Abstract
The ZnO nanoparticle (NP) effects on typical ammonia-oxidizing bacteria, Nitrosomonas europaea in a chemostat bioreactor, and the cells’ toxicity adaptation and recovery potentials were explored. Hardly any inhibition was observed when the NP concentration was high up to 10 mg/L. The cells exposed to 50 mg/L ZnO NPs displayed time-dependent impairment and recovery potentials in terms of cell density, membrane integrity, nitrite production rate, and ammonia monooxygenase activity. The 6-h NP stress impaired cells were nearly completely restored during a 12-h recovery incubation, while the longer exposure time would cause irretrievable cell damage. Microarray analysis further indicated the transcriptional adaptation of N. europaea to NP stress. The regulations of genes encoding for membrane permeability or osmoprotectant, membrane integrity preservation, and inorganic ion transport during NP exposure and cell recovery revealed the importance of membrane fixation and the associated metabolisms for cells’ self-protection and the following recovery from NP stress. The oxidative phosphorylation, carbon assimilation, and tricarboxylic acid (TCA) cycling pathways involved in the cells’ antitoxicity activities and would promote the energy production/conversion efficiency for cell recovery. The heavy metal resistance, histidine metabolism, toxin-antitoxin defense, glycolysis, and sulfate reduction pathways were also suggested to participate in the cell detoxication and recovery processes. All these findings provided valuable insights into the mechanisms of cell-mediated ZnO NP cytotoxicity and their potential impacts on wastewater nitrogen removal system.
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References
Alito CL, Gunsch CK (2014) Assessing the effects of silver nanoparticles on biological nutrient removal in bench-scale activated sludge sequencing batch reactors. Environ Sci Technol 48(2):970–976. doi:10.1021/es403640j
Arnaout CL, Gunsch CK (2012) Impacts of silver nanoparticle coating on the nitrification potential of Nitrosomonas europaea. Environ Sci Technol 46(10):5387–5395. doi:10.1021/es204540z
Baker TJ, Tyler CR, Galloway TS (2014) Impacts of metal and metal oxide nanoparticles on marine organisms. Environ Pollut 186:257–271. doi:10.1016/j.envpol.2013.11.014
Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J, Sayavedra-Soto L, Arciero D, Hommes N, Whittaker M, Arp D (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185(9):2759–2773. doi:10.1128/jb.185.9.2759-2773.2003
Chen J, Tang YQ, Li Y, Nie Y, Hou L, Li XQ, Wu XL (2014) Impacts of different nanoparticles on functional bacterial community in activated sludge. Chemosphere 104:141–148. doi:10.1016/j.chemosphere.2013.10.082
Fabrega J, Tantra R, Amer A, Stolpe B, Tomkins J, Fry T, Lead JR, Tyler CR, Galloway TS (2012) Sequestration of zinc from zinc oxide nanoparticles and life cycle effects in the sediment dweller amphipod Corophium volutator. Environ Sci Technol 46(2):1128–1135. doi:10.1021/es202570g
Fang X, Yu R, Li B, Somasundaran P, Chandran K (2010) Stresses exerted by ZnO, CeO2 and anatase TiO2 nanoparticles on the Nitrosomonas europaea. J Colloid Interf Sci 348(2):329–334. doi:10.1016/j.jcis.2010.04.075
Feris K, Otto C, Tinker J, Wingett D, Punnoose A, Thurber A, Kongara M, Sabetian M, Quinn B, Hanna C (2010) Electrostatic interactions affect nanoparticle-mediated toxicity to gram-negative bacterium Pseudomonas aeruginosa PAO1. Langmuir 26(6):4429–4436. doi:10.1021/la903491z
Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43(24):9216–9222. doi:10.1021/es9015553
Greer S, Perham RN (1986) Glutathione reductase from Escherichia coli: cloning and sequence analysis of the gene and relationship to other flavoprotein disulfide oxidoreductases. Biochemistry 25(9):2736–2742. doi:10.1021/bi00357a069
Gvakharia B, Permina E, Gelfand M, Bottomley P, Sayavedra-Soto L, Arp D (2007) Global transcriptional response of Nitrosomonas europaea to chloroform and chloromethane. Appl Environ Microbiol 73(10):3440–3445. doi:10.1128/AEM.02831-06
