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. 2022 Mar 14;12(6):1779–1790. doi: 10.1007/s13204-022-02422-9

Graphene nanoplatelets/CeO2 nanotiles nanocomposites as effective antibacterial material for multiple drug-resistant bacteria

Saliha ur Rehman 1, Robina Khan Niazi 2, M Zulqurnain 3, Qaisar Mansoor 5, Javed Iqbal 6, Aqsa Arshad 1,4,✉
PMCID: PMC8918601  PMID: 35308867

Abstract

Antibacterial agents with low toxicity to normal cells, redox activity and free radical scavenging property are urgently needed to address the global health crisis. The phenomenal conducting nature of graphene is a best fit to enhance the antibacterial properties of metal oxides. In this work, CeO2 nanotiles and graphene nanoplatelets/CeO2 nanotiles nanocomposites (G/CeO2) have been synthesized by a solvothermal method. The prepared materials have been characterized using XRD, FE-SEM, EDX, and UV–visible spectroscopy techniques to investigate their crystallinity, morphology, composition, and optical bandgap energies. The CeO2 and G/CeO2 nanocomposites have also been tested for antibacterial applications. The neat CeO2 nanotiles sample inhibits the bacterial growth of Pseudomonas aeruginosa and Staphylococcus aureus up to 14.21% and 39.53% respectively. The antibacterial activity was tremendously enhanced using 25% graphene-loaded sample (G/CeO2-II) i.e., approximately 83% loss of P. aeruginosa and 89% in case of S. aureus has been observed. This can be attributed to the unique nano-architecture, oxidative stress due to the excellent ability of reversible conversion between the two electronic states of CeO2 and the stress exerted by the planar graphene and CeO2 nanotiles. Therefore, the G/CeO2 nanocomposites can find potential application as nano-antibiotics for controlling pathogens.

Keywords: Ceria nanotiles, Graphene nanoplatelets, Antibacterial properties

Introduction

Antimicrobial drug resistance (ADR) is one of the greatest health issues faced globally (Majumder et al. 2020). Antibiotics are the human defence armours that fight against pathogens, but the excessive use of antibiotics and rapid transfer of resistance genes has led to ineffective antibiotics. The alarming rate of worldwide antibiotic resistance has threatened the human health by increasing the mortality rate along with an increased treatment cost (AlSheikh et al. 2020). UN Ad hoc integrity coordinating group of antimicrobial resistance reported that drug resistance-related diseases cause 10 million deaths each year by 2025. Currently, 700,000 people die every year due to drug-resistant diseases, which includes 230,000 deaths due to multidrug-resistant (MDR) tuberculosis (TB). The severity of microbial co-infection is also highlighted in COVID-19 pandemic. Bacterial pathogens are highly probable to be found in viral respiratory infections like COVID-19. The use of antibiotics is essential in such cases (Langford et al. 2020). Therefore, the current global pandemic along with possibility of multiple drug resistance in the human body has posed major health challenges. TB, MRSA and VRE infections, diarrhoea, severe sexual complications and some CRE infections are caused by mycobacterium, Vancomycin-resistant Enterococci, Methicillin-resistant Staphylococcus aureus (MRSA), Neisseria gonorrhoea, Clostridium difficile and Carbapenem-resistant Enterobacteriaceae, i.e., Klebsiella species and Escherichia coli respectively. These bacteria have developed resistance to antibacterial drugs over the years. In many parts of the world, the high resistance of E. coli against fluoroquinolone antibiotics has made it ineffective in half of the patients suffering with urinary tract infections. The Staphylococcus aureus has also been resistant to first-line drugs. People with MRSA are 64% more probable to die than people with non-resistant form of bacteria (AL-Saadi 2016; Hibbitts et al. 2019). Therefore, some immediate steps are needed to prevent a potentially disastrous drug resistance, e.g., it is necessary to develop novel nano-medicines that have tendency to fight against bacterial infection-related morbidity.

