Fate and toxicity of graphene oxide in aquatic environment
Lü Xiao-hui1,2, CHEN Bai-yang1, ZHU Xiao-shan2
1. Shenzhen Key Laboratory of Water Resource Utilization and Environmental Pollution Control, Harbin Institute of Technology Shenzhen Graduate School, Shenzhen 518055, China;
2. Shenzhen Key Laboratory for Coastal Ocean Dynamic and Environment, Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China
As a special graphene derivative, graphene oxide features unique properties and broad applicability in a wide range of industrial areas. However, due to its high hydrophilicity and surface reactivity, its fate and environmental risks to aquatic organisms in the environment have drawn considerable attention worldwide recently. Therefore, more knowledge regarding the aquatic behaviors and ecological effects of graphene oxide is of great importance to guide its future application and recovery. In this context, this review summarized a list of literature concerning the fate of graphene oxide in the environment, including dispersion/aggregation, adsorption, and reduction of graphene oxide, as well as its toxicity to a variety of aquatic organisms, such as zooplanktons and fishes.Accordingly, this paper discussed some challenges and prospects of its use on future studies.
Zhu Y, Murali S, Cai W, et al. Graphene and graphene oxide:synthesis, properties, and applications[J]. Advanced Materials, 2010,22(35):3906-3924.
[2]
Zhao J, Wang Z, White J C, et al. Graphene in the Aquatic Environment:Adsorption, Dispersion, Toxicity and Transformation[J]. Environmental Science & Technology, 2014,48(17):9995-10009.
Dreyer D R, Park S, Bielawski C W, et al. The chemistry of graphene oxide[J]. Chemical Society Reviews, 2010,39(1):228-240.
[5]
Paredes J I, Villar-Rodil S, Martinez-Alonso A, et al. Graphene oxide dispersions in organic solvents[J]. Langmuir, 2008,24(19):10560-10564.
[6]
Compton O C, Nguyen S T. Graphene oxide, highly reduced graphene oxide, and graphene:versatile building blocks for carbon-based materials[J]. Small, 2010,6(6):711-723.
[7]
Hegab H M, Zou L D. Graphene oxide-assisted membranes:Fabrication and potential applications in desalination and water purification[J]. Journal of Membrane Science, 2015,484:95-106.
[8]
Ren W, Mura S, Irudayaraj J M K. Modified graphene oxide sensors for ultra-sensitive detection of nitrate ions in water[J]. Talanta, 2015,143:234-239.
[9]
Balapanuru J, Yang J-X, Xiao S, et al. A graphene oxide-organic dye ionic complex with DNA-sensing and optical-limiting properties[J]. Angewandte Chemie-International Edition, 2010,49(37):6549-6553.
[10]
Zhang L M, Xia J G, Zhao Q H, et al. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs[J]. Small, 2010,6(4):537-544.
[11]
Szabo T, Berkesi O, Forgo P, et al. Evolution of surface functional groups in a series of progressively oxidized graphite oxides[J]. Chemistry of Materials, 2006,18(11):2740-2749.
[12]
Cote L J, Kim J, Tung V C, et al. Graphene oxide as surfactant sheets[J]. Pure and Applied Chemistry, 2011,83(1):95-110.
[13]
Chowdhury I, Duch M C, Mansukhani N D, et al. Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment[J]. Environmental Science & Technology, 2013,47(12):6288-6296.
[14]
Lanphere J D, Luth C J, Walker S L. Effects of solution chemistry on the transport of graphene oxide in saturated porous media[J]. Environmental Science & Technology, 2013, 47(9):4255-4261.
[15]
Hua Z, Tang Z, Bai X, et al. Aggregation and resuspension of graphene oxide in simulated natural surface aquatic environments[J]. Environmental Pollution (Barking, Essex:1987), 2015,205:161-169.
[16]
Zhao J, Liu F, Wang Z, et al. Heteroaggregation of graphene oxide with minerals in aqueous phase[J]. Environmental Science & Technology, 2015,49(5):2849-2857.
[17]
Lanphere J D, Rogers B, Luth C, et al. Stability and transport of graphene oxide nanoparticles in groundwater and surface water[J]. Environmental Engineering Science, 2014,31(7):350-359.
[18]
Chowdhury I, Hou W C, Goodwin D, et al. Sunlight affects aggregation and deposition of graphene oxide in the aquatic environment[J]. Water Research, 2015,78:37-46.
[19]
Qi Z, Zhang L, Wang F, et al. Factors controling transport of graphene oxide nanoparticles in saturated sand columns[J]. Environmental Toxicology and Chemistry, 2014,33(5):998-1004.
