Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes

Abstract Similar to many eukaryotes, the thermoacidophilic archaeon Saccharolobus islandicus follows a defined cell cycle program, with two growth phases, G1 and G2, interspersed by a chromosome replication phase (S), and followed by genome segregation and cytokinesis (M-D) phases. To study whether...

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Main Authors: Miguel V. Gomez-Raya-Vilanova, Jérôme Teulière, Sofia Medvedeva, Yuping Dai, Eduardo Corel, Philippe Lopez, François-Joseph Lapointe, Debashish Bhattacharya, Louis-Patrick Haraoui, Elodie Turc, Marc Monot, Virginija Cvirkaite-Krupovic, Eric Bapteste, Mart Krupovic
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60613-8
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author Miguel V. Gomez-Raya-Vilanova
Jérôme Teulière
Sofia Medvedeva
Yuping Dai
Eduardo Corel
Philippe Lopez
François-Joseph Lapointe
Debashish Bhattacharya
Louis-Patrick Haraoui
Elodie Turc
Marc Monot
Virginija Cvirkaite-Krupovic
Eric Bapteste
Mart Krupovic
author_facet Miguel V. Gomez-Raya-Vilanova
Jérôme Teulière
Sofia Medvedeva
Yuping Dai
Eduardo Corel
Philippe Lopez
François-Joseph Lapointe
Debashish Bhattacharya
Louis-Patrick Haraoui
Elodie Turc
Marc Monot
Virginija Cvirkaite-Krupovic
Eric Bapteste
Mart Krupovic
author_sort Miguel V. Gomez-Raya-Vilanova
collection DOAJ
description Abstract Similar to many eukaryotes, the thermoacidophilic archaeon Saccharolobus islandicus follows a defined cell cycle program, with two growth phases, G1 and G2, interspersed by a chromosome replication phase (S), and followed by genome segregation and cytokinesis (M-D) phases. To study whether and which other processes are cell cycle-coordinated, we synchronized cultures of S. islandicus and performed an in-depth transcriptomic analysis of samples enriched in cells undergoing the M-G1, S, and G2 phases, providing a holistic view of the S. islandicus cell cycle. We show that diverse metabolic pathways, protein synthesis, cell motility and even antiviral defense systems, are expressed in a cell cycle-dependent fashion. Moreover, application of a transcriptome deconvolution method defined sets of phase-specific signature genes, whose peaks of expression roughly matched those of yeast homologs. Collectively, our data elucidates the complexity of the S. islandicus cell cycle, suggesting that it more closely resembles the cell cycle of certain eukaryotes than previously appreciated.
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spelling doaj-art-e3cb396e482c4d0cb6b32db0aaa41e412025-08-20T04:01:36ZengNature PortfolioNature Communications2041-17232025-07-0116111710.1038/s41467-025-60613-8Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotesMiguel V. Gomez-Raya-Vilanova0Jérôme Teulière1Sofia Medvedeva2Yuping Dai3Eduardo Corel4Philippe Lopez5François-Joseph Lapointe6Debashish Bhattacharya7Louis-Patrick Haraoui8Elodie Turc9Marc Monot10Virginija Cvirkaite-Krupovic11Eric Bapteste12Mart Krupovic13Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology UnitInstitut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université Des AntillesInstitut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology UnitInstitut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université Des AntillesInstitut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université Des AntillesInstitut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université Des AntillesDépartement de Sciences Biologiques, Complexe Des Sciences, Université de MontréalDepartment of Biochemistry and Microbiology, Rutgers UniversityDepartment of Microbiology and Infectious Diseases, Faculty of Medicine and Health Sciences, Université de SherbrookeInstitut Pasteur, Université Paris Cité, Plate-forme Technologique BiomicsInstitut Pasteur, Université Paris Cité, Plate-forme Technologique BiomicsInstitut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology UnitInstitut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université Des AntillesInstitut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology UnitAbstract Similar to many eukaryotes, the thermoacidophilic archaeon Saccharolobus islandicus follows a defined cell cycle program, with two growth phases, G1 and G2, interspersed by a chromosome replication phase (S), and followed by genome segregation and cytokinesis (M-D) phases. To study whether and which other processes are cell cycle-coordinated, we synchronized cultures of S. islandicus and performed an in-depth transcriptomic analysis of samples enriched in cells undergoing the M-G1, S, and G2 phases, providing a holistic view of the S. islandicus cell cycle. We show that diverse metabolic pathways, protein synthesis, cell motility and even antiviral defense systems, are expressed in a cell cycle-dependent fashion. Moreover, application of a transcriptome deconvolution method defined sets of phase-specific signature genes, whose peaks of expression roughly matched those of yeast homologs. Collectively, our data elucidates the complexity of the S. islandicus cell cycle, suggesting that it more closely resembles the cell cycle of certain eukaryotes than previously appreciated.https://doi.org/10.1038/s41467-025-60613-8
spellingShingle Miguel V. Gomez-Raya-Vilanova
Jérôme Teulière
Sofia Medvedeva
Yuping Dai
Eduardo Corel
Philippe Lopez
François-Joseph Lapointe
Debashish Bhattacharya
Louis-Patrick Haraoui
Elodie Turc
Marc Monot
Virginija Cvirkaite-Krupovic
Eric Bapteste
Mart Krupovic
Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
Nature Communications
title Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
title_full Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
title_fullStr Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
title_full_unstemmed Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
title_short Transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
title_sort transcriptional landscape of the cell cycle in a model thermoacidophilic archaeon reveals similarities to eukaryotes
url https://doi.org/10.1038/s41467-025-60613-8
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