Abstract
In this paper, the effects of cerium oxide nanoparticles (CeO2 NPs) on the group bacterial behaviors were elaborated. After 36-h cultivation, the biofilm biomass was enhanced by the sub-lethal concentrations of 0.5 and 2 mg/L CeO2 NP exposure. Meanwhile, the promoted production of total amino acids in microbes further resulted in the increased surface hydrophobicity and percentage aggregation. To resist the CeO2 NPs stress, the biofilm exhibited a double-layer microstructure, with the protein (PRO) and living cells occupying the bottom, the polysaccharide (PS), and dead cells dominating the top. The bacterial diversity was highly suppressed and Citrobacter and Pseudomonas from the phylum of γ-Proteobacteria strongly dominated the biofilm, indicating the selective and enriched effects of CeO2 NPs on resistant bacteria. The stimulated inherent resistance of biofilm was reflected by the reduced adenosine triphosphate (ATP) content after 4 h exposure. The increased levels of reactive oxygen species (ROS) in the treatments of 8 h CeO2 NP exposure led to the upregulated quorum sensing signals of acylated homoserine lactone (AHL) and autoinducer 2 (AI-2), beneficial to mitigating the environmental disturbance of CeO2 NPs. These results provide evidences for the accelerating effects of CeO2 NPs on biofilm formation through oxidative stress, which expand the understanding of the ecological effects of CeO2 NPs.







Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Bassler BL (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109:421–424
Blaser SA, Scheringer M, Macleod M, Hungerbühler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 390:396–409
Bo F, Palmgren R, Keiding K, Nielsen PH (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res 30:1749–1758
Cáp M, Váchová L, Palková Z (2012) Reactive oxygen species in the signaling and adaptation of multicellular microbial communities. Oxidative Med Cell Longev 11:976753
Cappitelli F, Principi P, Sorlini C (2006) Biodeterioration of modern materials in contemporary collections: can biotechnology help? Trends Biotechnol 24:350–354
Chen MY, Duujong L, Yang Z, Peng XF, Lai JY (2006) Fluorescent staining for study of extracellular polymeric substances in membrane biofouling layers. Environ Sci Technol 40:6642–6646
Chen MY, Lee DJ, Tay JH, Show KY (2007) Staining of extracellular polymeric substances and cells in bioaggregates. Appl Microbiol Biotechnol 75:467–474
Collin B, Oostveen E, Tsyusko OV, Unrine JM (2014) Influence of natural organic matter and surface charge on the toxicity and bioaccumulation of functionalized ceria nanoparticles in Caenorhabditis elegans. Environ Sci Technol 48:1280–1289
Dou XY, He LN, Yang ZZ, Wang JL (2010) Reaction of N-acylhomoserine lactones with hydroxyl radicals: rates, products, and effects on signaling activity. Environ Sci Technol 44:7465–7469
Field TR, White A, Elborn JS, Tunney MM (2005) Effect of oxygen limitation on the in vitro antimicrobial susceptibility of clinical isolates of Pseudomonas aeruginosa grown planktonically and as biofilms. Eur J Clin Microbiol 24:677–687
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Fleurke SR, Formentin, Külske (1988) Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium-substratum separation distance. J Bacteriol 170:2027–2030
Gambino M, Cappitelli F (2016) Mini-review: biofilm responses to oxidative stress. Biofouling 32:167–178
García A, Delgado L, Torà JA, Casals E, González E, Puntes V, Font X, Carrera J, Sánchez A (2012) Effect of cerium dioxide, titanium dioxide, silver, and gold nanoparticles on the activity of microbial communities intended in wastewater treatment. J Hazard Mater 199:64–72
Goh SY, Khan SA, Tee KK, Kasim NHA, Yin WF, Chan KG (2016) Quorum sensing activity of Citrobacter amalonaticus L8A, a bacterium isolated from dental plaque. Sci Rep 6:20702
