The patterned assembly and stepwise Vps4-mediated disassembly of composite ESCRT-III polymers drives archaeal cell division

Abstract

ESCRT-III family proteins form composite polymers that deform and cut membrane tubes in the context of a wide range of cell biological processes across the tree of life. In reconstituted systems, sequential changes in the composition of ESCRT-III polymers induced by the AAA–adenosine triphosphatase Vps4 have been shown to remodel membranes. However, it is not known how composite ESCRT-III polymers are organized and remodeled in space and time in a cellular context. Taking advantage of the relative simplicity of the ESCRT-III–dependent division system in Sulfolobus acidocaldarius , one of the closest experimentally tractable prokaryotic relatives of eukaryotes, we use super-resolution microscopy, electron microscopy, and computational modeling to show how CdvB/CdvB1/CdvB2 proteins form a precisely patterned composite ESCRT-III division ring, which undergoes stepwise Vps4-dependent disassembly and contracts to cut cells into two. These observations lead us to suggest sequential changes in a patterned composite polymer as a general mechanism of ESCRT-III–dependent membrane remodeling.

The canonical single-stranded DNA binding protein SSB is not an essential replication protein but an RNA chaperon in the hyperthermophilic archaeonSaccharolobus islandicusREY15A

“…The reason behind the differences between ours and the recent report is not clear, it could be due to difference between two microbes. For example, S. acidocaldarius differs from S. islandicus in several processes, such as cell division (62,63).…”

Roles of ESCRT-III polymers in cell division across the tree of life

“…ESCRT-III filaments can also form hetero-polymers (e.g. Vps2/Vps24 or CHMP2/CHMP3) and composite filaments generated via the lateral association of different homopolymers [ 79 ], which may widen the range of preferred geometries that the composite filament can access. Because each filament has a preferred geometry, filaments recruited into composite polymers that are forced to deviate from their ideal shape can store mechanical energy that can be later deployed to remodel the membrane [ 72 , 77 , 80 ] once neighbouring filaments that constrain it have been removed by Vps4.…”

“…Although the detailed genetic analysis of this Cdv cluster is complicated by the fact that the genes for CdvA, B and C are all essential for viability [ 124 , 125 ], the interaction between CdvA and CdvB proteins (mediated via complementation of the broken winged helix domain in CdvB by CdvA) has been shown to be important for division, along with the AAA-ATPase activity of the Vps4 homologue, CdvC [ 79 , 118 , 124 ]. In parallel, biochemical and structural studies have revealed that both CdvA and CdvB form polymers that can associate with membranes [ 120 , 121 ].…”

STORM Super-Resolution Visualization of Self-Assembled γPFD Chaperone Ultrastructures in Methanocaldococcus jannaschii

“…While fluorescence microscopy provides the desired molecular specificity, − the ∼1 μm size of archaea makes it difficult to resolve subcellular structures with the ∼300 nm resolution afforded by conventional, diffraction-limited microscopy. Recent advances in super-resolution microscopy (SRM) have enabled subdiffractional imaging in biological specimens , and in vitro filaments. − For archaeal imaging, 3D-structured illumination microscopy, super-resolution radial fluctuations, stimulated emission depletion microscopy, and fluorescence photoactivated localization microscopy have been applied to investigate DNA replication, cell division, − and spatial organization, bringing valuable sights down to ∼100 nm spatial resolution.…”