Metal oxides have been a promising candidate (He et al. 2015) for the development of novel nano-antibiotics. They have other potential applications like photocatalysis, superconductivity, electronics, nanorobotics, and automobile industry (Zhang et al. 2020; Huang and Chen 2009; Kim et al. 2010; Halder and Sun 2019; Meixner et al. 1995; Kummer 1986). Many transition metal oxides show significant antibacterial performance towards a wide range of Gram-negative and Gram-positive bacteria (Paul et al. 2020; Talat et al. 2020). These properties are further enhanced if the same materials with reduced dimensions are employed, which mainly is attributed to distinct physicochemical properties appearing at nanoscale (Sanpo et al. 2013; Wang et al. 2010). Metal oxides have a common feature of producing oxidative stress due to generation of reactive oxygen species (ROS) in presence of UV light. CeO2 is unique as it can generate ROS even without UV light exposure (Jones et al. 2008). Moreover, the oxidative stress generation is a unique property of nano-CeO2 because it has an excellent ability of reversible conversion between its two electronic states in an auto-regenerative cycle (Ce4+ → Ce3+ → Ce4+) (Stoianov et al. 2014). CeO2 being a natural scavenger of ROS and nitrogen species, oxidizes from Ce (III) to Ce (IV) in the presence of ROS and then undergoes back to Ce (III) through a regeneration process. Therefore, CeO2 NPs can reduce oxidative stress by acting as antioxidants and may also be toxic to cancerous and bacterial cells by generating ROS under some conditions (Zhang et al. 2019). The ROS generating capability of CeO2 contributes towards inhibition of the bacterial growth, which is due to the oxidative stress on lipids and proteins (that are found in plasma membrane of microorganisms) caused by the reduction of Ce (IV) into Ce (III) (Gliga et al. 2017). Therefore, the antibacterial properties of CeO2 based materials are expected to be extraordinary as compared to other metal oxides, based on its naturally free radical scavenging property.

Also, metal oxide nanostructures with higher surface area than their bulk counterparts lead to higher chemical and biological activity. With these characteristics, metal oxide nanostructures can efficiently target cell membranes for better inactivation of bacteria (Subbiahdoss et al. 2012). These properties are also expected to enable nano-CeO2 to uniquely take up antibiotic drug resistance. However, it is always needed to add highly efficient antibiotic materials to the existing ones to combat ever increasing drug resistance (Bellio et al. 1860). Therefore, new strategies are required to improve antibacterial efficiency of CeO2. Some methods include its modification using dopants and (or) by compositing it with other chemical species. An effective strategy can be the formation of its composites with graphene family nano-materials. Graphene and CeO2 nano-composites have found various applications, e.g., as biosensors (Yang et al. 2016), cholesterol detectors (Zhang et al. 2013), catalysts (Yang et al. 2017), super-capacitive electrodes (Xie et al. 2018), anodes in lithium ion battery (Wang et al. 2011) and microwave absorbers (Wu et al. 2020).

Graphene-based metal oxide nano-composites have emerged as an extremely promising class of antibacterial materials due to their distinct electrical properties and low toxicity towards mammalian cells (Joung et al. 2011; Rojas-Andrade et al. 2017; Mathew et al. 2020; Alhazmi et al. 2022). When compared to published reports on biomedical applications of CeO2, very limited information is available on the biomedical applications of graphene-based CeO2 nanocomposites. Some related materials have been studied, e.g., antimicrobial efficiency of CeO2/GO nano-composites has been tested (Kashinath et al. 2019; Bharathi and Stalin 2019). However, the anti-bacterial activity of CeO2 and neat graphene nanocomposites has not been studied so far. Graphene-based composites are phenomenally effective in bacterial killing due to their bio-compatibility, sharp edges-based sheets like morphology and high specific surface area (Ni et al. 2010). Therefore, it can be anticipated that the antibacterial potential of CeO2 may possibly be enhanced by the formation of a unique nano-architecture of G/CeO2 nanocomposites.

