Abstract
Biofouling is a serious issue in membrane-based water and wastewater treatment as it critically compromises the efficacy of the water treatment processes. This investigation demonstrates the antimicrobial and antifouling properties of a nanocomposite membrane system composed of carboxyl-functionalized graphene oxide (COOH-GO) and polyphenylsulfone (PPSU). The PPSU/COOH-GO nanocomposite membrane exhibited excellent antimicrobial properties, achieving maximum bacteriostasis rates of 74.2% and 81.1% against the representative Gram-negative bacteria (Escherichia coli and Pseudomonas aeruginosa, respectively) and 41.9% against the representative Gram-positive bacterium (Staphylococcus aureus). The PPSU/COOH-GO nanocomposite membrane inhibited the attachment, colonization, and the biofilm formation of three species. Antifouling was assessed through filtration experiments using a model foulant bovine serum albumin (BSA). The fouling mechanisms were investigated by Hermia’s models (complete blocking, intermediate blocking, standard blocking, and cake formation), and the analysis involved fitting the volumetric flux decline experimental data to models. The fouling study revealed a less irreversible fouling and increased flux recovery ratio for the PPSU/COOH-GO nanocomposite membrane. Complete blocking of pores and cake formation were the major fouling mechanisms for the membrane.
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Abbreviations
- PPSU:
-
polyphenylsulfone
- COOH-GO:
-
carboxyl-functionalized graphene oxide
- E. coli :
-
Escherichia coli
- P. aeruginosa :
-
Pseudomonas aeruginosa
- S. aureus :
-
Staphylococcus aureus
- BSA:
-
bovine serum albumin
- CFU:
-
colony-forming unit
- TMP:
-
transmembrane pressure
- J v :
-
pure water volumetric flux
- J vp :
-
foulant volumetric flux
- J v1 :
-
final water volumetric flux
- J v RR :
-
flux recovery ratio
- R t :
-
total fouling ratio
- R r :
-
reversible fouling ratio
- R ir :
-
irreversible fouling ratio
- J vp0 :
-
initial volume flow rate
- J vpt :
-
volume flow at a particular time
- K c :
-
membrane surface area blocked per unit of permeate volume
- t :
-
time
- K s :
-
constant of the standard blocking model
- K i :
-
constant of the intermediate blocking model
- K cf :
-
constant of the cake formation model
References
Abdel-Karim A, Leaper S, Alberto M, Vijayaraghavan A, Fan X, Holmes SM, Souaya ER, Badawy MI, Gorgojo P (2018) High flux and fouling resistant flat sheet polyethersulfone membranes incorporated with graphene oxide for ultrafiltration applications. Chem Eng J 334:789–799. https://doi.org/10.1016/j.cej.2017.10.069
Abinaya M, Vaseeharan B, Divya M, Vijayakumar S, Govindarajan M, Alharbi NS, Khaled JM, al-anbr MN, Benelli G (2018) Structural characterization of Bacillus licheniformis Dahb1 exopolysaccharide—antimicrobial potential and larvicidal activity on malaria and Zika virus mosquito vectors. Environ Sci Pollut Res 25:18604–18619. https://doi.org/10.1007/s11356-018-2002-6
Ahmed F, Santos CM, Vergara RAMV, Tria MCR, Advincula R, Rodrigues DF (2012) Antimicrobial applications of electroactive PVK-SWNT nanocomposites. Environ Sci Technol 46:1804–1810. https://doi.org/10.1021/es202374e
Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–5736. https://doi.org/10.1021/nn101390x