Golowczyc MA, Mobili P, Garrote GL, De LASM, Abraham AG, De Antoni GL (2009) Interaction between lactobacillus kefir and Saccharomyces lipolytica isolated from kefir grains: evidence for lectin-like activity of bacterial surface proteins. J Dairy Res 76:111–116
Gottschalk F, Nowack B (2011) The release of engineered nanomaterials to the environment. J Environ Monit 13:1145–1155
Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966
Hassett DJ, Ma JF, Elkins JG, Mcdermott TR, Ochsner UA, West SE, Huang CT, Fredericks J, Burnett S, Stewart PS (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093
Hou X, Liu S, Zhang Z (2015a) Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge. Water Res 75:51–62
Hou J, You G, Xu Y, Wang C, Wang P, Miao L, Ao Y, Li Y, Lv B (2015b) Effects of CeO2 nanoparticles on biological nitrogen removal in a sequencing batch biofilm reactor and mechanism of toxicity. Bioresour Technol 191:73–78
Hou J, You G, Xu Y, Wang C, Wang P, Miao L, Li Y, Ao Y, Lv B, Yang Y (2016) Long-term effects of CuO nanoparticles on the surface physicochemical properties of biofilms in a sequencing batch biofilm reactor. Appl Microbiol Biotechnol 100:1–11
Hou L, Zhou Q, Wu Q, Gu Q, Sun M, Zhang J (2017) Spatiotemporal changes in bacterial community and microbial activity in a full-scale drinking water treatment plant. Sci Total Environ 625:449–459
Hu X, Liu X, Yang X, Guo F, Su X, Chen Y (2018) Acute and chronic responses of macrophyte and microorganisms in constructed wetlands to cerium dioxide nanoparticles: implications for wastewater treatment. Chem Eng J 348:35–45
Joelsson A, Kan B, Zhu J (2007) Quorum sensing enhances the stress response in Vibrio cholerae. Appl Environ Microbiol 73:3742–3746
Kaldalu N, Mei R, Lewis K (2004) Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob Agents Chemother 48:890–896
Koetsem FV, Verstraete S, Meeren PVD, Laing GD (2015) Stability of engineered nanomaterials in complex aqueous matrices: settling behaviour of CeO2 nanoparticles in natural surface waters. Environ Res 142:207–214
Lalucque H, Silar P (2003) NADPH oxidase: an enzyme for multicellularity? Trends Microbiol 11:9–12
Lam H, Oh DC, Cava F, Takacs CN, Clardy J, Pedro MAD, Waldor MK (2009) D-amino acids govern stationary phase cell wall re-modeling in bacteria. Science 325:1552–1555
Lazareva A, Keller AA (2014) Estimating potential life cycle releases of engineered nanomaterials from wastewater treatment plants. ACS Sustain Chem Eng 2:1656–1665
Maynard AD (2016) Nanotechnology: assessing the risks. Nano Today 1:22–33
Miyaoka Y, Haishima K, Takagi M, Haishima H, Jin A, Yamada Y (2010) Lack of CbrB in Pseudomonas putida affects not only amino acids metabolism but also different stress responses and biofilm development. Environ Microbiol 12:1748–1761
Molin S, Tolkernielsen T (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261
Nakao R, Ramstedt M, Sun NW, Uhlin BE (2012) Enhanced biofilm formation by Escherichia coli LPS mutants defective in Hep biosynthesis. PLoS One 7:e51241
Nguyen D, Visvanathan C, Jacob P, Jegatheesan V (2015) Effects of nano cerium (IV) oxide and zinc oxide particles on biogas production. Int Biodeterior Biodegrad 102:165–171
Palmer J, Flint S, Brooks J (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34:577–588
Pontes MH, Babst M, Lochhead R, Oakeson K, Smith K, Dale C (2008) Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius. Plos One 3:e3541
Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. CSH Perspect Med 2:705–709
Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210
Thill A, Zeyons O, Spalla O, Chauvat F, Jerôme Rose MAA, Flank AM (2006) Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanism. Environ Sci Technol 40:6151–6156
