Abstract
The growing use of silver nanoparticles (AgNPs) has created concerns about its potential impacts on natural microbial communities. In this study, the physicochemical properties of AgNPs and its toxicity on natural bacteria Bacillus subtilis (B. subtilis) were investigated in aqueous conditions. The characterization data showed that AgNPs highly aggregated in aqueous conditions, and the hydrodynamic diameter of AgNPs in aqueous conditions was larger than its primary size. The studied AgNPs was less toxic to B. subtilis in estuarine water as compared to that in Milli-Q water and artificial seawater, which might be due to the observed enhanced aggregation of AgNPs in estuarine water. The toxicity of AgNPs to B. subtilis was greatly reduced when their surface contact was blocked by a dialysis membrane. Scanning electron microscope images showed that exposure contact to AgNPs resulted in damage of the microbial cell wall and enhanced formation of fibrillar structures. These results suggest that particle-cell contact is largely responsible for the observed toxicity of AgNPs in B. subtilis. This study can help to understand the potential impacts of AgNPs to natural microbes, especially in the complex aquatic environments.
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Ahmad A, Wei Y, Syed F et al. (2017) The effects of bacteria-nanoparticles interface on the antibacterial activity of green synthesized silver nanoparticles. Microb Pathog 102:133–142. doi:10.1016/j.micpath.2016.11.030
Areepitak T, Ren J (2011) Model simulations of particle aggregation effect on colloid exchange between streams and streambeds. Environ Sci Technol 45:5614–5621. doi:10.1021/es200586v
Barisik M, Atalay S, Beskok A, Qian S (2014) Size dependent surface charge properties of silica nanoparticles. J Phys Chem C 118:1836–1842. doi:10.1021/jp410536n
Bizmark N, Ioannidis MA (2015) Effects of ionic strength on the colloidal stability and interfacial assembly of hydrophobic ethyl cellulose nanoparticles. Langmuir 31:9282–9289. doi:10.1021/acs.langmuir.5b01857
Blinova I, Niskanen J, Kajankari P et al. (2013) Toxicity of two types of silver nanoparticles to aquatic crustaceans Daphnia magna and Thamnocephalus platyurus. Environ Sci Pollut Res 20:3456–3463. doi:10.1007/s11356-012-1290-5
Bondarenko O, Ivask A, Käkinen A et al. (2013) Particle-cell contact enhances antibacterial activity of silver nanoparticles. PLoS ONE 8:e64060. doi:10.1371/journal.pone.0064060
Bone AJ, Matson CW, Colman BP et al. (2015) Silver nanoparticle toxicity to Atlantic killifish (Fundulus heteroclitus) and Caenorhabditis elegans: a comparison of mesocosm, microcosm, and conventional laboratory studies. Environ Toxicol Chem 34:275–282. doi:10.1002/etc.2806
Boopathy R, Kern C, Corbin A (2015) Use of Bacillus consortium in waste digestion and pathogen control in shrimp aquaculture. Int Biodeterior Biodegradation 102:159–164. doi:10.1016/j.ibiod.2015.02.001
Bridier A, Meylheuc T, Briandet R (2013) Realistic representation of Bacillus subtilis biofilms architecture using combined microscopy (CLSM, ESEM and FESEM). Micron 48:65–69. doi:10.1016/j.micron.2013.02.013
Chambers BA, Afrooz ARMN, Bae S et al. (2014) Effects of chloride and ionic strength on physical morphology, dissolution, and bacterial toxicity of silver nanoparticles. Environ Sci Technol 48:761–769. doi:10.1021/es403969x
Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588. doi:10.1021/es703238h
Choi O, Kanjun K, Kim N-J et al. (2008) The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res 42:3066–3074. doi:10.1016/j.watres.2008.02.021
Choi O, Yu CP, Esteban Fernández G, Hu Z (2010) Interactions of nanosilver with Escherichia coli cells in planktonic and biofilm cultures. Water Res 44:6095–6103. doi:10.1016/j.watres.2010.06.069
Dasari TP, Hwang H-M (2010) The effect of humic acids on the cytotoxicity of silver nanoparticles to a natural aquatic bacterial assemblage. Sci Total Environ 408:5817–5823. doi:10.1016/j.scitotenv.2010.08.030
