Abstract
Due to their enhanced reactivity, metal and metal-oxide nanoscale zero-valent iron (nZVI) nanomaterials have been introduced into remediation practice. To ensure that environmental applications of nanomaterials are safe, their possible toxic effects should be described. However, there is still a lack of suitable toxicity tests that address the specific mode of action of nanoparticles, especially for nZVI. This contribution presents a novel approach for monitoring one of the most discussed adverse effects of nanoparticles, i.e., oxidative stress (OS). We optimized and developed an assay based on headspace-SPME-GC-MS analysis that enables the direct determination of volatile oxidative damage products (aldehydes) of lipids and proteins in microbial cultures after exposure to commercial types of nZVI. The method employs PDMS/DVB SPME fibers and pentafluorobenzyl derivatization, and the protocol was successfully tested using representatives of bacteria, fungi, and algae. Six aldehydes, namely, formaldehyde, acrolein, methional, benzaldehyde, glyoxal, and methylglyoxal, were detected in the cultures, and all of them exhibited dose-dependent sigmoidal responses. The presence of methional, which was detected in all cultures except those including an algal strain, documents that nZVI also caused oxidative damage to proteins in addition to lipids. The most sensitive toward nZVI exposure in terms of aldehyde production was the yeast strain Saccharomyces cerevisiae, which had an EC50 value of 0.08 g/L nZVI. To the best of our knowledge, this paper is the first to document the production of aldehydes resulting from lipids and proteins as a result of OS in microorganisms from different kingdoms after exposure to iron nanoparticles.
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References
Bao ML, Pantani F, Griffini O, Burrini D, Santianni D, Barbieri K (1998) Determination of carbonyl compounds in water by derivatization - solid-phase microextraction and gas chromatographic analysis. J Chromatogr A 809:75–87. https://doi.org/10.1016/s0021-9673(98)00188-5
Cancho B, Ventura F, Galceran MT (2002) Determination of aldehydes in drinking water using pentafluorobenzylhydroxylamine derivatization and solid-phase microextraction. J Chromatogr A 943:1–13. https://doi.org/10.1016/S0021-9673(01)01437-6
Chen XQ, Wang F, Hyun JY, Wei TW, Qiang J, Ren XT, Shin I, Yoon J (2016) Recent progress in the development of fluorescent, luminescent and colorimetric probes for detection of reactive oxygen and nitrogen species. Chem Soc Rev 45:2976–3016. https://doi.org/10.1039/c6cs00192k
Chu FL, Yaylayan VA (2008) Model studies on the oxygen-induced formation of benzaldehyde from phenylacetaldehyde using pyrolysis GC-MS and FTIR. J Agric Food Chem 56:10697–10704. https://doi.org/10.1021/jf8022468
Cullere L, Cacho J, Ferreira V (2004) Analysis for wine C5-C8 aldehydes through the determination of their O-(2,3,4,5,6-pentafluorobenzyl)oximes formed directly in the solid phase extraction cartridge. Anal Chim Acta 524:201–206. https://doi.org/10.1016/j.aca.2004.03.025
Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52:601–623. https://doi.org/10.1373/clinchem.2005.061408
Dong HR, Li L, Lu Y, Cheng YJ, Wang YY, Ning Q, Wang B, Zhang L, Zeng G (2019) Integration of nanoscale zero-valent iron and functional anaerobic bacteria for groundwater remediation: a review. Environ Int 124:265–277. https://doi.org/10.1016/j.envint.2019.01.030
Esterbauer H (1993) Cytotoxicity and genotoxicity of lipid-oxidation products. Am J Clin Nutr 57:779S–786S. https://doi.org/10.1093/ajcn/57.5.779S
Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81–128. https://doi.org/10.1016/0891-5849(91)90192-6
Ferreira V, Cullere L, Lopez R, Cacho J (2004) Determination of important odor-active aldehydes of wine through gas chromatography-mass spectrometry of their O-(2,3,4,5,6-pentafluorobenzyl)oximes formed directly in the solid phase extraction cartridge used for selective isolation. J Chromatogr A 1028:339–345. https://doi.org/10.1016/j.chroma.2003.11.104
