Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions

Abstract

Surface layers (S-layers) are self-assembling, ordered structures composed of repeating protein subunits found as components of the cell walls throughout the Bacteria and the Archaea. S-layers act as an interface between prokaryotic cells and their surrounding environment, and provide protection for microorganisms against diverse environmental stresses including heavy metal stress. We have previously characterized the process by which S-layers serve as a nucleation site for metal mineralization in the presence of high concentration of metals. Here, we test the hypothesis originally proposed in cyanobacteria that a \"shedding\" mechanism exists in prokaryotes for replacing S-layers that have become mineral-encrusted. We used a metallotolerant gram-positive bacterium bearing an S-layer, Lysinibacillus sp. TchIII 20n38, as a model organism. We characterize for the first time a mechanism for resistance to metals through S-layer shedding and regeneration. S-layers nucleate the formation of Fe-mineral on the cell surface, leading to the encrustation of the S-layer. Using a combination of scanning electron microscopy (SEM) and nanoSIMS, we show that mineral-encrusted S-layers are shed by the bacterial cells, and the emerging cells regenerate new S-layers as part of their cell wall structure. This novel mechanism for the survival of prokaryotes in metal-contaminated environments may also provide elements necessary for the development of renewable systems for metal bioremediation.