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Transcriptional heterogeneity and tightly regulated changes in gene expression during Plasmodium berghei sporozoite development.

ABSTRACT: Despite the critical role of Plasmodium sporozoites in malaria transmission, we still know little about the mechanisms underlying their development in mosquitoes. Here, we use single-cell RNA sequencing to characterize the gene expression profiles of 16,038 Plasmodium berghei sporozoites isolated throughout their development from midgut oocysts to salivary glands, and from forced salivation experiments. Our results reveal a succession of tightly regulated changes in gene expression occurring during the maturation of sporozoites and highlight candidate genes that could play important roles in oocyst egress, sporozoite motility, and the mechanisms underlying the invasion of mosquito salivary glands and mammalian hepatocytes. In addition, the single-cell data reveal extensive transcriptional heterogeneity among parasites isolated from the same anatomical site, suggesting that Plasmodium development in mosquitoes is asynchronous and regulated by intrinsic as well as environmental factors. Finally, our analyses show a decrease in transcriptional activity preceding the translational repression observed in mature sporozoites and associated with their quiescent state in salivary glands, followed by a rapid reactivation of the transcriptional machinery immediately upon salivation.

SUBMITTER: Bogale HN

PROVIDER: S-EPMC7958459 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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Transcriptional heterogeneity and tightly regulated changes in gene expression during Plasmodium berghei sporozoite development.

Bogale Haikel N HN Pascini Tales V TV Kanatani Sachie S Sá Juliana M JM Wellems Thomas E TE Sinnis Photini P Vega-Rodríguez Joel J Serre David D

Proceedings of the National Academy of Sciences of the United States of America 20210301 10

Despite the critical role of Plasmodium sporozoites in malaria transmission, we still know little about the mechanisms underlying their development in mosquitoes. Here, we use single-cell RNA sequencing to characterize the gene expression profiles of 16,038 Plasmodium berghei sporozoites isolated throughout their development from midgut oocysts to salivary glands, and from forced salivation experiments. Our results reveal a succession of tightly regulated changes in gene expression ...[more]

PMID: 33653959

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Project description:BackgroundThe complex life cycle of malaria parasites requires well-orchestrated stage specific gene expression. In the vertebrate host the parasites grow and multiply by schizogony in two different environments: within erythrocytes and within hepatocytes. Whereas erythrocytic parasites are well-studied in this respect, relatively little is known about the exo-erythrocytic stages.MethodsIn an attempt to fill this gap, genome wide RNA-seq analyses of various exo-erythrocytic stages of Plasmodium berghei including sporozoites, samples from a time-course of liver stage development and detached cells were performed. These latter contain infectious merozoites and represent the final step in exo-erythrocytic development.ResultsThe analysis represents the complete transcriptome of the entire life cycle of P. berghei parasites with temporal detailed analysis of the liver stage allowing comparison of gene expression across the progression of the life cycle. These RNA-seq data from different developmental stages were used to cluster genes with similar expression profiles, in order to infer their functions. A comparison with published data from other parasite stages confirmed stage-specific gene expression and revealed numerous genes that are expressed differentially in blood and exo-erythrocytic stages. One of the most exo-erythrocytic stage-specific genes was PBANKA_1003900, which has previously been annotated as a "gametocyte specific protein". The promoter of this gene drove high GFP expression in exo-erythrocytic stages, confirming its expression profile seen by RNA-seq.ConclusionsThe comparative analysis of the genome wide mRNA expression profiles of erythrocytic and different exo-erythrocytic stages could be used to improve the understanding of gene regulation in Plasmodium parasites and can be used to model exo-erythrocytic stage metabolic networks toward the identification of differences in metabolic processes during schizogony in erythrocytes and hepatocytes.

Dataset Information

Transcriptional heterogeneity and tightly regulated changes in gene expression during Plasmodium berghei sporozoite development.

Publications

Transcriptional heterogeneity and tightly regulated changes in gene expression during <i>Plasmodium berghei</i> sporozoite development.

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Transcriptional heterogeneity and tightly regulated changes in gene expression during Plasmodium berghei sporozoite development.

Publications

Transcriptional heterogeneity and tightly regulated changes in gene expression during &lt;i&gt;Plasmodium berghei&lt;/i&gt; sporozoite development.

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OmicsDI is part of the ELIXIR infrastructure

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Transcriptional heterogeneity and tightly regulated changes in gene expression during <i>Plasmodium berghei</i> sporozoite development.