Filip J, Karlicky F, Marusak Z, Lazar P, Cernik M, Otyepka M et al (2014) Anaerobic reaction of nanoscale zerovalent iron with Water: Mechanism and Kinetics. J Phys Chem C. https://doi.org/10.1021/jp501846f
Grieger KD, Fjordboge A, Hartmann NB, Eriksson E, Bjerg PL, Baun A (2010) Environmental benefits and risks of zero-valent iron nanoparticles (nZVI) for in situ remediation: risk mitigation or trade-off? J Contam Hydrol 118:165–183. https://doi.org/10.1016/j.jconhyd.2010.07.011
Grimsrud PA, Xie HW, Griffin TJ, Bernlohr DA (2008) Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem 283:21837–21841. https://doi.org/10.1074/jbc.R700019200
Hauck AK, Bernlohr DA (2016) Oxidative stress and lipotoxicity. J Lipid Res 57:1976–1986. https://doi.org/10.1194/jlr.R066597
Huang WJ, Cheng YL, Cheng BL (2008) Ozonation byproducts and determination of extracellular release in freshwater algae and cyanobacteria. Environ Eng Sci 25:139–152. https://doi.org/10.1089/ees.2006.0113
Hussain SP, Hofseth LJ, Harris CC (2003) Radical causes of cancer. Nat Rev Cancer 3:276–285. https://doi.org/10.1038/nrc1046
Iglesias J, Gallardo JM, Medina I (2010) Determination of carbonyl compounds in fish species samples with solid-phase microextraction with on-fibre derivatization. Food Chem 123:771–778. https://doi.org/10.1016/j.foodchem.2010.05.025
Jenner P (2003) Oxidative stress in Parkinson's disease. Ann Neurol 53:S26–S38. https://doi.org/10.1002/ana.10483
Karn B, Kuiken T, Otto M (2011) Nanotechnology and in situ remediation: a review of the benefits and potential risks. Cienc Saude Coletiva 16:165–178. https://doi.org/10.1590/s1413-81232011000100020
Kaslik J, Kolarik J, Filip J, Medrik I, Tomanec O, Petr M et al (2018) Nanoarchitecture of advanced core-shell zero-valent iron particles with controlled reactivity for contaminant removal. Chem Eng J 354:335–345. https://doi.org/10.1016/j.cej.2018.08.015
Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650. https://doi.org/10.1080/01926230290166724
Le TT, Nguyen K-H, Jeon J-R, Francis AJ, Chang Y-S (2015) Nano/bio treatment of polychlorinated biphenyls with evaluation of comparative toxicity. J Hazard Mater 287:335–341. https://doi.org/10.1016/j.jhazmat.2015.02.001
Lefevre E, Bossa N, Wiesner MR, Gunsch CK (2016) A review of the environmental implications of in situ remediation by nanoscale zero valent iron (nZVI): behavior, transport and impacts on microbial communities. Sci Total Environ 565:889–901. https://doi.org/10.1016/j.scitotenv.2016.02.003
Lv YC, Niu ZY, Chen YC, Hu YY (2017) Bacterial effects and interfacial inactivation mechanism of nZVI/Pd on Pseudomonas putida strain. Water Res 115:297–308. https://doi.org/10.1016/j.watres.2017.03.012
Maessen DEM, Stehouwer CDA, Schalkwijk CG (2015) The role of methylglyoxal and the glyoxalase system in diabetes and other age-related diseases. Clin Sci 128:839–861. https://doi.org/10.1042/cs20140683
Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23:134–147. https://doi.org/10.1016/s0891-5849(96)00629-6
Martos PA, Pawliszyn J (1998) Sampling and determination of formaldehyde using solid-phase microextraction with on-fiber derivatization. Anal Chem 70:2311–2320. https://doi.org/10.1021/ac9711394
Mistry N, Podmore I, Cooke M, Butler P, Griffiths H, Herbert K, Lunec J (2003) Novel monoclonal antibody recognition of oxidative DNA damage adduct, deoxycytidine-glyoxal. Lab Investig 83:241–250. https://doi.org/10.1097/01.lab.0000053915.88556.ed
Moghe A, Ghare S, Lamoreau B, Mohammad M, Barve S, McClain C et al (2015) Molecular mechanisms of acrolein Toxicity: Relevance to Human Disease. Toxicol Sci. https://doi.org/10.1093/toxsci/kfu233
Moreira N, Meireles S, Brandão T, De Pinho PG (2013) Optimization of the HS-SPME-GC-IT/MS method using a central composite design for volatile carbonyl compounds determination in beers. Talanta. 117:523–531. https://doi.org/10.1016/j.talanta.2013.09.027
