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A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon

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Τίτλος: A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon
Συγγραφείς: Liu, Junfeng, Lelek, Mickaël, Yang, Yunfeng, Salles, Audrey, Zimmer, Christophe, Shen, Yulong, Krupovic, Mart
Συνεισφορές: Virologie des archées - Archaeal Virology, Université Paris Cité (UPCité)-Microbiologie Intégrative et Moléculaire (UMR6047), Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS), Shandong University, Imagerie et Modélisation - Imaging and Modeling, Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), BioImagerie Photonique – Photonic BioImaging (UTechS PBI), Institut Pasteur Paris (IP)-Université Paris Cité (UPCité), Julius-Maximilians-Universität Würzburg = University of Würzburg Würsburg, Germany (JMU), This work was supported by a grant from Ville de Paris (Emergence(s) project MEMREMA) and Agence Nationale de la Recherche (ANR-23-CE13-022) to M.K. and grants from the National Key Research and Development Program of China (2020YFA0906800) and the National Natural Science Foundation of China (32393973, 32370033) to Y.S., We thank the UTechS PBI, which is part of the France-BioImaging infrastructure network (FBI) supported by the French National Research Agency (ANR-10-INBS-04, Investments for the Future), and acknowledge support from Institut Pasteur for the use of the Leica SP8 confocal microscope. We are grateful to the Ultrastructural BioImaging Core Facility of Institut Pasteur for the access to electron microscopes. We thank Benoît Lelandais for help with the quantitative characterization and simulations of ring-like ESCRT-III structures., ANR-23-CE13-0022,ARCHANE,Reconstruction de la biologie cellulaire de l'ancêtre archéen des eucaryotes(2023)
Πηγή: ISSN: 2161-2129.
Στοιχεία εκδότη: CCSD
American Society for Microbiology
Έτος έκδοσης: 2025
Θεματικοί όροι: cell division, ESCRT system, Crenarchaeota, Sulfolobus, Saccharolobus islandicus, Archaea, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
Περιγραφή: International audience ; Cell division is a fundamental process ensuring the perpetuation of all cellular life forms. Archaea of the order Sulfolobales divide using a simpler version of the eukaryotic endosomal sorting complexes required for transport (ESCRT) machinery, composed of three ESCRT-III homologs (ESCRT-III, -III-1, and -III-2), AAA+ ATPase Vps4 and an archaea-specific component CdvA. Here, we clarify how these components act sequentially to drive the division of the hyperthermophilic archaeon Saccharolobus islandicus . Our data suggest that ESCRT-III plays an active role during the early stage of membrane constriction during cytokinesis, whereas ESCRT-III-1 and ESCRT-III-2 are indispensable for the “pre-late” and “late” stages of cytokinesis, respectively. In the escrt-III-1 deletion strain, the division is blocked when the mid-cell constriction reaches ~30% of the initial cell diameter (“pre-late” stage), yielding “chain-like” cellular aggregates. Depletion of ESCRT-III-2 leads to the accumulation of cells connected through narrow membrane bridges (“late” stage), consistent with the key role of this protein in the final membrane abscission. We used 3D-single molecule localization microscopy to image ESCRT-III rings of different diameters and show that the decrease in the ESCRT-III ring diameter and membrane constriction are inconsistent with a mechanism exclusively based on spiraling of the ESCRT-III filaments. By contrast, the cone-shaped assemblies of ESCRT-III-1 and ESCRT-III-2 are consistent with spiral formation, highlighting the distinct roles of the three ESCRT-III proteins during the cytokinesis. We propose the “relay race” model, whereby the cytokinesis is achieved through a sequential and concerted action of different ESCRT machinery components. IMPORTANCE Two major cytokinesis mechanisms, rooted in contractile FtsZ and endosomal sorting complexes required for transport (ESCRT) rings, respectively, have emerged in the course of evolution. Whereas bacteria rely on the FtsZ-based mechanism, ...
