Abstract
This study investigated the cytotoxicity, genotoxicity, and growth inhibition effects of four different inorganic nanoparticles (NPs) such as aluminum (nAl), iron (nFe), nickel (nNi), and zinc (nZn) on a dibenzofuran (DF) degrading bacterium Agrobacterium sp. PH-08. NP (0–1,000 mg L−1) -treated bacterial cells were assessed for cytotoxicity, genotoxicity, growth and biodegradation activities at biochemical and molecular levels. In an aqueous system, the bacterial cells treated with nAl, nZn and nNi at 500 mg L−1 showed significant reduction in cell viability (30–93.6 %, p < 0.05), while nFe had no significant inhibition on bacterial cell viability. In the presence of nAl, nZn and nNi, the cells exhibited elevated levels of reactive oxygen species (ROS), DNA damage and cell death. Furthermore, NP exposure showed significant (p < 0.05) impairment in DF and catechol biodegradation activities. The reduction in DF biodegradation was ranged about 71.7–91.6 % with single NPs treatments while reached up to 96.3 % with a mixture of NPs. Molecular and biochemical investigations also clearly revealed that NP exposure drastically affected the catechol-2,3-dioxygenase activities and its gene (c23o) expression. However, no significant inhibition was observed in nFe treatment. The bacterial extracellular polymeric materials and by-products from DF degradation can be assumed as key factors in diminishing the toxic effects of NPs, especially for nFe. This study clearly demonstrates the impact of single and mixed NPs on the microbial catabolism of xenobiotic-degrading bacteria at biochemical and molecular levels. This is the first study on estimating the impact of mixed NPs on microbial biodegradation.
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Adams LK, Lyon DY, Alvarez PJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40:3527–3532
Agasti SS, Rana S, Park MH, Kim CK, You CC, Rotello VM (2010) Nanoparticles for detection and diagnosis. Adv Drug Deliv Rev 62:316–328
Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR (2009a) Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634–641
Auffan M, Rose J, Wiesner MR, Bottero JY (2009b) Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ Pollut 157:1127–1133
Baek YW, An YJ (2011) Microbial toxicity of metal oxide nanoparticles (CuO, NiO, ZnO, and Sb2O3) to Escherichia coli, Bacillus subtilis, and Streptococcus aureus. Sci Total Environ 409:1603–1608
Braud A, Geoffroy V, Hoegy F, Mislin GLA, Schalk IJ (2010) Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ Microbiol Rep 2:419–425
Crane RA, Scott TB (2012) Nanoscale zero-valent iron: future prospects for an emerging water treatment technology. J Hazard Mater 211–212:112–125
Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2012) CuO and ZnO nanoparticles differently affect the secretion of fluorescent siderophores in the beneficial root colonizer, Pseudomonas chlororaphis O6. Nanotoxicology 6:635–642
Elsaesser A, Howard CV (2011) Toxicology of nanoparticles. Adv Drug Deliv Rev 64:129–137
Fortnagel P, Harms H, Wittich RH, Krohn S, Meyer H, Sinnwell V, Wilkes H, Francke W (1990) Metabolism of dibenzofuran by Pseudomonas sp. strain HH69 and the mixed culture HH27. Appl Environ Microbiol 56:1148–1156
Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS (2007) Comparative Toxicity of Nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a freshwater microalgae (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41:8484–8490
García-Saucedo C, Field JA, Otero-Gonzalez L, Sierra-Álvarez R (2011) Low toxicity of HfO2, SiO2, Al2O3 and CeO2 nanoparticles to the yeast, Saccharomyces cerevisiae. J Hazard Mater 192:1572–1579
Gonzalez-Estrella J, Sierra-Alvarez R, Field R (2013) Toxicity assessment of inorganic nanoparticles to acetoclastic and hydrogenotrophic methanogenic activity in anaerobic granular sludge. J Hazard Mater 260:278–285
Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625
Jiang W, Yang K, Vachet RW, Xing B (2010) Interaction between oxide nanoparticles and biomolecules of the bacterial cell envelope as examined by infrared spectroscopy. Langmuir 26:18071–18077
Joshi N, Ngweny BT, French CE (2012) Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances. J Hazard Mater 241–242:363–370
Jung H, Choi H (2006) Catalytic decomposition of ozone and para-Chlorobenzoic acid (pCBA) in the presence of nanosized ZnO. Appl Catal B 66:288–294
Karn B, Kuiken T, Otto M (2011) Nanotechnology and in situ remediation: a review of the benefits and potential risks. Environ Health Perspect 117:1813–1831
Kim EJ, Kim JH, Azard AM, Chang YS (2011) Facile synthesis and characterization of Fe/FeS nanoparticles for environmental applications. ACS Appl Mater Interfaces 3:1457–1462
Kim YM, Murugesan K, Chang YY, Kim EJ, Chang YS (2012) Degradation of polybrominated diphenyl ethers by a sequential treatment with nanoscale zero valent iron and aerobic biodegradation. J Chem Technol Biot 87:216–224
Kumar A, Pandey AK, Singh SS, Shankera R, Dhawan A (2011a) Engineered ZnO and TiO2 nanoparticles induce oxidative stress and DNA damage leading to reduced viability of Escherichia coli. Free Radical Biol Med 51:1872–1881