[20]
Fu H, Qu X, Chen W, et al. Transformation and destabilzation of graphene oxide in reducing aqueous solutions containning sulfide[J]. Environmental Toxicology and Chemistry, 2014,33(12):2647-2653.
[21]
Yang Z, Yan H, Yang H, et al. Flocculation performance and mechanism of graphene oxide for removal of various contaminants from water[J]. Water Research, 2013,47:3037-3046.
[22]
Tang L, Wang Y, Liu Y, et al. DNA-Directed self-assembly of graphene oxide with applications to ultrasensitive oligonucleotide assay[J]. Acs Nano, 2011,5(5):3817-3822.
[23]
Gorham J M, Wnuk J D, Shin M, et al. Adsorption of natural organic matter onto carbonaceous surfaces:Atomic force microscopy study[J]. Environmental Science & Technology, 2007,41(4):1238-1244.
[24]
Ren X, Li J, Tan X, et al. Impact of Al2O3 on the aggregation and deposition of graphene oxide[J]. Environmental Science & Technology, 2014,48(10):5493-5500.
[25]
Luo J, Cote L J, Tung V C, et al. Graphene oxide nanocolloids[J]. Journal of the American Chemical Society, 2010,132(50):17667-17669.
[26]
Yoon K Y, An S J, Chen Y, et al. Graphene oxide nanoplatelet dispersions in concentrated NaCl and stabilization of oil/water emulsions[J]. Journal of Colloid and Interface Science, 2013, 403:1-6.
[27]
Wu W Q, Yang Y, Zhou H H, et al. Highly efficient removal of Cu(Ⅱ) from aqueous solution by using graphene oxide[J]. Water, Air, & Soil Pollution, 2013,224(1):1372-1372.
[28]
Sitko R, Turek E, Zawisza B, et al. Adsorption of divalent metal ions from aqueous solutions using graphene oxide[J]. Dalton Transactions, 2013,42(16):5682-5689.
[29]
Zhao G, Wen T, Yang X, et al. Preconcentration of U(VI) ions on few-layered graphene oxide nanosheets from aqueous solutions[J]. Dalton Transactions, 2012,41(20):6182-6188.
[30]
Zhao G, Li J, Ren X, et al. Few-Layered Graphene oxide nanosheets as superior sorbents for heavy metal ion pollution management[J]. Environmental Science & Technology, 2011, 45(24):10454-10462.
[31]
Cui L, Wang Y, Gao L, et al. Removal of Hg(Ⅱ) from aqueous solution by resin loaded magnetic beta-cyclodextrin bead and graphene oxide sheet:Synthesis, adsorption mechanism and separation properties[J]. Journal of Colloid and Interface Science, 2015,456:42-49.
[32]
Jiu-Hua D, Xiu-Rong Z, Guang-Ming Z, et al. Simultaneous removal of Cd(Ⅱ) and ionic dyes from aqueous solution using magnetic graphene oxide nanocomposite as an adsorbent[J]. Chemical Engineering Journal, 2013,226:189-200.
[33]
Li X, Tang X, Fang Y. Using graphene oxide as a superior adsorbent for the highly efficient immobilization of Cu(Ⅱ) from aqueous solution[J]. Journal of Molecular Liquids, 2014,199:237-243.
[34]
Mishra A K, Ramaprabhu S. Functionalized graphene sheets for arsenic removal and desalination of sea water[J]. Desalination, 2011,282:39-45.
[35]
Chen W, Yan L, Bangal P R. Chemical reduction of graphene oxide to graphene by sulfur-containing compounds[J]. Journal of Physical Chemistry C, 2010,114(47):19885-19890.
[36]
Gao J, Liu F, Liu Y, et al. Environment-friendly method to produce graphene that employs vitamin C and amino acid[J]. Chemistry of Materials, 2010,22(7):2213-2218.
[37]
Bose S, Kuila T, Mishra A K, et al. Dual role of glycine as a chemical functionalizer and a reducing agent in the preparation of graphene:an environmentally friendly method[J]. Journal of Materials Chemistry, 2012,22(19):9696-9703.
[38]
Zhu C, Guo S, Fang Y, et al. Reducing sugar:new functional molecules for the green synthesis of graphene nanosheets[J]. Acs Nano, 2010,4(4):2429-2437.
[39]
Liu J, Fu S, Yuan B, et al. Toward a universal "adhesive nanosheet" for the assembly of multiple nanoparticles based on a protein-induced reduction/decoration of graphene oxide[J]. Journal of the American Chemical Society, 2010,132(21):7279-7281.