Hooper AB, Vannelli T, Bergmann DJ, Arciero DM (1997) Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Van Leeuwenhoek 71(1–2):59–67. doi:10.1023/a:1000133919203
Hou LL, Xia J, Li KY, Chen J, Wu XL, Li XQ (2013) Removal of ZnO nanoparticles in simulated wastewater treatment processes and its effects on COD and NH4 + −N reduction. Water Sci Technol 67(2):254–260. doi:10.2166/wst.2012.530
Keilin D, Hartree EF (1939) Cytochrome and cytochrome oxidase. Proc R Soc of Lond B Biol Sci 127(847):167–191. doi:10.1098/rspb.1939.0016
Kumar S, Nicholas DJD (1982) A protonmotive force-dependent adenosine-5′ triphosphate synthesis in spheroplasts of Nitrosomonas europaea. FEMS Microbiol Lett 14(1):21–25. doi:10.1111/j.1574-6968.1982.tb08627.x
Kumar A, Pandey AK, Singh SS, Shanker R, Dhawan A (2011) Cellular uptake and mutagenic potential of metal oxide nanoparticles in bacterial cells. Chemosphere 83(8):1124–1132. doi:10.1016/j.chemosphere.2011.01.025
Landa P, Prerostova S, Petrova S, Knirsch V, Vankova R, Vanek T (2015) The transcriptomic response of Arabidopsis thaliana to zinc oxide: a comparison of the impact of nanoparticle, bulk, and ionic zinc. Environ Sci Technol 49(24):14537–14545. doi:10.1021/acs.est.5b03330
Lauchnor EG, Radniecki TS, Semprini L (2011) Inhibition and gene expression of Nitrosomonas europaea biofilms exposed to phenol and toluene. Biotechnol Bioeng 108(4):750–757. doi:10.1002/bit.22999
Li Y, Zhang W, Niu JF, Chen YS (2012) Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano 6(6):5164–5173. doi:10.1021/nn300934k
Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles—a review. Environ Pollut 172:76–85. doi:10.1016/j.envpol.2012.08.011
Ma R, Levard C, Judy JD, Unrine JM, Durenkamp M, Martin B, Jefferson B, Lowry GV (2014) Fate of zinc oxide and silver nanoparticles in a pilot wastewater treatment plant and in processed biosolids. Environ Sci Technol 48(1):104–112. doi:10.1021/es403646x
Mobarry BK, Wagner M, Urbain V, Rittmann BE, Stahl DA (1996) Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl Environ Microbiol 62(6):2156–2162
Moeck GS, Coulton JW (1998) TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 28(4):675–681. doi:10.1046/j.1365-2958.1998.00817.x
Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(5761):622–627. doi:10.1126/science.1114397
Park S, Ely RL (2008) Genome-wide transcriptional responses of Nitrosomonas europaea to zinc. Arch Microbiol 189(6):541–548. doi:10.1007/s00203-007-0341-7
Park S, Ely RL (2009) Whole-genome transcriptional and physiological responses of Nitrosomonas europaea to cyanide: identification of cyanide stress response genes. Biotechnol Bioeng 102(6):1645–1653. doi:10.1002/bit.22194
Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanopart Res 14(9):1109. doi:10.1007/s11051-012-1109-9
Radniecki TS, Dolan ME, Semprini L (2008) Physiological and transcriptional responses of Nitrosomonas europaea to toluene and benzene inhibition. Environ Sci Technol 42(11):4093–4098. doi:10.1021/es702623s
Radniecki TS, Semprini L, Dolan ME (2009) Expression of merA, amoA and hao in continuously cultured Nitrosomonas europaea cells exposed to zinc chloride additions. Biotechnol Bioeng 102(2):546–553. doi:10.1002/bit.22069
Radniecki TS, Stankus DP, Neigh A, Nason JA, Semprini L (2011) Influence of liberated silver from silver nanoparticles on nitrification inhibition of Nitrosomonas europaea. Chemosphere 85(1):43–49. doi:10.1016/j.chemosphere.2011.06.039
SEPAC (2002) Methods for monitor and analysis of water and wastewater, 4th edn. China Environment Science Press (in Chinese), Beijing
Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76. doi:10.1016/j.envpol.2013.10.004
Vollmer W, Blanot D, De Pedro M (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32(2):149–167
Wang H, Wu F, Meng W, White JC, Holden PA, Xing B (2013) Engineered nanoparticles may induce genotoxicity. Environ Sci Technol 47(23):13212–13214. doi:10.1021/es404527d
