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Abstract
Zinc oxide nanoparticles (ZnO NPs) are an important antimicrobial additive in many industrial applications. However, mass-produced ZnO NPs are ultimately disposed of in the environment, which can threaten soil-dwelling microorganisms that play important roles in biodegradation, nutrient recycling, plant protection, and ecological balance. This study sought to understand how ZnO NPs affect Bacillus subtilis, a plant-beneficial bacterium ubiquitously found in soil. The impact of ZnO NPs on B. subtilis growth, FtsZ ring formation, cytosolic protein activity, and biofilm formation were assessed, and our results show that B. subtilis growth is inhibited by high concentrations of ZnO NPs (≥ 50 ppm), with cells exhibiting a prolonged lag phase and delayed medial FtsZ ring formation. RedoxSensor and Phag-GFP fluorescence data further show that at ZnO-NP concentrations above 50 ppm, B. subtilis reductase activity, membrane stability, and protein expression all decrease. SDS-PAGE Stains-All staining results and FT-IR data further demonstrate that ZnO NPs negatively affect exopolysaccharide production. Moreover, it was found that B. subtilis biofilm surface structures became smooth under ZnO-NP concentrations of only 5–10 ppm, with concentrations ≤ 25 ppm significantly reducing biofilm formation activity. XANES and EXAFS spectra analysis further confirmed the presence of ZnO in co-cultured B. subtilis cells, which suggests penetration of cell membranes by either ZnO NPs or toxic Zn+ ions from ionized ZnO NPs, the latter of which may be deionized to ZnO within bacterial cells. Together, these results demonstrate that ZnO NPs can affect B. subtilis viability through the inhibition of cell growth, cytosolic protein expression, and biofilm formation, and suggest that future ZnO-NP waste management strategies would do well to mitigate the potential environmental impact engendered by the disposal of these nanoparticles.
Highlights
Zinc oxide nanoparticles (ZnO NPs) are known to be effective against many types of bacteria and fungi, both under ambient illumination and in the absence of ultraviolet (UV) light [1,2,3,4,5,6,7].PLOS ONE | DOI:10.1371/journal.pone.0128457 June 3, 2015B. subtilis Growth & Biofilm Inhibition by ZnO NPsAntifouling paints have increasingly replaced bulk ZnO with ZnO NPs, due to their superior antibacterial properties [8]
This study investigated the effects of ZnO NPs against B. subtilis planktonic and biofilm cells, to elucidate the physiological consequences of exposure to ZnO NPs
We found that ZnO-NP concentrations exceeding 50 ppm slow bacterial growth and prolong the lag phase
Summary
Zinc oxide nanoparticles (ZnO NPs) are known to be effective against many types of bacteria and fungi, both under ambient illumination and in the absence of ultraviolet (UV) light [1,2,3,4,5,6,7].PLOS ONE | DOI:10.1371/journal.pone.0128457 June 3, 2015B. subtilis Growth & Biofilm Inhibition by ZnO NPsAntifouling paints have increasingly replaced bulk ZnO with ZnO NPs, due to their superior antibacterial properties [8]. Various morphologies of ZnO NPs have been studied in order to elucidate the mechanisms underlying their antimicrobial effects, and the precise mechanism remains unclear, several theories have been proposed, including the generation of reactive oxygen species (ROS) [4] or the release of cell membrane-damaging Zn2+ ions [12]. ROS are produced by ZnO NPs under light irradiation at frequencies of 368 nm or above [4, 13, 14], and can induce a range of biological responses in bacterial cells [15,16,17]. Studies have shown that ZnO-NP antibacterial activity against Escherichia coli and Candida albicans may be due to lethal hydroxyl radicals generated by interactions between ZnO NPs and water [18, 19]. Gram-positive bacteria, such as Staphylococcus aureus, are more sensitive to ZnO NPs than gram-negative bacteria such as Escherichia coli [3, 22]
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