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The establishment of variant surface glycoprotein monoallelic expression revealed by single-cell RNA-seq of Trypanosoma brucei in the tsetse fly salivary glands

View ORCID ProfileSebastian Hutchinson, Sophie Foulon, Aline Crouzols, Roberta Menafra, View ORCID ProfileBrice Rotureau, Andrew D. Griffiths, View ORCID ProfilePhilippe Bastin
doi: https://doi.org/10.1101/2021.03.01.433049
Sebastian Hutchinson
1Trypanosome Cell Biology Unit and INSERM U1201, 25-28 Rue du Dr Roux, Institut Pasteur, Paris, France
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  • For correspondence: sebastian.hutchinson@pasteur.fr
Sophie Foulon
2Laboratoire de Biochimie, CBI, ESPCI Paris, Université PSL, CNRS UMR 8231, 75005 Paris, France
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Aline Crouzols
1Trypanosome Cell Biology Unit and INSERM U1201, 25-28 Rue du Dr Roux, Institut Pasteur, Paris, France
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Roberta Menafra
2Laboratoire de Biochimie, CBI, ESPCI Paris, Université PSL, CNRS UMR 8231, 75005 Paris, France
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Brice Rotureau
1Trypanosome Cell Biology Unit and INSERM U1201, 25-28 Rue du Dr Roux, Institut Pasteur, Paris, France
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Andrew D. Griffiths
2Laboratoire de Biochimie, CBI, ESPCI Paris, Université PSL, CNRS UMR 8231, 75005 Paris, France
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Philippe Bastin
1Trypanosome Cell Biology Unit and INSERM U1201, 25-28 Rue du Dr Roux, Institut Pasteur, Paris, France
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Abstract

The long and complex Trypanosoma brucei development in the tsetse fly vector culminates when parasites gain mammalian infectivity in the salivary glands. A key step in this process is the establishment of monoallelic variant surface glycoprotein (VSG) expression and the formation of the VSG coat. The establishment of VSG monoallelic expression is complex and poorly understood, due to the multiple parasite stages present in the salivary glands. Therefore, we sought to further our understanding of this phenomenon by performing single-cell RNA-sequencing (scRNA-seq) on these trypanosome populations. We were able to capture the developmental program of trypanosomes in the salivary glands, identifying populations of epimastigote, gamete, pre-metacyclic and metacyclic cells. Our results show that parasite metabolism is dramatically remodeled during development in the salivary glands, with a shift in transcript abundance from tricarboxylic acid metabolism to glycolytic metabolism. Analysis of VSG gene expression in pre-metacyclic and metacyclic cells revealed a dynamic VSG gene activation program. Strikingly, we found that pre-metacyclic cells contain transcripts from multiple VSG genes, which resolves to singular VSG gene expression in mature metacyclic cells. Single molecule RNA fluorescence in situ hybridisation (smRNA-FISH) of VSG gene expression following in vitro metacyclogenesis confirmed this finding. Our data demonstrate that multiple VSG genes are transcribed before a single gene is chosen. We propose a transcriptional race model governs the initiation of monoallelic expression.

Competing Interest Statement

A.D.G. is a shareholder in 1CellBio

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 01, 2021.
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The establishment of variant surface glycoprotein monoallelic expression revealed by single-cell RNA-seq of Trypanosoma brucei in the tsetse fly salivary glands
Sebastian Hutchinson, Sophie Foulon, Aline Crouzols, Roberta Menafra, Brice Rotureau, Andrew D. Griffiths, Philippe Bastin
bioRxiv 2021.03.01.433049; doi: https://doi.org/10.1101/2021.03.01.433049
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The establishment of variant surface glycoprotein monoallelic expression revealed by single-cell RNA-seq of Trypanosoma brucei in the tsetse fly salivary glands
Sebastian Hutchinson, Sophie Foulon, Aline Crouzols, Roberta Menafra, Brice Rotureau, Andrew D. Griffiths, Philippe Bastin
bioRxiv 2021.03.01.433049; doi: https://doi.org/10.1101/2021.03.01.433049

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