Nemecek J, Lhotsky O, Cajthaml T (2014) Nanoscale zero-valent iron application for in situ reduction of hexavalent chromium and its effects on indigenous microorganism populations. Sci Total Environ 485-486:739–747. https://doi.org/10.1016/j.scitotenv.2013.11.105
Nemecek J, Pokorny P, Lacinova L, Cernik M, Masopustova Z, Lhotsky O et al (2015) Combined abiotic and biotic in-situ reduction of hexavalent chromium in groundwater using nZVI and whey: a remedial pilot test. J Hazard Mater 300:670–679. https://doi.org/10.1016/j.jhazmat.2015.07.056
Nemecek J, Pokorny P, Lhotsky O, Knytl V, Najmanova P, Steinova J et al (2016) Combined nano-biotechnology for in-situ remediation of mixed contamination of groundwater by hexavalent chromium and chlorinated solvents. Sci Total Environ 563-564:822–834. https://doi.org/10.1016/j.scitotenv.2016.01.019
Nishikawa H, Sakai T (1995) Derivatization and chromatographic determination of aldehydes in gaseous and air samples. J Chromatogr A 710:159–165. https://doi.org/10.1016/0021-9673(94)01006-z
O'Brien PJ, Siraki AG, Shangari N (2005) Aldehyde sources, metabolism, molecular toxicity mechanisms, and possible effects on human health. Crit Rev Toxicol 35:609–662. https://doi.org/10.1080/10408440591002183
Perluigi M, Coccia R, Butterfield DA (2012) 4-Hydroxy-2-nonenal, a reactive product of lipid peroxidation, and neurodegenerative diseases: a toxic combination illuminated by redox proteomics studies. Antioxid Redox Signal 17:1590–1609. https://doi.org/10.1089/ars.2011.4406
Ribas D, Cernik M, Benito JA, Filip J, Marti V (2017) Activation process of air stable nanoscale zero-valent iron particles. Chem Eng J 320:290–299. https://doi.org/10.1016/j.cej.2017.03.056
Roch AM, Panaye G, Michal Y, Quash G (1998) Methional, a cellular metabolite, induces apoptosis preferentially in G2/M-synchronized BAF3 murine lymphoid cells. Cytometry. 31:10–19. https://doi.org/10.1002/(sici)1097-0320(19980101)31:1<10::aid-cyto2>3.0.co;2-n
Schmarr HG, Potouridis T, Ganss S, Sang W, Koepp B, Bokuz U et al (2008a) Analysis of carbonyl compounds via headspace solid-phase microextraction with on-fiber derivatization and gas chromatographic-ion trap tandem mass spectrometric determination of their O-(2,3,4,5,6-pentafluorobenzyl)oxime derivatives. Anal Chim Acta 617:119–131. https://doi.org/10.1016/j.aca.2008.02.002
Schmarr HG, Sang W, Ganss S, Fischer U, Kopp B, Schulz C et al (2008b) Analysis of aldehydes via headspace SPME with on-fiber derivatization to their O-(2,3,4,5,6-pentafluorobenzyl)oxime derivatives and comprehensive 2D-GC-MS. J Sep Sci 31:3458–3465. https://doi.org/10.1002/jssc.200800294
Schonberg A, Moubacher R (1952) The Strecker degradation of α-amino acids. Chem Rev 50:261–277. https://doi.org/10.1021/cr60156a002
Semerad J, Cajthaml T (2016) Ecotoxicity and environmental safety related to nano-scale zerovalent iron remediation applications. Appl Microbiol Biotechnol 100:9809–9819. https://doi.org/10.1007/s00253-016-7901-1
Semerád J, Čvančarová M, Filip J, Kašlík J, Zlotá J, Soukupová J, Cajthaml T (2018) Novel assay for the toxicity evaluation of nanoscale zero-valent iron and derived nanomaterials based on lipid peroxidation in bacterial species. Chemosphere. 213:568–577. https://doi.org/10.1016/j.chemosphere.2018.09.029
Sevcu A, El-Temsah YS, Joner EJ, Cernik M (2011) Oxidative stress induced in microorganisms by zero-valent iron nanoparticles. Microbes Environ 26:271–281. https://doi.org/10.1264/jsme2.ME11126
Shara MA, Dickson PH, Bagchi D, Stohs SJ (1992) Excretion of formaldehyde, malondialdehyde, acetaldehyde and acetone in the urine of rats in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin, paraquat, endrin and carbon tetrachloride. J Chromatogr B Biomed Sci Appl 576:221–233. https://doi.org/10.1016/0378-4347(92)80196-w
Shibamoto T (2006) Analytical methods for trace levels of reactive carbonyl compounds formed in lipid peroxidation systems. J Pharm Biomed Anal 41:12–25. https://doi.org/10.1016/j.jpba.2006.01.047
