The proteasome controls ESCRT-III–mediated cell division in an archaeon

Risa, Gabriel Tarrason; Hurtig, Fredrik; Bray, Sian; Hafner, Anne E.; Harker-Kirschneck, Lena; Faull, Peter; Davis, Colin T.; Papatziamou, Dimitra; Mutavchiev, Delyan R.; Fan, Catherine; Meneguello, Letícia; Pulschen, André Arashiro; Dey, G.K.; Culley, Siân; Kilkenny, M.L.; Souza, Diorge P.; Pellegrini, Luca; Bruin, Robertus A.M. de; Henriques, Ricardo; Snijders, Ambrosius P.; Šarić, Anđela; Lindås, Ann-Christin; Robinson, Nicholas P.; Baum, Buzz

doi:10.1126/science.aaz2532

Cited by 67 publications

(98 citation statements)

References 64 publications

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“…In vitro reconstitutions suggest that Snf7, Vps24, and Vps2 are essential for membrane budding, and Vps4 for vesicle scission (11,17). Vps4-mediated turnover of a laterally-associating and helix-inducing polymer of Vps24-Vps2 would constrict the Snf7 scaffold to a fission-competent structure, as predicted by simulations (38) and as recently proposed to occur in archaeal cell division (39). While Did2 and Ist1 are not essential for intraluminal vesicle formation in vitro and in vivo, they have regulatory roles that are controlled by sequential polymerization dynamics through Vps4 (17).…”

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confidence: 53%

Design Principles of the ESCRT-III Vps24-Vps2 Module

Banjade

Shah

Tang³

et al. 2020

Preprint

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ESCRT-III polymerization is required for all ESCRT-dependent events in the cell. However, the relative contributions of the eight ESCRT-III subunits differ between each process. The minimal features of ESCRT-III proteins necessary for function, and the role for the multiple ESCRT-III subunits remain unclear. To identify essential features of ESCRT-III subunits, we previously studied the polymerization mechanisms of two ESCRT-III subunits Snf7 and Vps24, identifying the association of the helix-4 region of Snf7 with the helix-1 region of Vps24 (Banjade et al., 2019). Here, we find that mutations in the helix-1 region of another ESCRT-III subunit Vps2 can functionally replace Vps24 in S. cerevisiae. Engineering and genetic selections revealed the required features of both subunits. Our data allow us to propose three minimal features required for ESCRT-III function – spiral formation, lateral association of the spirals through heteropolymerization, and binding to the AAA+ ATPase Vps4 for dynamic remodeling.

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confidence: 53%

Design Principles of the ESCRT-III Vps24-Vps2 Module

Banjade

Shah

Tang³

et al. 2020

Preprint

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Section: Resultsmentioning

confidence: 99%

“…To test this idea, we instantaneously changed the target radius of the filament to 5% of the cell radius and let the system evolve. Since filament disassembly is needed for scission [6], as soon as the new equilibrium bond lengths have been imposed, we initiated the disassembly process by severing bonds between filament monomers sequentially from both ends of the helix at a specified rate v dis . Interestingly, rather than adapting the target shape of a single tight helix, we find that the filament upon constriction instantly transforms into a collection of short tight helices of alternating chiralities separated by kinks called perversions (Figure 1c).…”

Section: A Minimal Model Of Cell Divisionmentioning

confidence: 99%

“…The first filamenteous ring (called CdvB) serves as a template for the assembly of a contractile ring (made of CdvB1 and CdvB2 proteins), see Figure 1. Recently it has been shown that the contractile ring is only free to exert forces to reshape the membrane once the template CdvB ring has been removed [6]. As the membrane constricts, the contractile CdvB1/2 ESCRT-III filament disassembles.…”

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confidence: 99%

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Physical mechanisms of ESCRT-III-driven cell division in archaea

Harker-Kirschneck

Yao³

et al. 2021

Preprint

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Living systems propagate by undergoing rounds of cell growth and division. Cell division is at heart a physical process that requires mechanical forces, usually exerted by protein assemblies. Here we developed the first physical model for the division of archaeal cells, which despite their structural simplicity share machinery and evolutionary origins with eukaryotes. We show how active geometry changes of elastic ESCRT-III filaments, coupled to filament disassembly, are sufficient to efficiently split the cell. We explore how the non-equilibrium processes that govern the filament behaviour impact the resulting cell division. We show how a quantitative comparison between our simulations and dynamic data for ESCRTIII-mediated division in Sulfolobus acidocaldarius, the closest archaeal relative to eukaryotic cells that can currently be cultured in the lab, and reveal the most likely physical mechanism behind its division.

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“…Crenarchaeota including Sulfolobus spp. rely on the endosomal sorting complexes required for transport (ESCRT III) machinery for cell division, vesicle formation and budding (36)(37)(38)(39). In response to 1-butanol exposure the genes encoding one of the three CdvB paralogs (cdvB1 gene, saci_0451) is significantly upregulated (38,39).…”

Section: Effect Of 1-butanol On Eps Compositionmentioning

confidence: 99%

Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress

Benninghoff

Kuschmierz

Zhou

et al. 2021

Appl Environ Microbiol

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Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80 °C and pH 2 - 3. Due to its unique physiological properties allowing life at environmental extremes and recent availability of genetic tools, this extremophile receives increasing interest for biotechnological application. In order to elucidate the potential of tolerating process-related stress conditions, we investigated the response of S. acidocaldarius towards the industrially relevant organic solvent 1-butanol. In response to butanol exposure, biofilm formation of S. acidocaldarius was enhanced and occurred up to 1.5% (v/v) 1-butanol, while planktonic growth was only observed up to 1% (v/v) 1-butanol. Confocal laser scanning microscopy revealed that biofilm architecture changed with the formation of denser and higher tower-like structures. Concomitantly, changes in the extracellular polymeric substances with enhanced carbohydrate and protein content were determined in 1-butanol-exposed biofilms. Using scanning electron microscopy three different cell morphotypes were observed in response to 1-butanol. Transcriptome and proteome analyses were performed comparing the response of planktonic and biofilm cells in absence and presence of 1-butanol. In response to 1% (v/v) 1-butanol transcript levels of genes encoding motility and cell envelope structures as well as membrane proteins were reduced. Cell division and/or vesicle formation was upregulated. Furthermore, changes of immune and defence systems, as well as metabolism and general stress response were observed. Our findings show that the extreme lifestyle of S. acidocaldarius coincided with a high tolerance to organic solvents. This study provides first insights into biofilm formation and membrane/cell stress caused by organic solvents in S. acidocaldarius. Importance Archaea are unique in terms of metabolic and cellular processes as well as the adaptation to extreme environments. In the past few years, the development of genetic systems and biochemical, genetic and poly-omics studies have provided deep insights into the physiology of some archaeal model organisms. In this study, we used S. acidocaldarius adapted to two extremes, low pH and high temperature, to study its tolerance and robustness as well as its global cellular response towards organic solvents exemplified by 1-butanol. We were able to identify biofilm formation as primary cellular response to 1-butanol. Furthermore, the triggered cell/membrane stress led to significant changes in culture heterogeneity accompanied by changes in central cellular processes such as cell division and cellular defense systems, thus suggesting a global response for the protection at population level.

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The proteasome controls ESCRT-III–mediated cell division in an archaeon

Cited by 67 publications

References 64 publications

Design Principles of the ESCRT-III Vps24-Vps2 Module

Design Principles of the ESCRT-III Vps24-Vps2 Module

Physical mechanisms of ESCRT-III-driven cell division in archaea

Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress

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