Keeping in view the mentioned discussion, we aim to boost the antibacterial performance by synthesizing cutter-like morphology of CeO2 nanostructures so that it can act synergistically with the sharp edges of graphene to achieve an outstanding bactericidal or bacteriostatic behaviour against both Gram-negative and Gram-positive bacteria. Therefore, in this work, we present synthesis of CeO2 nanotiles and G/CeO2 nanocomposites and study their structural, morphological, optical, and antibacterial properties against two model pathogenic bacterial strains S. aureus and P. aeruginosa. S. aureus is found in skin and respiratory tract, causes a wide range of clinical infections i.e., pneumonia, pimples etc. It is a Gram-positive bacterium (Tong et al. 2015). P. aeruginosa causes pneumonia, septic shock and many blood infections in humans (Todar 2006). To the best of our knowledge, this is the first report on the synthesis of CeO2 nanotiles and the investigation of antibacterial behaviour of G/CeO2 nanocomposites.

Experimental

Preparation of CeO2 nanotiles

The materials used for making CeO2 and G/CeO2 nanocomposites are: cerium nitrate hexahydrate Ce(NO3)3.6H2O, 5 M aqueous sodium hydroxide solution (NaOH), isopropyl alcohol (99%, Sigma Aldrich), ethyl alcohol (99%, Merck), citric acid (C6H8O7), distilled water and graphene nanoplatelets (100%, KNANO) with the thickness ≤ 15 nm and size ca. 15 μm. All the chemicals were used as obtained.

A simple, surfactant-free and cost-effective solvothermal method was used to fabricate CeO2 and G/CeO2. The reaction took place in the beakers first and then it was shifted to an autoclave. Initially 8.642 g Ce (NO3)3.6H2O and 11.52 g C6H8O7 were dispersed in 100 ml distilled water separately in two beakers. These two solutions were mixed. This solution with pH 1 was stirred magnetically. A 5 M aqueous NaOH solution was then added drop-wise to the precursor solution to adjust its pH to 2. This solution was then shifted to an autoclave, which was heat-treated at 90 ℃ for 24 h. The solid was retained after washing it for three times in a centrifuge machine using distilled water and ethanol. The precipitates so collected were dried in oven at 120 ℃ overnight and were ground. The powder was heat-treated in a box furnace at 400 ℃ for 3 h to get a phase pure form.

Preparation of G/CeO2 nanocomposites

Two different samples of nanocomposites were synthesized using different quantities of graphene, i.e., 12% and 25% using a similar method depicted above, except the addition of GNPs. GNPs were dispersed ultrasonically in a solution containing distilled water and isopropyl alcohol (equal volume). This solution was then added to the CeO2 solution followed by similar procedure as depicted above. The process is presented schematically in Fig. 1. 

Fig. 1.

Fig. 1

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Schematic presentation of G/CeO2 synthesis

Antibacterial experiment

The effect of graphene-based CeO2 nanocomposites on P. aeruginosa and S. aureus can be studied by making disc diffusion assays. Disc diffusion method or Kirby–Bauer test method is used to check the effect of antibiotics on bacteria. We have followed the same protocol as described in previous work (Luc 2015; Arshad et al. 2017a). Briefly, in this testing method, bacteria are kept in agar plates and antibiotic wafers are placed on them. 10 mg/L of each test sample (CeO2, G/CeO2-I and G/CeO2-II) are sonicated in sterile water. 5 mL of LB medium (Luria–Bertani Broth) is mixed with 200 μL of each sonicated solution which is then inoculated into 100 μL of the bacterial culture in LB and incubated at 37 °C for 24 h.

Characterizations

The structural and phase analysis was performed using powder X-ray diffraction technique at PANalytical X’Pert PRO diffractometer. The surface, substructure and shape of prepared nanomaterials were obtained using SEM (MIRA3-TESCAN) that has a coupled electron dispersive X-ray (EDX) spectrometer. The absorbance profiles were studied using UV-1700 UV–visible spectrophotometer (SHIMADZU PharmaSpec). The Raman spectra were obtained using Raman spectrophotometer (Nost).