Kumar N, Shah V, Walker VK (2011b) Perturbation of an arctic soil microbial community by metal nanoparticles. J Hazard Mater 190:816–822
Le TT, Murugesan K, Nam IH, Jeon JR, Chang YS (2014) Degradation of dibenzofuran via multiple dioxygenation by a newly isolated Agrobacterium sp. PH-08. J Appl Microbiol 116:542–553
Li Z, Greden K, Alvarez PJ, Gregory KB, Lowry GV (2010) Adsorbed polymer and NOM limits adhesion and toxicity of nano scale zerovalent iron to E. coli. Environ Sci Technol 44:3462–3467
Mudunkotuwa IA, Grassian VH (2010) Citric acid adsorption on TiO2 nanoparticles in aqueous suspensions at acidic and circumneutral pH: surface coverage, surface speciation, and its impact on nanoparticle–nanoparticle interactions. J Am Chem Soc 132:14986–14994
Murugesan K, Bokare V, Jeon JR, Kim EJ, Kim JH, Chang YS (2011) Effect of Fe–Pd bimetallic nanoparticles on Sphingomonas sp. PH-07 and a nano-bio hybrid process for triclosan degradation. Bioresour Technol 102:6019–6025
Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22
Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839
Pan X, Redding JE, Wiley PA, Wen L, McConnell JS, Zhang B (2010) Mutagenicity evaluation of metal oxide nanoparticles by the bacterial reverse mutation assay. Chemosphere 79:113–116
Peralta-Videa JR, Zhao L, Lopez-Moreno ML, de la Rosa G, Hong J, Gardea-Torresdey JL (2011) Nanomaterials and the environment: a review for the biennium 2008-2010. J Hazard Mater 186:1–15
Pereira R, Rocha-Santos TA, Antunes FE, Rasteiro MG, Ribeiro R, Gonçalves F, Soares AM, Lopes I (2011) Screening evaluation of the ecotoxicity and genotoxicity of soils contaminated with organic and inorganic nanoparticles: the role of ageing. J Hazard Mater 194:345–354
Pettibone JM, Cwiertny DM, Scherer M, Grassian VH (2008) Adsorption of organic acids on TiO2 nanoparticles: effects of pH, nanoparticle size, and nanoparticle aggregation. Langmuir 24:6659–6667
Sadiq IM, Chowdhury B, Chandrasekaran N, Mukherjee A (2009) Antimicrobial sensitivity of Escherichia coli to alumina nanoparticles. Nanomedicine 5:282–286
Shi L, Günther S, Hübschmann T, Wick LY, Harms H, Müller S (2007) Limits of propidium iodide as a cell viability indicator for environmental bacteria. Cytometry A 71:592–598
Singh N, Manshian B, Jenkins GJ, Griffiths SM, Williams PM, Maffeis TG, Wright CJ, Doak SH (2009) NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 30:3891–3914
Sinha R, Karan R, Sinha A, Khare SK (2011) Interaction and nanotoxic effect of ZnO and Ag nanoparticles on mesophilic and halophilic bacterial cells. Bioresour Technol 102:1516–1520
Skotland T, Iversen TG, Sandvig K (2010) New metal-based nanoparticles for intravenous use: requirements for clinical success with focus on medical imaging. Nanomedicine 6:730–737
Soenen SJ, Rivera-Gil P, Montenegrob JM, Parakb JW, Smedta SCD, Braeckmans K (2011) Cellular toxicity of inorganic nanoparticles: common aspects and guidelines for improved nanotoxicity evaluation. Nano Today 6:446–465
Studer AM, Limbach LK, Van Duc L, Krumeich F, Athanassiou EK, Gerber LC, Moch H, Stark WJ (2010) Nanoparticle cytotoxicity depends on intracellular solubility: comparison of stabilized copper metal and degradable copper oxide nanoparticles. Toxicol Lett 197:169–174
Tong Z, Bischoff M, Nies L, Applegate B, Turco RF (2007) Impact of fullerene (C60) on a soil microbial community. Environ Sci Technol 41:2985–2991
Tratnyek PG, Johnson RL (2006) Nanotechnologies for environmental cleanup. Nano Today 1:44–48
Varima B, Murugesan K, Kim JH, Kim EJ, Chang YS (2012) Integrated hybrid treatment for the remediation of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Sci Total Environ 435–436:563–566
Varima B, Jung JL, Chang YY, Chang YS (2013) Reductive dechlorination of octachlorodibenzo-p-dioxin by nanosized zero-valent zinc: modeling of rate kinetics and congener profile. J Hazard Mater 250–251:397–402
Wani MY, Hashim MA, Nabi F, Malik MA (2011) Nanotoxicity: dimensional and morphological concerns. Adv Phys Chem. doi:10.1155/2011/450912
Yamamoto A, Honma R, Sumita M, Hanawa T (2004) Cytotoxicity evaluation of ceramic particles of different sizes and shapes. J Biomed Mater Res A 68:244–256
Zhou L, Thanh TL, Gong J, Kim JH, Kim EJ, Chang YS (2014) Carboxymethyl cellulose coating decreases toxicity and oxidizing capacity of nanoscale zerovalent iron. Chemosphere 104:155–161
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This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (No. 2011-0028723) and “The GAIA Project” by Korea Ministry of Environment.
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Le, T.T., Murugesan, K., Kim, EJ. et al. Effects of inorganic nanoparticles on viability and catabolic activities of Agrobacterium sp. PH-08 during biodegradation of dibenzofuran. Biodegradation 25, 655–668 (2014). https://doi.org/10.1007/s10532-014-9689-y
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DOI: https://doi.org/10.1007/s10532-014-9689-y