Ansari MA, Khan HM, Khan AA, Ahmad MK, Mahdi AA, Pal R, Cameotra SS (2014) Interaction of silver nanoparticles with Escherichia coli and their cell envelope biomolecules. J Basic Microbiol 54:905–915. https://doi.org/10.1002/jobm.201300457
Ayyaru S, Ahn YH (2017) Application of sulfonic acid group functionalized graphene oxide to improve hydrophilicity, permeability, and antifouling of PVDF nanocomposite ultrafiltration membranes. J Memb Sci 525:210–219. https://doi.org/10.1016/j.memsci.2016.10.048
Benelli G (2018) Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology. Environ Sci Pollut Res 25:10149–10150. https://doi.org/10.1007/s11356-017-9960-y
Ben-Sasson M, Zodrow KR, Genggeng Q, Kang Y, Giannelis EP, Elimelech M (2014) Surface functionalization of thin-film composite membranes with copper nanoparticles for antimicrobial surface properties. Environ Sci Technol 48:384–393. https://doi.org/10.1021/es404232s
Bogdanović U, Vodnik V, Mitrić M, Dimitrijević S, Škapin SD, Žunič V, Budimir M, Stoiljković M (2015) Nanomaterial with high antimicrobial efficacy copper/polyaniline nanocomposite. ACS Appl Mater Interfaces 7:1955–1966. https://doi.org/10.1021/am507746m
Chen F, Shi X, Chen X, Chen W (2018) Preparation and characterization of amphiphilic copolymer PVDF-g-PMABS and its application in improving hydrophilicity and protein fouling resistance of PVDF membrane. Appl Surf Sci 427:787–797. https://doi.org/10.1016/j.apsusc.2017.08.096
Chung YT, Mahmoudi E, Mohammad AW, Benamor A, Johnson D, Hilal N (2017) Development of polysulfone-nanohybrid membranes using ZnO-GO composite for enhanced antifouling and antibacterial control. Desalination 402:123–132. https://doi.org/10.1016/j.desal.2016.09.030
Corbatón-Báguena M-J, Álvarez-Blanco S, Vincent-Vela M-C (2018) Evaluation of fouling resistances during the ultrafiltration of whey model solutions. J Clean Prod 172:358–367. https://doi.org/10.1016/j.jclepro.2017.10.149
Emadzadeh D, Ghanbari M, Lau WJ, Rahbari-Sisakht M, Rana D, Matsuura T, Kruczek B, Ismail AF (2017) Surface modification of thin film composite membrane by nanoporous titanate nanoparticles for improving combined organic and inorganic antifouling properties. Mater Sci Eng C 75:463–470. https://doi.org/10.1016/j.msec.2017.02.079
Eng AYS, Sofer Z, Sedmidubský D, Pumera M (2017) Synthesis of carboxylated-graphenes by the Kolbe-Schmitt process. ACS Nano 11:1789–1797. https://doi.org/10.1021/acsnano.6b07746
Gao Q, Yu M, Su Y, Xie M, Zhao X, Li P, Ma PX (2017a) Rationally designed dual functional block copolymers for bottlebrush-like coatings: in vitro and in vivo antimicrobial, antibiofilm, and antifouling properties. Acta Biomater 51:112–124. https://doi.org/10.1016/j.actbio.2017.01.061
Gao Y, Wu J, Ren X, Tan X, Hayat T, Alsaedi A, Cheng C, Chen C (2017b) Impact of graphene oxide on the antibacterial activity of antibiotics against bacteria. Environ Sci Nano 4:1016–1024. https://doi.org/10.1039/C7EN00052A
Gurunathan S, Han JW, Dayem AA et al (2012) Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomedicine 7:5901–5914. https://doi.org/10.2147/IJN.S37397
He L, Dumée LF, Feng C, Velleman L, Reis R, She F, Gao W, Kong L (2015) Promoted water transport across graphene oxide–poly(amide) thin film composite membranes and their antibacterial activity. Desalination 365:126–135. https://doi.org/10.1016/j.desal.2015.02.032
Ho KC, Teow YH, Ang WL, Mohammad AW (2017) Novel GO/OMWCNTs mixed-matrix membrane with enhanced antifouling property for palm oil mill effluent treatment. Sep Purif Technol 177:337–349. https://doi.org/10.1016/j.seppur.2017.01.014