Τύπος εγγράφου: article in journal/newspaper
Γλώσσα: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/39699168; PUBMED: 39699168; PUBMEDCENTRAL: PMC11796394
DOI: 10.1128/mbio.00991-24
Διαθεσιμότητα: https://pasteur.hal.science/pasteur-04961408
https://pasteur.hal.science/pasteur-04961408v1/document
https://pasteur.hal.science/pasteur-04961408v1/file/Liu2025mBio.pdf
https://doi.org/10.1128/mbio.00991-24
Rights: http://creativecommons.org/licenses/by/ ; info:eu-repo/semantics/OpenAccess
Αριθμός Καταχώρησης: edsbas.DA318D7B
Βάση Δεδομένων: BASE
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  Data: A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon
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  Data: <searchLink fieldCode="AR" term="%22Liu%2C+Junfeng%22">Liu, Junfeng</searchLink><br /><searchLink fieldCode="AR" term="%22Lelek%2C+Mickaël%22">Lelek, Mickaël</searchLink><br /><searchLink fieldCode="AR" term="%22Yang%2C+Yunfeng%22">Yang, Yunfeng</searchLink><br /><searchLink fieldCode="AR" term="%22Salles%2C+Audrey%22">Salles, Audrey</searchLink><br /><searchLink fieldCode="AR" term="%22Zimmer%2C+Christophe%22">Zimmer, Christophe</searchLink><br /><searchLink fieldCode="AR" term="%22Shen%2C+Yulong%22">Shen, Yulong</searchLink><br /><searchLink fieldCode="AR" term="%22Krupovic%2C+Mart%22">Krupovic, Mart</searchLink>
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  Data: Virologie des archées - Archaeal Virology<br />Université Paris Cité (UPCité)-Microbiologie Intégrative et Moléculaire (UMR6047)<br />Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)<br />Shandong University<br />Imagerie et Modélisation - Imaging and Modeling<br />Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)<br />BioImagerie Photonique – Photonic BioImaging (UTechS PBI)<br />Institut Pasteur Paris (IP)-Université Paris Cité (UPCité)<br />Julius-Maximilians-Universität Würzburg = University of Würzburg Würsburg, Germany (JMU)<br />This work was supported by a grant from Ville de Paris (Emergence(s) project MEMREMA) and Agence Nationale de la Recherche (ANR-23-CE13-022) to M.K. and grants from the National Key Research and Development Program of China (2020YFA0906800) and the National Natural Science Foundation of China (32393973, 32370033) to Y.S.<br />We thank the UTechS PBI, which is part of the France-BioImaging infrastructure network (FBI) supported by the French National Research Agency (ANR-10-INBS-04<br />Investments for the Future), and acknowledge support from Institut Pasteur for the use of the Leica SP8 confocal microscope. We are grateful to the Ultrastructural BioImaging Core Facility of Institut Pasteur for the access to electron microscopes. We thank Benoît Lelandais for help with the quantitative characterization and simulations of ring-like ESCRT-III structures.<br />ANR-23-CE13-0022,ARCHANE,Reconstruction de la biologie cellulaire de l'ancêtre archéen des eucaryotes(2023)
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  Data: 2025
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  Data: <searchLink fieldCode="DE" term="%22cell+division%22">cell division</searchLink><br /><searchLink fieldCode="DE" term="%22ESCRT+system%22">ESCRT system</searchLink><br /><searchLink fieldCode="DE" term="%22Crenarchaeota%22">Crenarchaeota</searchLink><br /><searchLink fieldCode="DE" term="%22Sulfolobus%22">Sulfolobus</searchLink><br /><searchLink fieldCode="DE" term="%22Saccharolobus+islandicus%22">Saccharolobus islandicus</searchLink><br /><searchLink fieldCode="DE" term="%22Archaea%22">Archaea</searchLink><br /><searchLink fieldCode="DE" term="%22[SDV%2EMP]Life+Sciences+[q-bio]%2FMicrobiology+and+Parasitology%22">[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology</searchLink>
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  Data: International audience ; Cell division is a fundamental process ensuring the perpetuation of all cellular life forms. Archaea of the order Sulfolobales divide using a simpler version of the eukaryotic endosomal sorting complexes required for transport (ESCRT) machinery, composed of three ESCRT-III homologs (ESCRT-III, -III-1, and -III-2), AAA+ ATPase Vps4 and an archaea-specific component CdvA. Here, we clarify how these components act sequentially to drive the division of the hyperthermophilic archaeon Saccharolobus islandicus . Our data suggest that ESCRT-III plays an active role during the early stage of membrane constriction during cytokinesis, whereas ESCRT-III-1 and ESCRT-III-2 are indispensable for the “pre-late” and “late” stages of cytokinesis, respectively. In the escrt-III-1 deletion strain, the division is blocked when the mid-cell constriction reaches ~30% of the initial cell diameter (“pre-late” stage), yielding “chain-like” cellular aggregates. Depletion of ESCRT-III-2 leads to the accumulation of cells connected through narrow membrane bridges (“late” stage), consistent with the key role of this protein in the final membrane abscission. We used 3D-single molecule localization microscopy to image ESCRT-III rings of different diameters and show that the decrease in the ESCRT-III ring diameter and membrane constriction are inconsistent with a mechanism exclusively based on spiraling of the ESCRT-III filaments. By contrast, the cone-shaped assemblies of ESCRT-III-1 and ESCRT-III-2 are consistent with spiral formation, highlighting the distinct roles of the three ESCRT-III proteins during the cytokinesis. We propose the “relay race” model, whereby the cytokinesis is achieved through a sequential and concerted action of different ESCRT machinery components. IMPORTANCE Two major cytokinesis mechanisms, rooted in contractile FtsZ and endosomal sorting complexes required for transport (ESCRT) rings, respectively, have emerged in the course of evolution. Whereas bacteria rely on the FtsZ-based mechanism, ...
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  Data: info:eu-repo/semantics/altIdentifier/pmid/39699168; PUBMED: 39699168; PUBMEDCENTRAL: PMC11796394
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