptomic signatures of individual P. vivax sporozoites, our work provides new insights into the factors driving their developmental trajectory and lays the groundwork for a more comprehensive P. vivax cell atlas.

Sections du résumé

BACKGROUND
Plasmodium vivax sporozoites reside in the salivary glands of a mosquito before infecting a human host and causing malaria. Previous transcriptome-wide studies in populations of these parasite forms were limited in their ability to elucidate cell-to-cell variation, thereby masking cellular states potentially important in understanding malaria transmission outcomes.
METHODOLOGY/PRINCIPAL FINDINGS
In this study, we performed transcription profiling on 9,947 P. vivax sporozoites to assess the extent to which they differ at single-cell resolution. We show that sporozoites residing in the mosquito's salivary glands exist in distinct developmental states, as defined by their transcriptomic signatures. Additionally, relative to P. falciparum, P. vivax displays overlapping and unique gene usage patterns, highlighting conserved and species-specific gene programs. Notably, distinguishing P. vivax from P. falciparum were a subset of P. vivax sporozoites expressing genes associated with translational regulation and repression. Finally, our comparison of single-cell transcriptomic data from P. vivax sporozoite and erythrocytic forms reveals gene usage patterns unique to sporozoites.
CONCLUSIONS/SIGNIFICANCE
In defining the transcriptomic signatures of individual P. vivax sporozoites, our work provides new insights into the factors driving their developmental trajectory and lays the groundwork for a more comprehensive P. vivax cell atlas.

Identifiants

pubmed: 35926062
doi: 10.1371/journal.pntd.0010633
pii: PNTD-D-21-01772
pmc: PMC9380936
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0010633

Subventions

Organisme : NIAID NIH HHS
ID : U19 AI129392
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Anthony A Ruberto (AA)

Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France.

Caitlin Bourke (C)

Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, The University of Melbourne, Parkville, Victoria, Australia.

Amélie Vantaux (A)

Malaria Molecular Epidemiology Unit, Institut Pasteur du Cambodge, Phnom Penh, Kingdom of Cambodia.

Steven P Maher (SP)

Center for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, United States of America.

Aaron Jex (A)

Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, The University of Melbourne, Parkville, Victoria, Australia.

Benoit Witkowski (B)

Malaria Molecular Epidemiology Unit, Institut Pasteur du Cambodge, Phnom Penh, Kingdom of Cambodia.

Georges Snounou (G)

Commissariat à l'Énergie Atomique et aux Énergies Alternatives-Université Paris Sud 11-INSERM U1184, Immunology of Viral Infections and Autoimmune Diseases (IMVA-HB), Infectious Disease Models and Innovative Therapies (IDMIT) Department, Institut de Biologie François Jacob (IBFJ), Direction de la Recherche Fondamentale (DRF), Fontenay-aux-Roses, France.

Ivo Mueller (I)

Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France.
Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, The University of Melbourne, Parkville, Victoria, Australia.

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