Hou S, Xing J, Dong X, Zheng J, Li S (2017) Integrated antimicrobial and antifouling ultrafiltration membrane by surface grafting PEO and N-chloramine functional groups. J Colloid Interface Sci 500:333–340. https://doi.org/10.1016/j.jcis.2017.04.028
Hu W, Peng C, Luo W, Lv M, Li X, Li D, Huang Q, Fan C (2010) Graphene-based antibacterial paper. ACS Nano 4:4317–4323. https://doi.org/10.1021/nn101097v
Hu M, Zheng S, Mi B (2016) Organic fouling of graphene oxide membranes and its implications for membrane fouling control in engineered osmosis. Environ Sci Technol 50:685–693. https://doi.org/10.1021/acs.est.5b03916
Hu Y, Lü Z, Wei C, Yu S, Liu M, Gao C (2018) Separation and antifouling properties of hydrolyzed PAN hybrid membranes prepared via in-situ sol-gel SiO2nanoparticles growth. J Membr Sci 545:250–258. https://doi.org/10.1016/j.memsci.2017.09.081
Huang H, Yu J, Guo H, Shen Y, Yang F, Wang H, Liu R, Liu Y (2018) Improved antifouling performance of ultrafiltration membrane via preparing novel zwitterionic polyimide. Appl Surf Sci 427:38–47. https://doi.org/10.1016/j.apsusc.2017.08.004
Ji H, Sun H, Qu X (2016) Antibacterial applications of graphene-based nanomaterials: recent achievements and challenges. Adv Drug Deliv Rev 105:176–189. https://doi.org/10.1016/j.addr.2016.04.009
Kaleekkal NJ, Thanigaivelan A, Rana D, Mohan D (2016) Studies on carboxylated graphene oxide incorporated polyetherimide mixed matrix ultrafiltration membranes. Mater Chem Phys 186:146–158. https://doi.org/10.1016/j.matchemphys.2016.10.040
Koh E, Lee YT (2017) Antimicrobial activity and fouling resistance of a polyvinylidene fluoride (PVDF) hollow-fiber membrane. J Ind Eng Chem 47:260–271. https://doi.org/10.1016/j.jiec.2016.11.042
Krishnamoorthy K, Veerapandian M, Zhang LH, Yun K, Kim SJ (2012) Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. J Phys Chem C 116:17280–17287. https://doi.org/10.1021/jp3047054
Lee A, Elam JW, Darling SB (2016) Membrane materials for water purification: design, development, and application. Environ Sci Water Res Technol 2:17–42. https://doi.org/10.1039/C5EW00159E
Liu S, Zeng TH, Hofmann M, Burcombe E, Wei J, Jiang R, Kong J, Chen Y (2011) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5:6971–6980. https://doi.org/10.1021/nn202451x
Liu C, Faria AF, Ma J, Elimelech M (2017) Mitigation of biofilm development on thin-film composite membranes functionalized with Zwitterionic polymers and silver nanoparticles. Environ Sci Technol 51:182–191. https://doi.org/10.1021/acs.est.6b03795
Lu X, Feng X, Werber JR, Chu C, Zucker I, Kim JH, Osuji CO, Elimelech M (2017) Enhanced antibacterial activity through the controlled alignment of graphene oxide nanosheets. Proc Natl Acad Sci 114:E9793–E9801. https://doi.org/10.1073/pnas.1710996114
Luyts K, Napierska D, Nemery B, Hoet PHM (2013) How physico-chemical characteristics of nanoparticles cause their toxicity: complex and unresolved interrelations. Environ Sci Impacts 15:23–38. https://doi.org/10.1039/c2em30237c
Ma R, Ji YL, Guo YS, Mi YF, An QF, Gao CJ (2017) Fabrication of antifouling reverse osmosis membranes by incorporating zwitterionic colloids nanoparticles for brackish water desalination. Desalination 416:35–44. https://doi.org/10.1016/j.desal.2017.04.016
