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Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles

Babesia is a genus of apicomplexan parasites that infect red blood cells in vertebrate hosts. Pathology occurs during rapid replication cycles in the asexual blood stage of infection. Current knowledge of Babesia replication cycle progression and regulation is limited and relies mostly on comparativ...

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Autores principales: Rezvani, Yasaman, Keroack, Caroline D., Elsworth, Brendan, Arriojas, Argenis, Gubbels, Marc-Jan, Duraisingh, Manoj T., Zarringhalam, Kourosh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9531838/
https://www.ncbi.nlm.nih.gov/pubmed/36137068
http://dx.doi.org/10.1371/journal.pbio.3001816
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author Rezvani, Yasaman
Keroack, Caroline D.
Elsworth, Brendan
Arriojas, Argenis
Gubbels, Marc-Jan
Duraisingh, Manoj T.
Zarringhalam, Kourosh
author_facet Rezvani, Yasaman
Keroack, Caroline D.
Elsworth, Brendan
Arriojas, Argenis
Gubbels, Marc-Jan
Duraisingh, Manoj T.
Zarringhalam, Kourosh
author_sort Rezvani, Yasaman
collection PubMed
description Babesia is a genus of apicomplexan parasites that infect red blood cells in vertebrate hosts. Pathology occurs during rapid replication cycles in the asexual blood stage of infection. Current knowledge of Babesia replication cycle progression and regulation is limited and relies mostly on comparative studies with related parasites. Due to limitations in synchronizing Babesia parasites, fine-scale time-course transcriptomic resources are not readily available. Single-cell transcriptomics provides a powerful unbiased alternative for profiling asynchronous cell populations. Here, we applied single-cell RNA sequencing to 3 Babesia species (B. divergens, B. bovis, and B. bigemina). We used analytical approaches and algorithms to map the replication cycle and construct pseudo-synchronized time-course gene expression profiles. We identify clusters of co-expressed genes showing “just-in-time” expression profiles, with gradually cascading peaks throughout asexual development. Moreover, clustering analysis of reconstructed gene curves reveals coordinated timing of peak expression in epigenetic markers and transcription factors. Using a regularized Gaussian graphical model, we reconstructed co-expression networks and identified conserved and species-specific nodes. Motif analysis of a co-expression interactome of AP2 transcription factors identified specific motifs previously reported to play a role in DNA replication in Plasmodium species. Finally, we present an interactive web application to visualize and interactively explore the datasets.
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spelling pubmed-95318382022-10-05 Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles Rezvani, Yasaman Keroack, Caroline D. Elsworth, Brendan Arriojas, Argenis Gubbels, Marc-Jan Duraisingh, Manoj T. Zarringhalam, Kourosh PLoS Biol Methods and Resources Babesia is a genus of apicomplexan parasites that infect red blood cells in vertebrate hosts. Pathology occurs during rapid replication cycles in the asexual blood stage of infection. Current knowledge of Babesia replication cycle progression and regulation is limited and relies mostly on comparative studies with related parasites. Due to limitations in synchronizing Babesia parasites, fine-scale time-course transcriptomic resources are not readily available. Single-cell transcriptomics provides a powerful unbiased alternative for profiling asynchronous cell populations. Here, we applied single-cell RNA sequencing to 3 Babesia species (B. divergens, B. bovis, and B. bigemina). We used analytical approaches and algorithms to map the replication cycle and construct pseudo-synchronized time-course gene expression profiles. We identify clusters of co-expressed genes showing “just-in-time” expression profiles, with gradually cascading peaks throughout asexual development. Moreover, clustering analysis of reconstructed gene curves reveals coordinated timing of peak expression in epigenetic markers and transcription factors. Using a regularized Gaussian graphical model, we reconstructed co-expression networks and identified conserved and species-specific nodes. Motif analysis of a co-expression interactome of AP2 transcription factors identified specific motifs previously reported to play a role in DNA replication in Plasmodium species. Finally, we present an interactive web application to visualize and interactively explore the datasets. Public Library of Science 2022-09-22 /pmc/articles/PMC9531838/ /pubmed/36137068 http://dx.doi.org/10.1371/journal.pbio.3001816 Text en © 2022 Rezvani et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Methods and Resources
Rezvani, Yasaman
Keroack, Caroline D.
Elsworth, Brendan
Arriojas, Argenis
Gubbels, Marc-Jan
Duraisingh, Manoj T.
Zarringhalam, Kourosh
Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title_full Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title_fullStr Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title_full_unstemmed Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title_short Comparative single-cell transcriptional atlases of Babesia species reveal conserved and species-specific expression profiles
title_sort comparative single-cell transcriptional atlases of babesia species reveal conserved and species-specific expression profiles
topic Methods and Resources
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9531838/
https://www.ncbi.nlm.nih.gov/pubmed/36137068
http://dx.doi.org/10.1371/journal.pbio.3001816
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