A Closer Look at the Surface. Structural biology of prokaryotic cell surface molecules.

Abstract

Most prokaryotes are encapsulated by a para-crystalline (glyco)protein array termed surface layer or S-layer, which mediates the interaction between the cell and its environment. Despite wide variation between prokaryotes and their S-layer protein sequences, S-layers share underlying organisational and assembly principles. Here, I used cryogenic electron microscopy (cryo-EM) and cryogenic electron tomography (cryo-ET) to study the molecular structure and organisation of the cell surfaces of archaea Nitrosopumilus maritimus and Pyrobaculum arsenaticum, the Gram-positive bacterium Paenibacillus alvei and the evolutionarily deep-branching diderm bacterium Deinococcus radiodurans. My work provides biological context to our structural knowledge of S-layer proteins and reveals common themes in S-layer protein structures. This work, along with other results, demonstrates that S-layers display a remarkable level of adaptation to the physical challenges of the prokaryotic environment, showing that higher order symmetric organisation and the presence of Immunoglobulin-like domains are ubiquitous in prokaryotic S-layers. Our combined approach of cryo-EM and cryo-ET shows potential for high-throughput S-layer structure determination and great promise for harvesting these structures for application in biotechnology. With our results, we have contributed to broadening the diversity of S-layer structural knowledge and of the underlying principles of prokaryotic cell surface biology.