Abstract
In contrast to many nanotoxicity studies where nanoparticles (NPs) are observed to be toxic or reduce viable cells in a population of bacteria, we observed that increasing concentration of TiO2 NPs increased the cell survival of Bacillus subtilis in autolysis-inducing buffer by 0.5 to 5 orders of magnitude over an 8 hour exposure. Molecular investigations revealed that TiO2 NPs prevent or delay cell autolysis, an important survival and growth-regulating process in bacterial populations. Overall, the results suggest two potential mechanisms for the disruption of autolysis by TiO2 NPs in a concentration dependent manner: (i) directly, through TiO2 NP deposition on the cell wall, delaying the collapse of the protonmotive-force and preventing the onset of autolysis; and (ii) indirectly, through adsorption of autolysins on TiO2 NP, limiting the activity of released autolysins and preventing further lytic activity. Enhanced darkfield microscopy coupled to hyperspectral analysis was used to map TiO2 deposition on B. subtilis cell walls and released enzymes, supporting both mechanisms of autolysis interference. The disruption of autolysis in B. subtilis cultures by TiO2 NPs suggests the mechanisms and kinetics of cell death may be influenced by nano-scale metal oxide materials, which are abundant in natural systems.
Highlights
In contrast to many nanotoxicity studies where nanoparticles (NPs) are observed to be toxic or reduce viable cells in a population of bacteria, we observed that increasing concentration of TiO2 NPs increased the cell survival of Bacillus subtilis in autolysis-inducing buffer by 0.5 to 5 orders of magnitude over an 8 hour exposure
In gram-positive bacteria, such as Bacillus subtilis, the autolytic process occurs in the cell wall, which is comprised of a matrix of peptidoglycan, teichoic acids, autolysins, and a proton gradient
It is possible that the mode of prevention arises from the direct interaction between TiO2 NPs and the outer layer of wall teichoic acids that make up the bacteria-nanoparticle interface
Summary
In contrast to many nanotoxicity studies where nanoparticles (NPs) are observed to be toxic or reduce viable cells in a population of bacteria, we observed that increasing concentration of TiO2 NPs increased the cell survival of Bacillus subtilis in autolysis-inducing buffer by 0.5 to 5 orders of magnitude over an 8 hour exposure. The self-digestion of the cell wall, is associated with several essential cell functions in bacteria, including spore formation, providing nutrients for persisting cells, and the transfer of genetic material to the remaining population[3,9]. In gram-positive bacteria, such as Bacillus subtilis, the autolytic process occurs in the cell wall, which is comprised of a matrix of peptidoglycan, teichoic acids, autolysins, and a proton gradient. Jolliffe et al.[12] demonstrated that when deprived of a carbon source, the PMF of B. subtilis collapses, leading to autolysis, characterized by the self-digestion of the cellular envelope and subsequent release of cytoplasmic materials to the surrounding environment (Fig. 1). Under more favorable cell growth conditions, where nutrients are abundant, autolysins are spatiotemporally activated within the peptidoglycan matrix in a controlled process where they mediate essential tasks such as peptidoglycan turnover, cellular division, and sporulation. The orderly cell wall proton and charge distribution is lost, which could lead to the uncontrolled confirmation of teichoic acids, giving rise to unlimited autolytic activity
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