Results and discussion

Phase analysis

The phase purity of the samples is examined by X-ray diffraction. The XRD results of CeO2, G/CeO2-I and G/CeO2-II are shown in Fig. 2. The XRD peaks of prepared samples have been obtained from 20° to 80°. Results show that CeO2 nanotiles can be indexed to the pure fluorite cubic structure with a lattice constant a = 5.41 Å. These results match well with JCPDS card no. 00-004-0593 and literature (Kannan and Sundrarajan 2014; Hirano and Kato 1999). Diffraction peaks at 28.55°, 33.07°, 47.49°, 56.328°, 76.73° and 79.079° can be assigned to (111), (200), (220), (311), (331) and (420) planes of CeO2 respectively. No impurity peaks are observed in the pure CeO2 sample. In G/CeO2-I and G/CeO2-II, presence of (002) carbon peak at 2θ = 26.228° proves the composition of graphene with CeO2. This confirms the formation of biphasic G/CeO2 nanocomposites. We have also determined the interlayer spacing of neat GNPs and G/CeO2 nanocomposites. The interlayer spacing for neat GNPs is 3.35 Å, whereas it has increased for G/CeO2 nanocomposites to 3.37 Å. This increase in interlayer spacing may be attributed to the presence of CeO2 along with multiple graphene sheets. The average crystallite size is calculated using Scherrer’s equation, D=kλβcosθ. The crystallite size of neat CeO2 sample is estimated to be 14.14 nm which is reduced to 13.57 nm and 2.16 nm for G/CeO2-I and G/CeO2-II, as determined using (111) peak only.

Fig. 2.

Fig. 2

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a XRD pattern of CeO2 and G/CeO2 nanocomposites, and b C(002) peak of graphene nanoplatelets

Morphological study

The morphology of prepared samples has been studied by scanning electron microscope (SEM). Figure 3a–c shows the morphology details of all the three samples. Figure 3a reveals that the CeO2 sample has nano-tiles like structure with the thickness ranging from 76 to 113 nm. Figure 3b, c depict SEM micrographs of G/CeO2-I and G/CeO2-II respectively. Graphene nanopatches plastered on CeO2 nanotiles can be seen clearly, that confirm the formation of bi-phase G/CeO2 nanocomposites. The TEM images of G/CeO2-II nanocomposite are presented in Fig. 3d–f. These images depict the transparent sheet-like structures are graphene sheets as observed in Fig. 3d, e. The images also show the random presence of CeO2 nanotiles on the graphene sheets. The semi-transparent to transparent graphene nanosheets are clearly visible in Fig. 3e. Figure 3f shows that the thickness of one of the CeO2 nanotiles is 144.4 nm. The TEM images provide further insight into the morphology of the prepared samples and confirm the formation of G/CeO2 nanocomposite.

Fig. 3.

Fig. 3

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SEM images of a CeO2 nanotiles, b G/CeO2-I, c G/CeO2-II nanocomposites and TEM images of G/CeO2-II nanocomposite d–f

EDX analysis

The energy-dispersive X-ray spectroscopy has been used to investigate the elemental composition of the synthesized samples. Figure 4a shows the elemental composition of CeO2 nanotiles. The elemental presence of Ce and O ensures the formation of CeO2, and no impurity elements are observed. Carbon peaks can be observed in G/CeO2-I and G/CeO2-II nanocomposite samples, in addition to Ce and O peaks, shown in Fig. 4b, c which are due to presence of graphene. However, making the sample’s surface conductive is important, which has been achieved by carbon coating on the sample’s surface. Therefore, a low intensity peak related to carbon has also been observed in neat CeO2, which is due to carbon coating. No impurity peaks have been observed.

Fig. 4.