Mejías Carpio IE, Santos CM, Wei X, Rodrigues DF (2012) Toxicity of a polymer–graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale 4:4746–4756. https://doi.org/10.1039/c2nr30774j
Mo Y, Tiraferri A, Yip NY, Adout A, Huang X, Elimelech M (2012) Improved antifouling properties of polyamide nanofiltration membranes by reducing the density of surface carboxyl groups. Environ Sci Technol 46:13253–13261. https://doi.org/10.1021/es303673p
Moradi G, Zinadini S, Rajabi L, Dadari S (2018) Fabrication of high flux and antifouling mixed matrix fumarate-alumoxane/PAN membranes via electrospinning for application in membrane bioreactors. Appl Surf Sci 427:830–842. https://doi.org/10.1016/j.apsusc.2017.09.039
Morelos-Gomez A, Cruz-Silva R, Muramatsu H, Ortiz-Medina J, Araki T, Fukuyo T, Tejima S, Takeuchi K, Hayashi T, Terrones M, Endo M (2017) Effective NaCl and dye rejection of hybrid graphene oxide/graphene layered membranes. Nat Nanotechnol 12:1083–1088. https://doi.org/10.1038/nnano.2017.160
Nasrollahi N, Vatanpour V, Aber S, Mahmoodi NM (2018) Preparation and characterization of a novel polyethersulfone (PES) ultrafiltration membrane modified with a CuO/ZnO nanocomposite to improve permeability and antifouling properties. Sep Purif Technol 192:369–382. https://doi.org/10.1016/j.seppur.2017.10.034
Ng CY, Mohammad AW, Ng LY, Jahim JM (2014) Membrane fouling mechanisms during ultrafiltration of skimmed coconut milk. J Food Eng 142:190–200. https://doi.org/10.1016/j.jfoodeng.2014.06.005
Perreault F, Tousley ME, Elimelech M (2013) Thin-film composite polyamide membranes functionalized with biocidal graphene oxide nanosheets. Environ Sci Technol Lett 1:71–76. https://doi.org/10.1021/ez4001356
Perreault F, Fonseca de Faria A, Elimelech M (2015) Environmental applications of graphene-based nanomaterials. Chem Soc Rev 44:5861–5896. https://doi.org/10.1039/C5CS00021A
Perreault F, Jaramillo H, Xie M, Ude M, Nghiem LD, Elimelech M (2016) Biofouling mitigation in forward osmosis using graphene oxide functionalized thin-film composite membranes. Environ Sci Technol 50:5840–5848. https://doi.org/10.1021/acs.est.5b06364
Qiu WZ, Zhao ZS, Du Y et al (2017) Antimicrobial membrane surfaces via efficient polyethyleneimine immobilization and cationization. Appl Surf Sci 426:972–979. https://doi.org/10.1016/j.apsusc.2017.07.217
Safarpour M, Vatanpour V, Khataee A (2016) Preparation and characterization of graphene oxide/TiO2 blended PES nanofiltration membrane with improved antifouling and separation performance. Desalination 393:65–78. https://doi.org/10.1016/j.desal.2015.07.003
Sanchez VC, Jachak A, Hurt RH, Kane AB (2012) Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 25:15–34. https://doi.org/10.1021/tx200339h
Sawada I, Fachrul R, Ito T, Ohmukai Y, Maruyama T, Matsuyama H (2012) Development of a hydrophilic polymer membrane containing silver nanoparticles with both organic antifouling and antibacterial properties. J Membr Sci 387–388:1–6. https://doi.org/10.1016/j.memsci.2011.06.020
Shanmuganathan R, MubarakAli D, Prabakar D, Muthukumar H, Thajuddin N, Kumar SS, Pugazhendhi A (2018) An enhancement of antimicrobial efficacy of biogenic and ceftriaxone-conjugated silver nanoparticles: green approach. Environ Sci Pollut Res 25:10362–10370. https://doi.org/10.1007/s11356-017-9367-9
Shannon MA, Bohn PW, Elimelech M, Georgiadis JG, Mariñas BJ, Mayes AM (2008) Science and technology for water purification in the coming decades. Nature 452:301–310. https://doi.org/10.1038/nature06599