Wang ST, Li SP, Wang WQ, You H (2015) The impact of zinc oxide nanoparticles on nitrification and the bacterial community in activated sludge in an SBR. RSC Adv 5(82):67335–67342. doi:10.1039/C5RA07106B
Wang S, Gao M, She Z, Zheng D, Jin C, Guo L, Zhao Y, Li Z, Wang X (2016) Long-term effects of ZnO nanoparticles on nitrogen and phosphorus removal, microbial activity and microbial community of a sequencing batch reactor. Bioresour Technol 216:428–436. doi:10.1016/j.biortech.2016.05.099
Weber FJ, deBont JAM (1996) Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. BBA-Bioenergetics 1286(3):225–245. doi:10.1016/s0304-4157(96)00010-x
Westerhoff P, Song G, Hristovski K, Kiser MA (2011) Occurrence and removal of titanium at full scale wastewater treatment plants: implications for TiO2 nanomaterials. J Environ Monit 13(5):1195–1203. doi:10.1039/c1em10017c
Westerhoff PK, Kiser A, Hristovski K (2013) Nanomaterial removal and transformation during biological wastewater treatment. Environ Eng Sci 30(3):109–117. doi:10.1089/ees.2012.0340
Whittaker M, Bergmann D, Arciero D, Hooper AB (2000) Electron transfer during the oxidation of ammonia by the chemolithotrophic bacterium Nitrosomonas europaea. BBA-Bioenergetics 1459(2–3):346–355. doi:10.1016/s0005-2728(00)00171-7
Xia T, Kovochich M, Liong M, Madler L, Gilbert B, Shi HB, Yeh JI, Zink JI, Nel AE (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2(10):2121–2134. doi:10.1021/nn800511k
Xiao Y, Vijver MG, Chen G, Peijnenburg WJGM (2015) Toxicity and accumulation of Cu and ZnO nanoparticles in Daphnia magna. Environ Sci Technol 49(7):4657–4664. doi:10.1021/acs.est.5b00538
Yu R, Fang X, Somasundaran P, Chandran K (2015) Short-term effects of TiO2, CeO2, and ZnO nanoparticles on metabolic activities and gene expression of Nitrosomonas europaea. Chemosphere 128:207–215. doi:10.1016/j.chemosphere.2015.02.002
Yu R, Wu J, Liu M, Chen L, Zhu G, Lu H (2016a) Physiological and transcriptional responses of Nitrosomonas europaea to TiO2 and ZnO nanoparticles and their mixtures. Environ Sci Pollut Res Int 23(13):13023–13034. doi:10.1007/s11356-016-6469-8
Yu R, Wu J, Liu M, Zhu G, Chen L, Chang Y, Lu H (2016b) Toxicity of binary mixtures of metal oxide nanoparticles to Nitrosomonas europaea. Chemosphere 153:187–197. doi:10.1016/j.chemosphere.2016.03.065
Zhao J, Wang Z, Dai Y, Xing B (2013) Mitigation of CuO nanoparticle-induced bacterial membrane damage by dissolved organic matter. Water Res 47(12):4169–4178. doi:10.1016/j.watres.2012.11.058
Zheng XO, Wu R, Chen YG (2011) Effects of ZnO nanoparticles on wastewater biological nitrogen and phosphorus removal. Environ Sci Technol 45(7):2826–2832. doi:10.1021/es2000744
Zheng X, Su Y, Chen Y, Wan R, Liu K, Li M, Yin D (2014) Zinc oxide nanoparticles cause inhibition of microbial denitrification by affecting transcriptional regulation and enzyme activity. Environ Sci Technol 48(23):13800–13807. doi:10.1021/es504251v
Zhu MM, Skraly FA, Cameron DC (2001) Accumulation of methylglyoxal in anaerobically grown Escherichia coli and its detoxification by expression of the Pseudomonas putida glyoxalase I gene. Metab Eng 3(3):218–225. doi:10.1006/mben.2001.0186
Acknowledgements
This study was supported by National Natural Science Foundation of China (No. 51678134 and No. 51208092), Natural Science Foundation of Jiangsu Province of China (BK2012124), and Doctoral Fund of Ministry of Education of China (20120092120010). We sincerely appreciate Professor Chang-ping Yu at Institute of Urban Environment at Chinese Academy of Science for his kind offer of N. europaea cultures.
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Wu, J., Lu, H., Zhu, G. et al. Regulation of membrane fixation and energy production/conversion for adaptation and recovery of ZnO nanoparticle impacted Nitrosomonas europaea . Appl Microbiol Biotechnol 101, 2953–2965 (2017). https://doi.org/10.1007/s00253-017-8092-0
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DOI: https://doi.org/10.1007/s00253-017-8092-0