Fig. 4

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EDX results of CeO2 and G/CeO2 nanocomposites

Optical analysis

The absorbance of prepared samples is investigated using UV–vis spectrophotometer. Figure 5 shows the absorbance spectra of CeO2 and its composites with graphene. Since, all the samples show a definite absorption peak, therefore, in this case, it is preferred to find the bandgap energies using the relation, Eg=1240λeV. Here λ is the wavelength associated with the prominent peak in respective absorbance profiles of all the three samples. The bandgap energies so obtained are 4.14 eV (for CeO2), 3.86 eV (for G/CeO2-I) and 3.80 eV (for G/CeO2-II). The observed bandgap of CeO2 is slightly higher than the reported values for bulk CeO2, but it agrees well with a study where 4.65 eV bandgap has been reported for CeO2 nanoparticles (Safat et al. 2021). The quantum size effects that occur in materials with nanoscale dimension lead to an increase in bandgap energies, observed in this case (Srdanov et al. 1994). It has been observed that the bandgap energies show a decreasing trend in their value due to the inclusion of graphene, in G/CeO2-I and G/CeO2-II nanocomposites, respectively.

Fig. 5.

Fig. 5

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Absorbance verses wavelength plots of CeO2, G/CeO2-I and G/CeO2-II nanocomposites

The decreasing trend of energy bandgap values is attributed to new energy levels. The existence of new energy levels between valence and conduction bands of CeO2 in the nanocomposite systems are due to the modification in the electronic band structure in the composite material. Electronic interaction between CeO2 and graphene sheets may result in the introduction of energy states associated with defects, and modification of band structure due to inclusion of graphene in the vicinity of CeO2 (Arshad et al. 2017b).

Raman spectroscopy

The study of phonon modes of G/CeO2 nanocomposite using Raman spectroscopy is presented in Fig. 6. The symmetric stretching mode of Ce–O vibrations (Fluorite, F2g) is observed at 461.39 cm−1. The three primary features of the graphene Raman spectra are D, D' and G band. The G peak in G/CeO2-II nanocomposite is associated with E2g vibrational mode of ordered in-plane sp2 carbons and is a characteristic for all sp2-hybridized carbon structures. The structural defects and impurities express themselves as D band. GNPs and CeO2 nanotiles in the nanocomposite give rise to D band with enhanced intensity, as compared to that of neat GNPs. This also confirms the formation of nanocomposite and the surface modification of neat GNPs in the G/CeO2 nanocomposite. The increased width of D band also quantifies the induced disorder in GNPs which is due to CeO2 presence in the nanocomposite. The D and D’ peaks exhibit themselves at 1342 cm−1 and 2695 cm−1, respectively in G/CeO2-II nanocomposite.

Fig. 6.

Fig. 6

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Raman spectrum of G/CeO2-II nanocomposite

Antibacterial properties

The time kill assay is used to study the effect of CeO2 and G/CeO2 nanocomposites on Gram-negative and Gram-positive bacterial strains. The growth inhibition curves are obtained by recording optical density at 600 nm, at different intervals of time during incubation period 24 h. The control sample presents untreated bacterial strains. The bacterial growth inhibition curves of S. aureus and P. aeruginosa are shown in Fig. 7a, c, whereas Fig. 7b, d depicts the respective cell viabilities. It can be observed from antibacterial experiment that the bacterial growth is significantly inhibited in the presence of prepared materials. For P. aeruginosa, the growth inhibition rates are 14.21%, 61.58% and 82.67% for CeO2, G/CeO2-I nanocomposite and G/CeO2-II nanocomposite, respectively. The growth of S. aureus has been controlled up to 39.53% by CeO2, whereas G/CeO2-I and G/CeO2-II have inhibited the bacterial growth up to 62.4% and 89.48% respectively. It can be concluded from experimental data that neat CeO2 nanotiles have decreased the cell growth to some extent, but the inclusion of GNPs in the nanocomposites further decreases the number of viable bacterial cells. The nanocomposite with a maximum GNPs content has achieved maximum bacterial growth inhibition rate. It is also evident that the prepared materials show selective cytotoxicity towards the Gram-negative and Gram-positive bacteria.

Fig. 7.