Shockravi A, Vatanpour V, Najjar Z, Bahadori S, Javadi A (2017) A new high performance polyamide as an effective additive for modification of antifouling properties and morphology of asymmetric PES blend ultrafiltration membranes. Microporous Mesoporous Mater 246:24–36. https://doi.org/10.1016/j.micromeso.2017.03.013
Shukla AK, Alam J, Alhoshan M, Dass LA, Muthumareeswaran MR (2017) Development of a nanocomposite ultrafiltration membrane based on polyphenylsulfone blended with graphene oxide. Sci Rep 7:41976–41987. https://doi.org/10.1038/srep41976
Shukla AK, Alam J, Alhoshan M, Arockiasamy Dass L, Ali FAA, M. R M, Mishra U, Ansari MA (2018) Removal of heavy metal ions using a carboxylated graphene oxide-incorporated polyphenylsulfone nanofiltration membrane. Environ Sci Water Res Technol 4:438–448. https://doi.org/10.1039/C7EW00506G
Srinivasan R, Vigneshwari L, Rajavel T, Durgadevi R, Kannappan A, Balamurugan K, Pandima Devi K, Veera Ravi A (2018) Biogenic synthesis of silver nanoparticles using Piper betle aqueous extract and evaluation of its anti-quorum sensing and antibiofilm potential against uropathogens with cytotoxic effects: an in vitro and in vivo approach. Environ Sci Pollut Res 25:10538–10554. https://doi.org/10.1007/s11356-017-1049-0
Torkamanzadeh M, Jahanshahi M, Peyravi M, Rad AS (2016) Comparative experimental study on fouling mechanisms in nano-porous membrane: cheese whey ultrafiltration as a case study. Water Sci Technol 74:2737–2750. https://doi.org/10.2166/wst.2016.352
Wang YN, Tang CY (2011) Fouling of nanofiltration, reverse osmosis, and ultrafiltration membranes by protein mixtures: the role of inter-foulant-species interaction. Environ Sci Technol 45:6373–6379. https://doi.org/10.1021/es2013177
Wang W, Zhu L, Shan B, Xie C, Liu C, Cui F, Li G (2018) Preparation and characterization of SLS-CNT/PES ultrafiltration membrane with antifouling and antibacterial properties. J Membr Sci 548:459–469. https://doi.org/10.1016/j.memsci.2017.11.046
Whitehead KA, Vaidya M, Liauw CM, Brownson DAC, Ramalingam P, Kamieniak J, Rowley-Neale SJ, Tetlow LA, Wilson-Nieuwenhuis JST, Brown D, McBain AJ, Kulandaivel J, Banks CE (2017) Antimicrobial activity of graphene oxide-metal hybrids. Int Biodeterior Biodegrad 123:182–190. https://doi.org/10.1016/j.ibiod.2017.06.020
Xu Q, Zeng M, Feng Z, Yin D, Huang Y, Chen Y, Yan C, Li R, Gu Y (2016) Understanding the effects of carboxylated groups of functionalized graphene oxide on the curing behavior and intermolecular interactions of benzoxazine nanocomposites. RSC Adv 6:31484–31496. https://doi.org/10.1039/C5RA28016H
Xu Z, Liao J, Tang H, Li N (2017) Antifouling polysulfone ultrafiltration membranes with pendent sulfonamide groups. J Membr Sci 548:481–489. https://doi.org/10.1016/j.memsci.2017.11.064
You X, Ma T, Su Y, Wu H, Wu M, Cai H, Sun G, Jiang Z (2017) Enhancing the permeation flux and antifouling performance of polyamide nanofiltration membrane by incorporation of PEG-POSS nanoparticles. J Membr Sci 540:454–463. https://doi.org/10.1016/j.memsci.2017.06.084
Yousefi M, Dadashpour M, Hejazi M, Hasanzadeh M, Behnam B, de la Guardia M, Shadjou N, Mokhtarzadeh A (2017) Anti-bacterial activity of graphene oxide as a new weapon nanomaterial to combat multidrug-resistance bacteria. Mater Sci Eng C 74:568–581. https://doi.org/10.1016/j.msec.2016.12.125