[40]
Salas E C, Sun Z, Luttge A, et al. Reduction of graphene oxide via bacterial respiration[J]. Acs Nano, 2010,4(8):4852-4856.
[41]
Wang G, Qian F, Saltikov C W, et al. Microbial reduction of graphene oxide by Shewanella[J]. Nano Research, 2011,4(6):563-570.
[42]
Jiao Y, Qian F, Li Y, et al. Deciphering the electron transport pathway for graphene oxide reduction by shewanella oneidensis MR-1[J]. Journal of Bacteriology, 2011,193(14):3662-3665.
[43]
Akhavan O, Ghaderi E. Escherichia coli bacteria reduce graphene oxide to bactericidal graphene in a self-limiting manner[J]. Carbon, 2012,50(5):1853-1860.
[44]
Khanra P, Kuila T, Kim NH, et al. Simultaneous biofunctionalization and reduction of graphene oxide by baker's yeast[J]. Chemical Engineering Journal, 2012,183:526-533.
[45]
Kuila T, Bose S, Khanra P, et al. A green approach for the reduction of graphene oxide by wild carrot root[J]. Carbon, 2012,50:914-921.
[46]
Li W, Tang X Z, Zhang H B, et al. Simultaneous surface functionalization and reduction of graphene oxide with octadecylamine for electrically conductive polystyrene composites[J]. Carbon, 2011,49(14):4724-4730.
[47]
Lv W, Tao Y, Ni W, et al. One-pot self-assembly of threedimensional graphene macroassemblies with porous core and layered shell[J]. Journal of Materials Chemistry, 2011,21(33):12352-12357.
[48]
Hou W C, Chowdhury I, Goodwin D G, Jr., et al. Photochemical transformation of graphene oxide in sunlight[J]. Environmental Science & Technology, 2015,49(6):3435-3443.
[49]
Li Z J, Chen F, Yuan L Y, et al. Uranium(VI) adsorption on graphene oxide nanosheets from aqueous solutions[J]. Chemical Engineering Journal, 2012,210:539-546.
[50]
Gao Y, Li Y, Zhang L, et al. Adsorption and removal of tetracycline antibiotics from aqueous solution by graphene oxide[J]. Journal of Colloid and Interface Science, 2012,368:540-546.
[51]
Hu X, Zhou M, Zhou Q. Ambient water and visible-light irradiation drive changes in graphene morphology, structure, surface chemistry, aggregation, and toxicity[J]. Environmental Science & Technology, 2015,49(6):3410-3418.
[52]
Zhang Y H, Tang Y l, Li S Y, et al. Sorption and removal of tetrabromobisphenol A from solution by graphene oxide[J]. Chemical Engineering Journal, 2013,222:94-100.
[53]
Apul O G, Wang Q, Zhou Y, et al. Adsorption of aromatic organic contaminants by graphene nanosheets:Comparison with carbon nanotubes and activated carbon[J]. Water Research, 2013,47(4):1648-1654.
[54]
Pavagadhi S, Tang A L L, Sathishkumar M, et al. Removal of microcystin-LR and microcystin-RR by graphene oxide:Adsorption and kinetic experiments[J]. Water Research, 2013, 47(13):4621-4629.
[55]
Kotchey G P, Allen B L, Vedala H, et al. The enzymatic oxidation of graphene oxide[J]. Acs Nano, 2011,5(3):2098-2108.
[56]
Girish C M, Sasidharan A, Gowd G S, et al. Confocal raman imaging study showing macrophage mediated biodegradation of graphene in vivo[J]. Advanced Healthcare Materials, 2013,2(11):1489-1500.
Kyzas G Z, Deliyanni E A, Matis K A. Graphene oxide and its application as an adsorbent for wastewater treatment[J]. Journal of Chemical Technology and Biotechnology, 2014,89(2):196-205.
[59]
Ruiz O N, Fernando KaS, Wang B, et al. Graphene oxide:A nonspecific enhancer of cellular growth[J]. Acs Nano, 2011, 5(10):8100-8107.
[60]
Liu S, Zeng T H, Hofmann M, et al. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide:membrane and oxidative stress[J]. Acs Nano, 2011,5(9):6971-6980.
[61]
Karmali P P, Simberg D. Interactions of nanoparticles with plasma proteins:implication on clearance and toxicity of drug delivery systems[J]. Expert Opinion on Drug Delivery, 2011, 8(3):343-357.