Fig. 7

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a Growth profile of P. aeruginosa in the presence of CeO2 and G/CeO2 composites, b cell viability of P. aeruginosa, c growth profile of S. aureus in the presence of CeO2 and G/CeO2 composites and d cell viability of S. aureus

The exact mechanism for the antibacterial activity of metal oxides and graphene-based systems is still controversial; however, several hypothetical mechanisms have been proposed to account for the control of bacterial growth (Ji et al. 2016; Hegab et al. 2016). The cell composition of bacteria plays a substantial role to determine the toxicity level of prepared materials. Gram-positive bacteria have a single membrane encased by a thick peptidoglycan layer with attached proteins and different glycol polymers like polysaccharides, whereas in Gram-negative bacterial cell, the cytoplasmic membrane is covered by a thin peptidoglycan layer which is over-layered by an asymmetrical phospholipids bilayer having some polysaccharides and proteins (Shahriari et al. 2018). This difference accounts for the difference in functioning of active nanomedicine on P. aeruginosa and S. aureus as observed in the results depicted above. S. aureus being Gram-positive is easily targeted by G/CeO2 nanocomposite as compared to P. aeruginosa which is Gram-negative (Arshad et al. 2017a). The selective cytotoxicity is due to different outer layers of Gram-negative and Gram-positive bacteria, as discussed above, and observed in this study.

The interfusion of planar graphene on bacteria can be one of factors that is responsible for inducing the irreversible annihilation of bacterial membrane. It can be speculated form the morphology (Fig. 3) that the rough sharp edges of planar graphene exert stress on bacterial cell membrane which can cause damage to bacterial cell membrane and leakage of cytoplasmic content (Arshad et al. 2019). This disruption of membrane is not only limited to the graphene, but the unique morphology of CeO2, prepared in this work, also contributes towards bacterial membrane rupture. CeO2 nanotiles enter the bacterial cell by rupturing its membrane. The sharp blade like sides of CeO2 nanotiles make it easy to break the cell membranes, thus directly allowing the nanomedicine to interact with the bacterial cytoplasm. This dissolution of bacterial membrane proves to be fatal for bacteria. Also, when bacteria are exposed to CeO2 nanotiles, the electrostatic charge attraction between negatively charged bacterial cell membrane and positively charged CeO2 nanotiles causes its adhesion to the bacteria (Kuang et al. 2011). Moreover, graphene being an excellent electron acceptor creates a charge imbalance on the cell membrane of bacteria (Harris et al. 2010). The bacterial cell membrane and cell wall are typically negatively charged. The contact between graphene and bacterial membrane causes charge flow from membrane to the graphene conducting sheets. This charge imbalance leads to an interruption in bacterial respiratory activity that can cause bacterial cell death. The charge variation at bacterial surface may induce ROS production. The study of graphene toxicity reveals that graphene-based materials mediate oxidative stress. When cellular components are in direct contact with graphene sheets, superoxide anions are generated due to conducting graphene bridge. A related case is depicted for metallic SWCNTs, where the electron transfer from bacterial intracellular components to external environment takes place through metallic SWCNTs (Vecitis et al. 2010). Graphene can also produce similar effects by modifying bacterial DNA, lipids, and proteins by following the similar analogy. Strong oxidation by RGO is also observed in a study (Liu et al. 2011) which also supports that rGO nanosheets can oxidize thiol groups of proteins and other bacterial cellular components.

The unique composition of prepared nanocomposites is also an important factor that determines the bacterial death. CeO2 has a very important feature related to Ce3+ to Ce4+ ratio. CeO2 nanotiles when enter inside bacterial cell may allow redox conversion of Ce ions. Ce4+ atoms may undergo a reduction process from Ce4+ to Ce3+ and vice versa in the cell environment. Generally, Ce3+ to Ce4+ ratio is maintained by CeO2(IV) + e− ⟶ CeO2(III). The ratio of Ce3+ also affects the bandgap values which ultimately influence the antioxidant ability of CeO2. This transformation to Ce3+ is the key parameter to control the ROS generation for effective antibacterial activity (Ansari et al. 2014).