Torres MA (2010) ROS in biotic interactions. Physiol Plant 138:414–429
Tou F, Yi Y, Feng J, Niu Z, Hui P, Qin Y, Guo X, Meng XZ, Min L, Hochella MF (2017) Environmental risk implications of metals in sludges from waste water treatment plants: the discovery of vast stores of metal-containing nanoparticles. Environ Sci Technol 51:4831–4840
Tuinier R, van Casteren WH, Looijesteijn PJ, Schols HA, Voragen AG, Zoon P (2015) Effects of structural modifications on some physical characteristics of exopolysaccharides from Lactococcus lactis. Biopolymers 59:160–166
Uzureau S, Lemaire J, Delaive E, Dieu M, Gaigneaux A, Raes M, Bolle XD, Letesson JJ (2010) Global analysis of quorum sensing targets in the intracellular pathogen Brucella melitensis 16 M. J Proteome Res 9:3200–3217
Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554
Wang S, Gao M, Li Z, She Z, Wu J, Dong Z, Liang G, Zhao Y, Feng G, Wang X (2016) Performance evaluation, microbial enzymatic activity and microbial community of a sequencing batch reactor under long-term exposure to cerium dioxide nanoparticles. Bioresour Technol 220:262–270
Wang P, You G, Hou J, Wang C, Xu Y, Miao L, Feng T, Zhang F (2018) Responses of wastewater biofilms to chronic CeO2 nanoparticles exposure: structural, physicochemical and microbial properties and potential mechanism. Water Res 133:208–217
Wiesner MR, Lowry GV, Jones KL, Jr HM, Di GR, Casman E, Bernhardt ES (2009) Decreasing uncertainties in assessing environmental exposure, risk, and ecological implications of nanomaterials. Environ Sci Technol 43:6458–6462
Xu Y, Wang C, Hou J, Wang P, You G, Miao L, Lv B, Yang Y (2016) Influence of CeO2 NPs on biological phosphorus removal and bacterial community shifts in a sequencing batch biofilm reactor with the differential effects of molecular oxygen. Environ Res 151:21–29
Xu Y, Wang C, Hou J, Wang P, You G, Miao L, Lv B, Yang Y (2017) Effects of cerium oxide nanoparticles on the species and distribution of phosphorus in enhanced phosphorus removal sequencing batch biofilm reactor. Bioresour Technol 227:393–397
Yang L, Hu Y, Liu Y, Zhang J, Ulstrup J, Molin S (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13:1705–1717
You G, Hou J, Xu Y, Wang C, Wang P, Miao L, Ao Y, Li Y, Lv B (2015) Effects of CeO2 nanoparticles on production and physicochemical characteristics of extracellular polymeric substances in biofilms in sequencing batch biofilm reactor. Bioresour Technol 194:91–98
Zhang H, He X, Zhang Z, Zhang P, Li Y, Ma Y, Kuang Y, Zhao Y, Chai Z (2011) Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environ Sci Technol 45:3725–3730
Zimmermann A, Bauer MA, Kroemer G, Madeo F, Carmona-Gutierrez D (2014) When less is more: hormesis against stress and disease. Microbial Cell 1:150–153
Acknowledgements
We are grateful for the grants from the projects supported by the National Natural Science Funds for Excellent Young Scholar (No.51722902); the National Natural Science Funds for Creative Research Groups of China (No.51421006); the Key Program of National Natural Science Foundation of China (No. 91647206); the Outstanding Youth Fund of Natural Science Foundation of Jiangsu, China (BK20160038); the Fundamental Research Funds for the Central Universities (2018B671X14); and the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX18_0636) and PAPD.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Diane Purchase
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOC 22339 kb)
Rights and permissions
About this article
Cite this article
Xu, Y., Wang, C., Hou, J. et al. Effects of cerium oxide nanoparticles on bacterial growth and behaviors: induction of biofilm formation and stress response. Environ Sci Pollut Res 26, 9293–9304 (2019). https://doi.org/10.1007/s11356-019-04340-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-04340-w