Soukupova J, Zboril R, Medrik I, Filip J, Safarova K, Ledl R, Mashlan M, Nosek J, Cernik M (2015) Highly concentrated, reactive and stable dispersion of zero-valent iron nanoparticles: direct surface modification and site application. Chem Eng J 262:813–822. https://doi.org/10.1016/j.cej.2014.10.024
Spiteller G, Kern W, Spiteller P (1999) Investigation of aldehydic lipid peroxidation products by gas chromatography-mass spectrometry. J Chromatogr A 843:29–98. https://doi.org/10.1016/s0021-9673(98)01078-4
Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25:207–218. https://doi.org/10.1007/s00726-003-0011-2
Stefaniuk M, Oleszczuk P, Ok YS (2016) Review on nano zerovalent iron (nZVI): from synthesis to environmental applications. Chem Eng J 287:618–632. https://doi.org/10.1016/j.cej.2015.11.046
Tucek J, Prucek R, Kolarik J, Zoppellaro G, Petr M, Filip J et al (2017) Zero-valent iron nanoparticles reduce arsenites and arsenates to as(0) firmly embedded in Core-Shell superstructure: challenging strategy of arsenic treatment under anoxic conditions. ACS Sustain Chem Eng 5:3027–3038. https://doi.org/10.1021/acssuschemeng.6b02698
Uchiyama S, Inaba Y, Kunugita N (2011) Derivatization of carbonyl compounds with 2,4-dinitrophenylhydrazine and their subsequent determination by high-performance liquid chromatography. J Chromatogr B. https://doi.org/10.1016/j.jchromb.2010.09.028
Vesely P, Lusk L, Basarova G, Seabrooks J, Ryder D (2003) Analysis of aldehydes in beer using solid-phase microextraction with on-fiber derivatization and gas chromatography/mass spectrometry. J Agric Food Chem 51:6941–6944. https://doi.org/10.1021/jf034410t
Voulgaridou G-P, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A (2011) DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res-Fundam Mol Mech Mutagen 711:13–27. https://doi.org/10.1016/j.mrfmmm.2011.03.006
Wang Q, O'Reilly J, Pawliszyn J (2005) Determination of low-molecular mass aldehydes by automated headspace solid-phase microextraction with in-fibre derivatisation. J Chromatogr A 1071:147–154. https://doi.org/10.1016/j.chroma.2004.09.031
Wu Y, Cao B (2015) Assessment of bacterial survival in the presence of nanomaterials: is colony forming unit count sufficient? Environ Eng Sci 32:977. https://doi.org/10.1089/ees.2015.0329
Wu S, Cajthaml T, Semerad J, Filipova A, Klementova M, Skala R et al (2019) Nano zero-valent iron aging interacts with the soil microbial community: a microcosm study. Environ Sci-Nano 6:1189–1206. https://doi.org/10.1039/C8EN01328D
Xue WJ, Huang DL, Zeng GM, Wan J, Cheng M, Zhang C, Hu C, Li J (2018) Performance and toxicity assessment of nanoscale zero valent iron particles in the remediation of contaminated soil: a review. Chemosphere. 210:1145–1156. https://doi.org/10.1016/j.chemosphere.2018.07.118
Zboril R, Andrle M, Oplustil F, Machala L, Tucek J, Filip J, Marusak Z, Sharma VK (2012) Treatment of chemical warfare agents by zero-valent iron nanoparticles and ferrate(VI)/(III) composite. J Hazard Mater 211-212:126–130. https://doi.org/10.1016/j.jhazmat.2011.10.094
Acknowledgments
This work was supported by Competence Center TE01020218 of the Technology Agency of the Czech Republic and by the Center for Geosphere Dynamics (UNCE/SCI/006). We acknowledge the Cytometry and Microscopy Facility at the Institute of Microbiology of the ASCR, v.v.i, Vídeňská 1083, Prague, CZ for the use of the cytometry equipment and support from the staff, as well as J. Kašlík for technical assistance.
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Semerád, J., Moeder, M., Filip, J. et al. Oxidative stress in microbes after exposure to iron nanoparticles: analysis of aldehydes as oxidative damage products of lipids and proteins. Environ Sci Pollut Res 26, 33670–33682 (2019). https://doi.org/10.1007/s11356-019-06370-w
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DOI: https://doi.org/10.1007/s11356-019-06370-w