El Badawy AM, Silva RG, Morris B et al. (2011) Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 45:283–287. doi:10.1021/es1034188
Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290. doi:10.1021/es803259g
Fabrega J, Zhang R, Renshaw JC et al. (2011) Impact of silver nanoparticles on natural marine biofilm bacteria. Chemosphere 85:961–966. doi:10.1016/j.chemosphere.2011.06.066
Hanaor D, Michelazzi M, Leonelli C, Sorrell CC (2012) The effects of carboxylic acids on the aqueous dispersion and electrophoretic deposition of ZrO2. J Eur Ceram Soc 32:235–244. doi:10.1016/j.jeurceramsoc.2011.08.015
Ivask A, Elbadawy A, Kaweeteerawat C et al. (2014) Toxicity mechanisms in Escherichia coli vary for silver nanoparticles and differ from ionic silver. ACS Nano 8:374–386. doi:10.1021/nn4044047
Levard C, Hotze EM, Colman BP et al. (2013) Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ Sci Technol 47:13440–13448. doi:10.1021/es403527n
Martinez-Gutierrez F, Boegli L, Agostinho A et al. (2013) Anti-biofilm activity of silver nanoparticles against different microorganisms. Biofouling 29:651–660. doi:10.1080/08927014.2013.794225
Middlemiss KL, Daniels CL, Urbina MA, Wilson RW (2015) Combined effects of UV irradiation, ozonation, and the probiotic Bacillus spp. on growth, survival, and general fitness in European lobster (Homarus gammarus). Aquaculture 444:99–107. doi:10.1016/j.aquaculture.2015.03.028
Nanotechproject (2016) Consumer Products Inventory. http://www.nanotechproject.org/cpi/browse/nanomaterials/silvernanoparticle/. Accessed Aug 2016
Pal S, Tak YK, Song JM (2015) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. J Biol Chem 290:1712–1720. doi:10.1128/AEM.02218-06
Patra S, Liu CQ, Wang FS et al. (2012) Behavior of major and minor elements in a temperate river estuary to the coastal sea. Int J Environ Sci Technol 9:647–654. doi:10.1007/s13762-012-0097-8
Qiao Y, Yang C, Coady DJ et al. (2012) Highly dynamic biodegradable micelles capable of lysing gram-positive and gram-negative bacterial membrane. Biomaterials 33:1146–1153. doi:10.1016/j.biomaterials.2011.10.020
Ribeiro F, Gallego-Urrea JA, Jurkschat K et al. (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466-467:232–241. doi:10.1016/j.scitotenv.2013.06.101
Seitz F, Rosenfeldt RR, Storm K et al. (2015) Effects of silver nanoparticle properties, media pH and dissolved organic matter on toxicity to Daphnia magna. Ecotoxicol Environ Saf 111:263–270. doi:10.1016/j.ecoenv.2014.09.031
Vance ME, Kuiken T, Vejerano EP et al. (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780
Wang Y-W, Cao A, Jiang Y et al. (2014) Superior antibacterial activity of zinc oxide/graphene oxide composites originating from high zinc concentration localized around bacteria. ACS Appl Mater Interfaces 6:2791–2798. doi:10.1021/am4053317
Wirth SM, Lowry GV, Tilton RD (2012) Natural organic matter alters biofilm tolerance to silver nanoparticles and dissolved silver. Environ Sci Technol 46:12687–12696. doi:10.1021/es301521p
Xiu Z-M, Ma J, Alvarez PJJ (2011) Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ Sci Technol 45:9003–9008. doi:10.1021/es201918f
Yin S, Feng C, Li Y et al (2015) Heavy metal pollution in the surface water of the Yangtze Estuary: a 5-year follow-up study. Chemosphere 138:718–725. doi:10.1016/j.chemosphere.2015.07.060
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This study was supported by grants from Natural Science Foundation of China (41101489), the Natural Science Foundation of Guangdong Province, China (s2012010010847), and the New Century Excellent Talents in University from Ministry of Education, China (NECT-12-0181).
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The authors declare that they have no competing interests.
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Yi, J., Cheng, J. Effects of water chemistry and surface contact on the toxicity of silver nanoparticles to Bacillus subtilis . Ecotoxicology 26, 639–647 (2017). https://doi.org/10.1007/s10646-017-1796-1
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DOI: https://doi.org/10.1007/s10646-017-1796-1