Generally, the metal oxide nanostructures (CeO2 nanotiles, in this case) can affect the cell viability into two ways either by influencing nutrient transport or by inducing oxidative stress. NPs have a high tendency to interact with biomolecules at sub-cellular level. There are proteins present on the cell membrane that extrude from bacterial membrane to perform nutrients transportation. Ce4+ nanotiles bind with thiol group (-SH) of these proteins resulting in enlarged proteins and decreased membrane permeability. This leads to the bacterial cell death due to lacking nutrients (Zhang et al. 2019). The Ce4+ nanotiles interacting with periplasm and DNA may cause difficulty in cell respiration and interferes with DNA replication and cell division, which in turn hinders the normal function of bacteria. The other factor, i.e., oxidative stress is mainly being developed by ROS generation. ROS are generated as by product of normal metabolic reaction and mitochondrion is the leading organelle responsible for its production. While generating ATP, various ROS like free radicals (i.e., OH−, ·OH, 1O2), superoxide ions (i.e., O2−) and nonradical molecules (i.e., H2O2) are formed. Also, the inter-conversion of Ce3+ and Ce4+ amplifies ROS generation. ROS-induced bacterial cell death is composed of oxidative stress and membrane lipid peroxidation. These highly reactive oxygen species can harm the individual bacterial components, such as proteins, mitochondria and nucleic acids, which leads to the interruption of bacterial cell cycle and ultimately induces cell death (Stankic et al. 2016). A detailed version of reactions taking place between G/CeO2 and bacteria is demonstrated below (Korsvik et al. 2007; Banavar et al. 2021):

G/CeO2→G+CeO2⟷Cell AtmosphereG+Ce3+/Ce4++O2
O2.-+Ce4+→O2+Ce3+
O2.-+Ce3++2H+→H2O2+Ce4+
2O2.-+2H+→H2O2+O2

Another factor that may govern the antibacterial activity is the optical bandgap energy of CeO2. The suitable light with energy enough to generate the charge carriers (i.e., electrons and holes) when falls on the material, helps the electrons and holes to be available for the generation of ROS. The ROS are essential for effective antibacterial activity. The observed bandgap for CeO2, and G/CeO2 nanocomposites falls in the UV range. Therefore, only a small fraction of light photons may contribute towards the generation of reactive oxygen species, in this case. From the above discussion, we conclude that both graphene and the CeO2 nanotiles, synergistically restrict the bacterial proliferation. A hypothetical mechanism based on the toxicity of planar graphene sheets and CeO2 nanotiles against bacterial pathogens is shown in the Fig. 8. All the possible factors that may influence the bacterial cell death in the presence of G/CeO2 are presented schematically below.

Fig. 8.

Fig. 8

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Schematic illustration of antibacterial activity by G/CeO2 nanocomposite

Various metal nanoparticles, metal oxide nanoparticles and their graphene-based composites have been employed to control bacterial growth. Biosynthesized CeO2 NPs and their nanocomposites have been previously demonstrated as good antibacterial agents. Also, some graphene family materials have also shown significant antibacterial properties. These results are tabulated in Table 1. CeO2 and GO/CeO2 have been analysed as an antibacterial material previously (Bharathi and Stalin 2019; Kannan and Sundrarajan 2014; Arunachalam et al. 2018; Surendra and Roopan 2016; Hassan et al. 2012; Magdalane et al. 2017; Ravishankar et al. 2015; Yadav et al. 2017; Arumugam et al. 2015; Babu et al. 2014; Khadar et al. 2019; Wang et al. 2013; Moongraksathum and Chen 2018), but this work, for the first time evaluates the antibacterial activity of G/CeO2 nanocomposites. The results are promising. Almost 83% growth inhibition of P. aeruginosa and 89% growth inhibition of S. aureus by the G/CeO2 has been achieved in this work. The unique morphology of CeO2 nanotiles has been one of the helpful factors towards achieving an excellent antibacterial performance as demonstrated in our work.

Table 1.

