Surface layers (S-layers) are components of the cell walls throughout the Bacteria and the Archaea that provide protection for microorganisms against diverse environmental stresses, including metal stress. We have previously characterized the process by which S-layers serve as a nucleation site for metal mineralization in an archaeon for which the S-layer represents the only cell wall component. Here, we test the hypothesis originally proposed in cyanobacteria that a “shedding” mechanism exists for replacing S-layers that have become mineral-encrusted, using Lysinibacillus sp. TchIII 20n38, metallotolerant gram-positive bacterium, 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, depending on physiological state of the cells and metal exposure times, leading to the encrustation of the S-layer and changes in the cell morphology as observed by scanning electron microscopy. Using Nanoscale Secondary Ion Mass Spectrometry, we show that mineral-encrusted S-layers are shed by the bacterial cells after a period of latency (2 days under the conditions tested) in a heterogeneous fashion likely reflecting natural variations in metal stress resistance. The emerging cells regenerate new S-layers as part of their cell wall structure. Given the wide diversity of S-layer bearing prokaryotes, S-layer shedding may represent an important mechanism for microbial survival in metal-contaminated environments.
12Surface layers (S-layers) are self-assembling, ordered structures composed of repeating protein 13 subunits found as components of the cell walls throughout the Bacteria and the Archaea. S-layers act 14as an interface between prokaryotic cells and their surrounding environment, and provide protection 15 for microorganisms against diverse environmental stresses including heavy metal stress. We have 16 previously characterized the process by which S-layers serve as a nucleation site for metal 17 mineralization in the presence of high concentration of metals. Here, we test the hypothesis originally 18proposed in cyanobacteria that a "shedding" mechanism exists in prokaryotes for replacing S-layers 19 that have become mineral-encrusted. We used a metallotolerant gram-positive bacterium bearing an 20 S-layer, Lysinibacillus sp. TchIII 20n38, as a model organism. We characterize for the first time a 21 mechanism for resistance to metals through S-layer shedding and regeneration. S-layers nucleate the 22 formation of Fe-mineral on the cell surface, leading to the encrustation of the S-layer. Using a 23 combination of scanning electron microscopy (SEM) and nanoSIMS, we show that mineral-encrusted 24 S-layers are shed by the bacterial cells, and the emerging cells regenerate new S-layers as part of 25 their cell wall structure. This novel mechanism for the survival of prokaryotes in metal-contaminated 26 environments may also provide elements necessary for the development of renewable systems for 27 metal bioremediation. 28
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