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

Archjana Chandramohan,Carine Lombard,Severine Zirah,Elodie Duprat,Adrienne Kish,Laurent Remusat

doi:10.3389/fmicb.2018.03210

Abstract

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.

Highlights

Environmental contamination by metals and radionuclides from activities such as mining and nuclear power generation pose a serious risk to human health
TchIII 20n38, is a metallotolerant gram-positive bacterium, possessing a cell envelope composed of the plasma membrane surrounded by a thick layer of peptidoglycan capped by an surface layer (S-layer) forming an ordered structure at the cell surface
Such interactions between Lysinibacillus sp. cells and metals can lead to cell surface mineralization, biosorption, or intracellular bioaccumulation, depending on the depending on the types of metals present and physicochemical parameters such as pH

Summary

Introduction

Environmental contamination by metals and radionuclides from activities such as mining and nuclear power generation pose a serious risk to human health. Lysinibacillus [formerly classified as part of the Bacillus genre (Ahmed et al, 2007)] gram-positive bacteria, with a peptidoglycan cell wall enclosed by a surface layer (“S-layer”) attached non-covalently to the lipopolysaccharides of the outer membrane (reviewed in Sleytr et al, 2014). These S-layers have proven to be a key mechanism for metallotolerance in Lysinibacillus as they have been shown to bind U, Pd(II), Cu, Pt(II), and Au(III) (Pollmann et al, 2006)

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