Proteasome-mediated protein degradation resets the cell division cycle and triggers ESCRT-III-mediated cytokinesis in an archaeon

Abstract

The archaeon Sulfolobus acidocaldarius is a relative of eukaryotes known to progress orderly through its cell division cycle despite lacking obvious CDK/cyclin homologues. Here, in exploring the mechanisms underpinning archaeal cell division cycle control, we show that the proteasome of S. acidocaldarius, like its eukaryotic counterpart, regulates the transition from the end of one cell division cycle to the beginning of the next. Further, we identify the archaeal ESCRT-III homologue CdvB as a key target of the proteasome, and show that state-dependent degradation of CdvB triggers archaeal cell division by allowing constriction of a CdvB1:CdvB2 ESCRT-III division ring. These findings suggest an ancient role for proteasome-mediated degradation in resetting the cell division cycle in both archaea and eukaryotes. ESCRT-III | Cell cycle | Evolution | Proteasome

Live cell imaging of the hyperthermophilic archaeon Sulfolobus acidocaldarius identifies complementary roles for two ESCRTIII homologues in ensuring a robust and symmetric cell division

“…Sudden degradation of CdvB via the archaeal proteasome then triggers division by allowing the CdvB1 and CdvB2 ring to undergo a change in curvature to induce membrane constriction and scission [22]. Under this model, CdvB1 and CdvB2 are treated as being equivalent in terms of their ability to drive scission [22]. This fits with their colocalisation [22] and is in keeping with previous studies that identified CdvB1 and CdvB2 as close paralogues that share 65% amino-acid identity and 80% similarity.…”

“…Under this model, CdvB1 and CdvB2 are treated as being equivalent in terms of their ability to drive scission [22]. This fits with their colocalisation [22] and is in keeping with previous studies that identified CdvB1 and CdvB2 as close paralogues that share 65% amino-acid identity and 80% similarity. We wondered, though, if live-cell inspection of cell division events using the Sulfoscope could reveal more details about the roles of CdvB1 and CdvB2.…”

“…Chromosome organization in Sulfolobus is partitioned into transcriptionally active and inactive domains [19], as it is in eukaryotic genomes, and the machinery driving Sulfolobus cell division includes homologues of ESCRT-III and VPS4 [20,21], proteins that execute abscission in many eukaryotic cells. Finally, it has recently been reported that proteasomal degradation is required to initiate ESCRTIII-mediated cell division and to reset the cell cycle in Sulfolobus, which resembles the role it plays in triggering mitotic exit in eukaryotes [22].…”

“…Movie 2), imaged at 75°C using the same setup, suggesting that the process is conserved between these closely related organisms. Risa and collaborators [22], recently put forward a model of ESCRTIII-mediated division for S. acidocaldarius based on data acquired from using fixed cells. These data suggested that cell division is regulated as follows: a rigid CdvB division ring is formed at the equatorial plane of dividing Sulfolobus cells, which functions as a template for the assembly of a contractile ESCRTIII heteropolymer based on two other ESCRTIII proteins, CdvB1 and CdvB2.…”

“…These data suggested that cell division is regulated as follows: a rigid CdvB division ring is formed at the equatorial plane of dividing Sulfolobus cells, which functions as a template for the assembly of a contractile ESCRTIII heteropolymer based on two other ESCRTIII proteins, CdvB1 and CdvB2. Sudden degradation of CdvB via the archaeal proteasome then triggers division by allowing the CdvB1 and CdvB2 ring to undergo a change in curvature to induce membrane constriction and scission [22]. Under this model, CdvB1 and CdvB2 are treated as being equivalent in terms of their ability to drive scission [22].…”