[62]
Akhavan O, Ghaderi E. Toxicity of graphene and graphene oxide nanowalls against bacteria[J]. Acs Nano, 2010,4(10):5731-5736.
[63]
Tang Y, Tian J, Li S, et al. Combined effects of graphene oxide and Cd on the photosynthetic capacity and survival of Microcystis aeruginosa[J]. The Science of the total environment, 2015,532:154-161.
[64]
Yue H, Wei W, Yue Z, et al. The role of the lateral dimension of graphene oxide in the regulation of cellular responses[J]. Biomaterials, 2012,33(16):4013-4021.
[65]
Mu Q, Su G, Li L, et al. Size-Dependent cell uptake of protein-coated graphene oxide nanosheets[J]. ACS Applied Materials & Interfaces, 2012,4(4):2259-2266.
[66]
Peng C, Hu W, Zhou Y, et al. Intracellular imaging with a graphene-based fluorescent probe[J]. Small, 2010,6(15):1686-1692.
[67]
Gurunathan S, Han J W, Dayem A A, et al. Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa[J]. International Journal of Nanomedicine, 2012,7:5901-5914.
[68]
Ahmed F, Rodrigues D F. Investigation of acute effects of graphene oxide on wastewater microbial community:A case study[J]. Journal of Hazardous Materials, 2013,256:33-39.
[69]
Castrillon S R V, Perreault F, De Faria A F, et al. Interaction of graphene oxide with bacterial cell membranes:insights from force spectroscopy[J]. Environmental Science & Technology Letters,2015,2(4):112-117.
[70]
Lei H, Mi L, Zhou X, et al. Adsorption of double-stranded DNA to graphene oxide preventing enzymatic digestion[J]. Nanoscale, 2011,3(9):3888-3892.
[71]
Li Y P, Wu Q L, Zhao Y L, et al. Response of microRNAs to in vitro treatment with graphene oxide[J]. Acs Nano, 2014,8(3):2100-2110.
[72]
Das S, Singh S, Singh V, et al. Oxygenated functional group density on graphene oxide:Its effect on cell toxicity[J]. Particle & Particle Systems Characterization, 2013,30(2):148-157.
[73]
Wang A, Pu K, Dong B, et al. Role of surface charge and oxidative stress in cytotoxicity and genotoxicity of graphene oxide towards human lung fibroblast cells[J]. Journal of Applied Toxicology, 2013,33(10):1156-1164.
[74]
Wahid M H, Eroglu E, Chen X J, et al. Entrapment of chlorella vulgaris cells within graphene oxide layers[J]. Rsc Advances, 2013,3(22):8180-8183.
[75]
Hu C W, Wang Q, Zhao H T, et al. Ecotoxicological effects of graphene oxide on the protozoan Euglena gracilis[J]. Chemosphere, 2015,128:184-190.
[76]
Nogueira P F M, Nakabayashi D, Zucolotto V. The effects of graphene oxide on green algae Raphidocelis subcapitata[J]. Aquatic toxicology (Amsterdam, Netherlands), 2015,166:29-35.
[77]
Hu X, Lu K, Mu L, et al. Interactions between graphene oxide and plant cells:Regulation of cell morphology, uptake, organelle damage, oxidative effects and metabolic disorders[J]. Carbon, 2014,80:665-676.
[78]
Ouyang S H, Hu X G, Zhou Q X. Envelopment-Internalization synergistic effects and metabolic mechanisms of graphene oxide on single-cell chlorella vulgaris are dependent on the nanomaterial particle size[J]. ACS Applied Materials & Interfaces, 2015,7(32):18104-18112.
[79]
Hu C, Wang Q, Zhao H, et al. Ecotoxicological effects of graphene oxide on the protozoan Euglena gracilis[J]. Chemosphere, 2015,128:184-190.
[80]
Van Hoecke K, Quik J T K, Mankiewicz-Boczek J, et al. Fate and effects of CeO2 nanoparticles in aquatic ecotoxicity tests[J]. Environmental Science & Technology, 2009,43(12):4537-4546.
[81]
Chen L, Hu P, Zhang L, et al. Toxicity of graphene oxide and multi-walled carbon nanotubes against human cells and zebrafish[J]. Science China-Chemistry, 2012,55(10):2209-2216.
[82]
Liu X T, Mu X Y, Wu X L, et al. Toxicity of multi-walled carbon nanotubes, graphene oxide, and reduced graphene oxide to zebrafish embryos[J]. Biomedical and Environmental Sciences, 2014,27(9):676-683.
