Cell cycle dependent coordination of surface layer biogenesis in Caulobacter crescentus

Matthew Herdman, Buse Isbilir, Andriko Kügelgen, Ulrike Schulze, Alan Wainman and Tanmay A. M. Bharat ()
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Matthew Herdman: University of Oxford
Buse Isbilir: MRC Laboratory of Molecular Biology
Andriko Kügelgen: University of Oxford
Ulrike Schulze: MRC Laboratory of Molecular Biology
Alan Wainman: University of Oxford
Tanmay A. M. Bharat: MRC Laboratory of Molecular Biology

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Surface layers (S-layers) are proteinaceous, two-dimensional paracrystalline arrays that constitute a major component of the cell envelope in many prokaryotic species. In this study, we investigated S-layer biogenesis in the bacterial model organism Caulobacter crescentus. Fluorescence microscopy revealed localised incorporation of new S-layer at the poles and mid-cell, consistent with regions of cell growth in the cell cycle. Light microscopy and electron cryotomography investigations of drug-treated bacteria revealed that localised S-layer insertion is retained when cell division is inhibited, but is disrupted upon dysregulation of MreB or lipopolysaccharide. We further uncovered that S-layer biogenesis follows new peptidoglycan synthesis and localises to regions of high cell wall turnover. Finally, correlated cryo-light microscopy and electron cryotomographic analysis of regions of S-layer insertion showed the presence of discontinuities in the hexagonal S-layer lattice, contrasting with other S-layers completed by defined symmetric defects. Our findings present insights into how C. crescentus cells form an ordered S-layer on their surface in coordination with the biogenesis of other cell envelope components.

Date: 2024
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DOI: 10.1038/s41467-024-47529-5

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