Abstract
Carbon nanotubes (CNTs) have emerged recently as superior adsorbent materials for the removal of recalcitrant pollutants. The potential of combining the sorption capability of CNTs with bacterial degradation for pollutant removal, however, necessitates further investigation of the mechanisms of CNTs’ toxicity towards bacterial cells. In this study, we used a panel of stress-responsive recombinant Escherichia coli bioluminescence bacterial strains to explore the possible mechanisms of toxicity of multiwalled carbon nanotubes (MWCNTs). The effects of MWCNTs on markers of oxidative stress, protein, DNA, and membrane damage enabled the exposition of some of the mechanisms of their antimicrobial properties. Using both a bioluminescence bioreporter panel and live/dead staining, we observed that membrane damage played a role in the toxicity of MWCNTs. A subsequent viability study using three strains of bacteria—two gram-negative (Escherichia coli, Pseudomonas aeruginosa) and one gram-positive (Bacillus subtilis)—showed significant MWCNT toxicity in hypotonic water and phosphate-buffered saline solution, compared with the MWCNT toxicity towards the same bacteria incubated in isotonic-rich media. Using a field-emission scanning electron microscope, we demonstrated that membrane damage is caused largely by MWCNTs trapping bacteria and piercing the cell walls. As a result of our observations, we propose integrating MWCNTs and bacteria degradation for pollutant removal in nutrient-rich media to minimize the toxicity effect of CNTs.
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References
Arias LR, Yang L (2009) Inactivation of bacterial pathogens by carbon nanotubes in suspensions. Langmuir 25(5):3003–3012. https://doi.org/10.1021/la802769m
Bohdziewicz J, Kamińska G (2013) Kinetics and equilibrium of the sorption of bisphenol A by carbon nanotubes from wastewater. Water Sci Technol 68(6):1306–1314. https://doi.org/10.2166/wst.2013.373
Chen H, Wang B, Gao D, Guan M, Zheng L, Ouyang H, Chai Z, Zhao Y, Feng W (2013) Broad-spectrum antibacterial activity of carbon nanotubes to human gut bacteria. Small 9(16):2735–2746. https://doi.org/10.1002/smll.201202792
Cortes P, Deng S, Smith GB (2014) The toxic effects of single wall carbon nanotubes on E. coli and a spore-forming bacillus species. Nanosci Nanotechnol Lett 6(1):26–30. https://doi.org/10.1166/nnl.2014.1719
De Volder MFL, Tawfick SH, Baughman RH, Hart AJ (2013) Carbon nanotubes: present and future commercial applications. Sci (New York, NY) 339:535–539
Dong L, Henderson A, Field C (2012) Antimicrobial activity of single-walled carbon nanotubes suspended in different surfactants. J Nanotechnol 2012:1–7. https://doi.org/10.1155/2012/928924
Eltzov E, Ben-Yosef DZ, Kushmaro A, Marks R (2008) Detection of sub-inhibitory antibiotic concentrations via luminescent sensing bacteria and prediction of their mode of action. Sensors Actuators B Chem 129(2):685–692. https://doi.org/10.1016/j.snb.2007.09.054
Gupta VK, Kumar R, Nayak A, Saleh TA, Barakat MA (2013) Adsorptive removal of dyes from aqueous solution onto carbon nanotubes: a review. Adv Colloid Interf Sci 193–194:24–34. https://doi.org/10.1016/j.cis.2013.03.003
Hall LW, Anderson RD (1995) The influence of salinity on the toxicity of various classes of chemicals to aquatic biota. Crit Rev Toxicol 25(4):281–346. https://doi.org/10.3109/10408449509021613
Hartono MR, Marks RS, Chen X, Kushmaro A (2014) Hybrid multi-walled carbon nanotubes-alginate-polysulfone beads for adsorption of bisphenol-A from aqueous solution. Desalin Water Treat 54:1167–1183
Hartono MR, Kushmaro A, Marks RS, Chen X (2016) Calcium-alginate/carbon nanotubes/TiO2 composite beads for removal of bisphenol A. Water Sci Technol 74(7):1585–1593. https://doi.org/10.2166/wst.2016.354
Hua A, Gueuné H, Cregut M et al (2015) Development of a bacterial bioassay for atrazine and cyanuric acid detection. Front Microbiol 6:1–6. https://doi.org/10.3389/fmicb.2015.00211
Jia K, Marks RS, Ionescu RE (2014) Influence of carbon-based nanomaterials on lux-bioreporter Escherichia coli. Talanta 126:208–213. https://doi.org/10.1016/j.talanta.2014.03.024
Kang S, Pinault M, Pfefferle LD, Elimelech M (2007) Single-walled carbon nanotubes exhibit strong antimicrobial activity. Langmuir 23(17):8670–8673. https://doi.org/10.1021/la701067r
Le TTA, McEvoy J, Khan E (2015) The effect of single-walled carbon nanotubes on Escherichia coli: multiple indicators of viability. J Nanopart Res 17(1):1–9. https://doi.org/10.1007/s11051-014-2827-y
Li M, Zhu L, Lin D (2011) Toxicity of ZnO nanoparticles to Escherichia coli: mechanism and the influence of medium components. Environ Sci Technol 45(5):1977–1983. https://doi.org/10.1021/es102624t
Li F, Lei C, Shen Q, Li L, Wang M, Guo M, Huang Y, Nie Z, Yao S (2013) Analysis of copper nanoparticles toxicity based on a stress-responsive bacterial biosensor array. Nano 5(2):653–662. https://doi.org/10.1039/c2nr32156d