[83]
Mu L, Gao Y, Hu X G. L-Cysteine:A biocompatible, breathable and beneficial coating for graphene oxide[J]. Biomaterials, 2015, 52:301-311.
[84]
Zhou X, Laroche F, Lamers G E M, et al. Ultra-small graphene oxide functionalized with polyethylenimine (PEI) for very efficient gene delivery in cell and zebrafish embryos[J]. Nano Research, 2012,5(10):703-709.
[85]
Mesaric T, Gambardella C, Milivojevic T, et al. High surface adsorption properties of carbon-based nanomaterials are responsible for mortality, swimming inhibition, and biochemical responses in Artemia salina larvae[J]. Aquatic Toxicology, 2015, 163:121-129.
[86]
Feng L, Liu Z. Graphene in biomedicine:opportunities and challenges[J]. Nanomedicine, 2011,6(2):317-324.
[87]
Geim A K, Novoselov K S. The rise of graphene[J]. Nature Materials, 2007,6(3):183-191.
[88]
Dan M, Wu P, Grulke E A, et al. Ceria-engineered nanomaterial distribution in, and clearance from, blood:size matters[J]. Nanomedicine, 2012,7(1):95-110.
[89]
Erickson K, Erni R, Lee Z, et al. Determination of the local chemical structure of graphene oxide and reduced graphene oxide[J]. Advanced Materials, 2010,22(40):4467-4472.
[90]
Perreault F, De Faria A F, Nejati S, et al. Antimicrobial properties of graphene oxide nanosheets:Why size matters[J]. Acs Nano, 2015,9(7):7226-7236.
[91]
Liu S, Hu M, Zeng T H, et al. Lateral dimension-dependent antibacterial activity of graphene oxide sheets[J]. Langmuir, 2012,28(33):12364-12372.
[92]
Liu J H, Yang S T, Wang H, et al. Effect of size and dose on the biodistribution of graphene oxide in mice[J]. Nanomedicine, 2012,7(12):1801-1812.
[93]
Chen Y M, Ren C X, Ouyang S H, et al. Mitigation in multiple effects of graphene oxide toxicity in zebrafish embryogenesis driven by humic acid[J]. Environmental Science & Technology, 2015,49(16):10147-10154.
[94]
Arias L R, Yang L. Inactivation of bacterial pathogens by carbon nanotubes in suspensions[J]. Langmuir, 2009,25(5):3003-3012.
[95]
Lyon D Y, Adams L K, Falkner J C, et al. Antibacterial activity of fullerene water suspensions:Effects of preparation method and particle size[J]. Environmental Science & Technology, 2006, 40(14):4360-4366.
[96]
Kang S, Mauter M S, Elimelech M. Microbial cytotoxicity of carbon-based nanomaterials:Implications for river water and wastewater effluent[J]. Environmental Science & Technology, 2009,43(7):2648-2653.
[97]
Hotze E M, Labille J, Alvarez P, et al. Mechanisms of photochemistry and reactive oxygen production by fullerene suspensions in water[J]. Environmental Science & Technology, 2008,42(11):4175-4180.
[98]
Ali-Boucetta H, Bitounis D, Raveendran-Nair R, et al. Purified graphene oxide dispersions lack in vitro cytotoxicity and in vivo pathogenicity[J]. Advanced Healthcare Materials, 2013,2(3):433-441.
[99]
Park S, Mohanty N, Suk J W, et al. Biocompatible, robust freestanding paper composed of a TWEEN/Graphene composite[J]. Advanced Materials, 2010,22(15):1736-+.
[100]
Liu Z, Robinson J T, Sun X M, et al. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs[J]. Journal of the American Chemical Society, 2008,130(33):10876-+.
[101]
Yang K, Zhang S, Zhang G, et al. Graphene in mice:Ultrahigh in vivo tumor uptake and efficient photothermal therapy[J]. Nano Letters, 2010,10(9):3318-3323.
[102]
Zhang S, Yang K, Feng L Z, et al. In vitro and in vivo behaviors of dextran functionalized graphene[J]. Carbon, 2011, 49(12):4040-4049.
[103]
Hu X G, Mu L, Wen J P, et al. Covalently synthesized graphene oxide-aptamer nanosheets for efficient visible-light photocatalysis of nucleic acids and proteins of viruses[J]. Carbon, 2012,50(8):2772-2781.
[104]
Duch M C, Budinger G R S, Liang Y T, et al. Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung[J]. Nano Letters, 2011, 11(12):5201-5207.