Yu H, Zhang X, Zhang Y, Liu J, Zhang H (2013a) Development of a hydrophilic PES ultrafiltration membrane containing SiO2@N-Halamine nanoparticles with both organic antifouling and antibacterial properties. Desalination 326:69–76. https://doi.org/10.1016/j.desal.2013.07.018
Yu L, Zhang Y, Zhang B, Liu J, Zhang H, Song C (2013b) Preparation and characterization of HPEI-GO/PES ultrafiltration membrane with antifouling and antibacterial properties. J Membr Sci 447:452–462. https://doi.org/10.1016/j.memsci.2013.07.042
Yu S, Liu J, Zhu W, Hu ZT, Lim TT, Yan X (2015) Facile room-temperature synthesis of carboxylated graphene oxide-copper sulfide nanocomposite with high photodegradation and disinfection activities under solar light irradiation. Sci Rep 5:16369–16380. https://doi.org/10.1038/srep16369
Zeng Z, Yu D, He Z, Liu J, Xiao FX, Zhang Y, Wang R, Bhattacharyya D, Tan TTY (2016) Graphene oxide quantum dots covalently functionalized PVDF membrane with significantly-enhanced bactericidal and antibiofouling performances. Sci Rep 6:20142–20152. https://doi.org/10.1038/srep20142
Zhang ZB, Wu JJ, Su Y, Zhou J, Gao Y, Yu HY, Gu JS (2015) Layer-by-layer assembly of graphene oxide on polypropylene macroporous membranes via click chemistry to improve antibacterial and antifouling performance. Appl Surf Sci 332:300–307. https://doi.org/10.1016/j.apsusc.2015.01.193
Zhang DY, Hao Q, Liu J, Shi YS, Zhu J, Su L, Wang Y (2018a) Antifouling polyimide membrane with grafted silver nanoparticles and zwitterion. Sep Purif Technol 192:230–239. https://doi.org/10.1016/j.seppur.2017.10.018
Zhang J, Xu Y, Chen S et al (2018b) Enhanced antifouling and antibacterial properties of poly (ether sulfone) membrane modified through blending with sulfonated poly (aryl ether sulfone) and copper nanoparticles. Appl Surf Sci 434:806–815. https://doi.org/10.1016/j.apsusc.2017.11.007
Zhu L, Song H, Zhang D, Wang G, Zeng Z, Xue Q (2017) Negatively charged polysulfone membranes with hydrophilicity and antifouling properties based on in situ cross-linked polymerization. J Colloid Interface Sci 498:136–143. https://doi.org/10.1016/j.jcis.2017.03.055
Zodrow K, Brunet L, Mahendra S, Li D, Zhang A, Li Q, Alvarez PJJ (2009) Polysulfone ultrafiltration membranes impregnated with silver nanoparticles show improved biofouling resistance and virus removal. Water Res 43:715–723. https://doi.org/10.1016/j.watres.2008.11.014
Zou F, Zhou H, Jeong DY, Kwon J, Eom SU, Park TJ, Hong SW, Lee J (2017) Wrinkled surface-mediated antibacterial activity of graphene oxide nanosheets. ACS Appl Mater Interfaces 9:1343–1351. https://doi.org/10.1021/acsami.6b15085
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The authors thank the Deanship of Scientific Research and RSSU at King Saud University for their technical support.
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The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group no (RG-1439-85).
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Shukla, A.K., Alam, J., Ansari, M.A. et al. Antimicrobial and antifouling properties of versatile PPSU/carboxylated GO nanocomposite membrane against Gram-positive and Gram-negative bacteria and protein. Environ Sci Pollut Res 25, 34103–34113 (2018). https://doi.org/10.1007/s11356-018-3212-7
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DOI: https://doi.org/10.1007/s11356-018-3212-7