Liu S, Wei L, Hao L, Fang N, Chang MW, Xu R, Yang Y, Chen Y (2009) Sharper and faster “Nano darts” kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. ACS Nano 3(12):3891–3902. https://doi.org/10.1021/nn901252r
Liu S, Ng AK, Xu R, Wei J, Tan CM, Yang Y, Chen Y (2010) Antibacterial action of dispersed single-walled carbon nanotubes on Escherichia coli and Bacillus subtilis investigated by atomic force microscopy. Nano 2(12):2744–2750. https://doi.org/10.1039/c0nr00441c
Long RQ, Yang RT (2001) Carbon nanotubes as superior sorbent for dioxin removal. J Am Chem Soc 123(9):2058–2059. https://doi.org/10.1177/004051758105100910
Lu C, Chiu H, Bai H (2007) Comparisons of adsorbent cost for the removal of zinc (II) from aqueous solution by carbon nanotubes and activated carbon. J Nanosci Nanotechnol 7(4):1647–1652. https://doi.org/10.1166/jnn.2007.349
MacDonald IA, Kuehna MJ (2013) Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J Bacteriol 195(13):2971–2981. https://doi.org/10.1128/JB.02267-12
Martin MJ, Serra E, Ros A, Balaguer MD, Rigola M (2004) Carbonaceous adsorbents from sewage sludge and their application in a combined activated sludge-powdered activated carbon (AS-PAC) treatment. Carbon N Y 42(7):1383–1388. https://doi.org/10.1016/j.carbon.2004.01.011
Morinaga H, Nehijima W, Okada M (2003) Stimulation of bacterial activity by the addition of different PACS. Environ Technol 24(2):179–186. https://doi.org/10.1080/09593330309385549
Nagai H, Toyokuni S (2012) Differences and similarities between carbon nanotubes and asbestos fibers during mesothelial carcinogenesis: Shedding light on fiber entry mechanism. Cancer Sci 103(8):1378–1390. https://doi.org/10.1111/j.1349-7006.2012.02326.x
Olivi M, Zanni E, De Bellis G, Talora C, Sarto MS, Palleschi C, Flahaut E, Monthioux M, Rapino S, Uccelletti D, Fiorito S (2013) Inhibition of microbial growth by carbon nanotube networks. Nano 5(19):9023–9029. https://doi.org/10.1039/c3nr02091f
Orshansky F, Narkis N (1997) Characteristics of organics removal by pact simultaneous adsorption and biodegradation. Water Res 31(3):391–398. https://doi.org/10.1016/S0043-1354(96)00227-8
Premkumar JR, Rosen R, Belkin S, Lev O (2002) Sol-gel luminescence biosensors: Encapsulation of recombinant E. coli reporters in thick silicate films. Anal Chim Acta 462:11–23. https://doi.org/10.1016/S0003-2670(02)00301-X
Sirotkin AS, Koshkina LY, Ippolitov KG (2001) The BAC-process for treatment of waste water containing non-ionogenic synthetic surfactants. Water Res 35(13):3265–3271. https://doi.org/10.1016/S0043-1354(01)00029-X
Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18(2):321–336. https://doi.org/10.1016/0891-5849(94)00159-H
Van Dyk TK, Majarian WR, Konstantinov KB, et al (1994) Rapid and sensitive pollutant detection by induction of heat shock gene-bioluminescence gene fusions. Appl Environ Microbiol 60:1414–1420
Vecitis CD, Zodrow KR, Kang S, Elimelech M (2010) Electronic-structure-dependent bacterial cytotoxicity of single-walled carbon nanotubes. ACS Nano 4(9):5471–5479. https://doi.org/10.1021/nn101558x
Virto R, Mañas P, Álvarez I et al (2005) Membrane damage and microbial inactivation by chlorine in the absence and presence of a chlorine-demanding substrate membrane damage and microbial inactivation by chlorine in the absence and presence of a chlorine-demanding substrate. Appl Environ Microbiol 71(9):5022–5028. https://doi.org/10.1128/AEM.71.9.5022
Vollmer AMYC, Belkin S, Smulski DR, Dyk TKVAN (1997) Detection of DNA Damage by Use of Escherichia coli Carrying recA’::lux, uvrA’::lux,or alkA’::lux Reporter Plasmids. Appl Environ Microbiol 63:2566–2571
Yang C, Mamouni J, Tang Y, Yang L (2010) Antimicrobial activity of single-walled carbon nanotubes: length effect. Langmuir 26(20):16013–16019. https://doi.org/10.1021/la103110g
Young Y-F, Lee H-J, Shen Y-S, Tseng SH, Lee CY, Tai NH, Chang HY (2012) Toxicity mechanism of carbon nanotubes on Escherichia coli. Mater Chem Phys 134(1):279–286. https://doi.org/10.1016/j.matchemphys.2012.02.066
Zhang C, Li M, Xu X, Liu N (2015) Effects of carbon nanotubes on atrazine biodegradation by Arthrobacter sp. J Hazard Mater 287:1–6. https://doi.org/10.1016/j.jhazmat.2015.01.039
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The authors acknowledge the support of the NTU-HUJ-BGU Nanomaterials for Energy and Water Management (NEW) program under the Campus for Research Excellence and Technological Enterprise (CREATE), which is supported by the National Research Foundation Singapore.
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Hartono, M.R., Kushmaro, A., Chen, X. et al. Probing the toxicity mechanism of multiwalled carbon nanotubes on bacteria. Environ Sci Pollut Res 25, 5003–5012 (2018). https://doi.org/10.1007/s11356-017-0782-8
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DOI: https://doi.org/10.1007/s11356-017-0782-8