Bacterial growth inhibition performance of different metal, metal oxide and graphene-based nanomaterials on P. aeruginosa and S. aureus

Material Bacterial growth inhibition % or ZoI (mm)
P. aeruginosa 		Bacterial growth inhibition % or ZoI (mm)
S. aureus 		References
GO 48% 93.7% Sengupta et al. (2019)
G QDs Not tested 92% Ristic et al. (2014)
CuO Not tested 16 mm Abboud et al. (2014)
RGO-Cu2O Not tested 65% Yang et al. (2019)
Nitrogen doped CeO2 Not tested 18 mm Iqbal et al. (2020)
CeO2 NPs extracted from Prosopis juliflora leaf 4.09 ± 0.22 12.43 ± 0.36 Arunachalam et al. (2018)
CeO2 NPs extracted from Moringa oleifera peel Not tested 5 mm Surendra and Roopan (2016)
CeO2 NPs extracted from Acalypha indicia Not tested 90% Kannan and Sundrarajan (2014)
Ce2O3/TiO2 Not tested 100% Hassan et al. (2012)
CeO2/Y2O3 17 mm 20 mm Magdalane et al. (2017)
CeO2 NPs extracted from Gloriosa Superba leaf 4.50 ± 0.29 Not tested Ravishankar et al. (2015)
CeO2 Not tested 11.67 ± 0.33 Yadav et al. (2017)
CeO2 NPs 4.67 mm Not tested Arumugam et al. (2015)
CeO2/Au Not tested 70.6% Babu et al. (2014)
CeO2-peppermint oil-PEO/GO Not tested 22.5 mm Bharathi and Stalin (2019)
8 M% Co doped CeO2 Not tested 23 mm Khadar et al. (2019)
Dextran coated CeO2 NPs 55.4% Not tested Wang et al. (2013)
Ag/CeO2–TiO2 Not tested 99.99% Moongraksathum and Chen (2018)
CeO2 nanoparticle-coated silk fabric 65% 88% Lu et al. (2014)
G/Cr2O3 80.76% 84.25% Talat et al. (2020)
G/CeO2 83% 89% Present study
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The work suggests G/CeO2 as an effective antibacterial material. However, the performance of this material can be further investigated by studying a dose-dependent response of the prepared material. This study only addresses the use of 10 mg/L of prepared samples, which has achieved 83% and 89% growth inhibition. The work can be extended to get the response of prepared materials towards growth inhibition of other bacterial strains (not included in this work).

Conclusion

G/CeO2 nanocomposites are successfully synthesized using a hydrothermal process. The XRD results reveal that CeO2 exists as fluorite crystal structure in G/CeO2 nanocomposite, thus confirming the bi-phase nature of the prepared nanocomposites. The morphology analysis obtained using FE-SEM shows that CeO2 exists as nanotiles, while semi-transparent sheets like graphene are also clearly observed in the nanocomposites. The EDX results confirm the purity and elemental composition of the samples. The optical properties as obtained from UV–vis spectroscopy indicate that the inclusion of graphene into neat CeO2 decreases the bandgap up to 3.80 eV in G/CeO2-II nanocomposite. The G/CeO2-II nanocomposite shows excellent antibacterial activity, i.e. up to 83% loss of P. aeruginosa and approximately 89% in case of S. aureus. The antibacterial performances of all the prepared nanomaterials reveal that G/CeO2-II can be considered as promising antibacterial material. It is noteworthy that the antibacterial activity of these nanomaterials may be attributed to the reversible conversion of Ce (III) and Ce (IV). The unique cutter-like morphology of CeO2 and graphene inclusion synergistically enhances the activity. These findings can be a landmark to combat ADR and developing PPE (personal protective equipment) in current global health crisis.

Acknowledgements

The similarity index checked via Turnitin ID: 1561698025, is 8%, well below the allowed limit of HEC. A. A acknowledges HEC for financial support. A. A. extends gratitude to Dr. K. Nadeem for the experimental support.

Funding

The funding had been received from Higher Education Commision, Pakistan Grant no. 980/01.

Declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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