The mechanics of a continuous self-assembling surface-layer aids cell division in an archaeon

The surface layer or "S-layer" is a planar lattice of glycosylated proteins that coats a wide range of archaea and bacteria instead of a classical cell wall or capsular polysaccharides, insulating them from the extracellular space and providing the cell membrane with physical support. Although the S-layers role as a mechanical support for the membrane might be expected to hinder cell division, we show that in rapidly dividing Sulfolobus acidocaldarius cells, the S-layer protein SlaA self-assembles into flexible lattice that helps flattens the cytokinetic furrow to accelerate ESCRT-III dependent cell division - a role that is especially important under conditions of mechanical stress. Taken together, these results generated using mutational analysis, live and fixed cellular imaging, along with electron cryomicroscopy, define the rules governing S-layer self-assembly and show how the mechanical properties of flexible lattice coats can enhance membrane functions to both physically support a cell and help to drive ESCRT-III dependent cell division. Significance statementThe bounding membrane of a cell must be protected from environmental insults. In many bacteria and archaea that lack a cell wall, this is achieved by an enveloping S-layer. By virtue of its rigid, planar structure, the S-layer is also expected to act as a barrier to the cell shape changes required for cytokinesis. In this study of the S-layer lattice in the archaeon Sulfolobus acidocaldarius however, we demonstrate a role for this self-assembling mechanical support in re-shaping the cytokinetic furrow as an aid to ESCRT-III-mediated division. In showing how mechanically active and passive structures can work together to give rise to mechanically stable cells that can divide, this reconciles what seems like a trade-off between resilience and flexibility.