A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon
ABSTRACT 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-I...
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American Society for Microbiology
2025-02-01
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.00991-24 |
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| author | Junfeng Liu Mickaël Lelek Yunfeng Yang Audrey Salles Christophe Zimmer Yulong Shen Mart Krupovic |
| author_facet | Junfeng Liu Mickaël Lelek Yunfeng Yang Audrey Salles Christophe Zimmer Yulong Shen Mart Krupovic |
| author_sort | Junfeng Liu |
| collection | DOAJ |
| description | ABSTRACT 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.IMPORTANCETwo 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, different lineages of archaea use either of the two systems, and eukaryotes have inherited the ESCRT-based cell division machinery from their archaeal ancestors. The mechanism of ESCRT-based cell division in archaea remains poorly understood and mechanistic studies on different archaeal model systems are essential to unravel the natural history of the ESCRT machinery. Here we investigate the interplay between three major ESCRT-III homologs during the division of a hyperthermophilic archaeon Saccharolobus islandicus and propose the “relay race” model of cytokinesis. |
| format | Article |
| id | doaj-art-381b73c3d8544406bc00bd388c712d46 |
| institution | Kabale University |
| issn | 2150-7511 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | American Society for Microbiology |
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| spelling | doaj-art-381b73c3d8544406bc00bd388c712d462025-02-05T14:00:48ZengAmerican Society for MicrobiologymBio2150-75112025-02-0116210.1128/mbio.00991-24A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeonJunfeng Liu0Mickaël Lelek1Yunfeng Yang2Audrey Salles3Christophe Zimmer4Yulong Shen5Mart Krupovic6Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, FranceImaging and Modeling Unit, Institut Pasteur, Université Paris Cité, Paris, FranceCRISPR and Archaea Biology Research Centre, Microbial Technology Institute and State Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaInstitut Pasteur, Université Paris Cité, Unit of Technology and Service Photonic BioImaging (UTechS PBI), C2RT, Paris, FranceImaging and Modeling Unit, Institut Pasteur, Université Paris Cité, Paris, FranceCRISPR and Archaea Biology Research Centre, Microbial Technology Institute and State Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaInstitut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, FranceABSTRACT 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.IMPORTANCETwo 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, different lineages of archaea use either of the two systems, and eukaryotes have inherited the ESCRT-based cell division machinery from their archaeal ancestors. The mechanism of ESCRT-based cell division in archaea remains poorly understood and mechanistic studies on different archaeal model systems are essential to unravel the natural history of the ESCRT machinery. Here we investigate the interplay between three major ESCRT-III homologs during the division of a hyperthermophilic archaeon Saccharolobus islandicus and propose the “relay race” model of cytokinesis.https://journals.asm.org/doi/10.1128/mbio.00991-24Archaeacell divisionESCRT systemCrenarchaeotaSulfolobusSaccharolobus islandicus |
| spellingShingle | Junfeng Liu Mickaël Lelek Yunfeng Yang Audrey Salles Christophe Zimmer Yulong Shen Mart Krupovic A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon mBio Archaea cell division ESCRT system Crenarchaeota Sulfolobus Saccharolobus islandicus |
| title | A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon |
| title_full | A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon |
| title_fullStr | A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon |
| title_full_unstemmed | A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon |
| title_short | A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon |
| title_sort | relay race of escrt iii paralogs drives cell division in a hyperthermophilic archaeon |
| topic | Archaea cell division ESCRT system Crenarchaeota Sulfolobus Saccharolobus islandicus |
| url | https://journals.asm.org/doi/10.1128/mbio.00991-24 |
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