Journal of Analysis and Testing

, Volume 2, Issue 1, pp 20–25 | Cite as

Electrochemical Biosensors for Detecting Microbial Toxins by Graphene-Based Nanocomposites

  • Girma Selale Geleta
  • Zhen Zhao
  • Zhenxin Wang


It is important to develop methods to determine microbial toxins at trace levels since these toxins are ubiquitous commonly found in water and foods, and pose potential threats to both human health and ecosystem safety. Taking the advantages of ultrahigh electron-transfer capability, extra-large surface area and easily functionalized ability, the graphene-based nanocomposites have been employed to fabricate electrochemical biosensors including immunosensors and aptasensors for detecting microbial toxins with high sensitivity. The specificity and selectivity of the electrochemical biosensors for targeting toxins can be achieved by combining graphene nanocomposites with antibodies and/or aptamers. The graphene nanocomposite-based electrochemical biosensors could become a promising technique in the detection of microbial toxins for public and environmental health protection.


Graphene nanocomposites Electrochemical immunosensors Electrochemical aptasensors Microbial toxins 

1 Introduction

The microbial toxins are generally catalogued into endotoxins (lipopolysaccharides, LPS) produced by Gram-negative bacteria, exotoxins (peptides and proteins) produced by Gram-negative or Gram-positive bacterial pathogens, and mycotoxins [e.g., deoxynivalenol (DON), aflatoxin, ochratoxin A (OTA), fumonisin B1 (FB1) and zearalenone] produced by certain fungi [1, 2, 3, 4]. With the molecular weight covering a broad range from less than 1 kDa to more than 100 kDa, these toxins exhibit different physico-chemical properties and are one of major threats to the life and health of humans and live stocks. Microbial toxins cause a broad variety of diseases, ranging from mild emesis and diarrhea to severe and fatal cancers and neurological disorders. For instance, Staphylococcus aureus enterotoxins (SEs) can cause gastroenteritis in the gastrointestinal tract and act as a superantigen on the immune system. Aflatoxin B1 (AFB1) has been listed as Group I carcinogens by the International Agency for Research on Cancer (IARC), a body of the World Health Organization. The poisonous effects of some of these molecules can be acute even at very low doses, and the cooccurrence of microbial toxins in nature may cause additive and/or synergistic effects.

Various methods/assays such as polymerase chain reaction (PCR), high-performance liquid chromatography (HPLC), high-performance liquid chromatography–tandem mass spectrometry (HPLC/MS/MS), surface plasmon resonance (SPR), electrochemical biosensors and immunoassays [e.g., competitive enzyme-linked immunosorbent assay (ELISAs) and microfluidic immunoassay] have been developed for detection of microbial toxins in different sources including foods, water and feeds [1, 2, 5, 6, 7, 8]. Among of these methods/assays, electrochemical biosensors are attractive since they have several advantages including high sensitivity, operational simplicity, low cost, and suitable rapid on-site analysis.

Due to its remarkable electrocatalytic activity and conductivity, graphene is an ideal material for electrochemical sensors and biosensors with the structure of the two-dimensional sheet of sp2-conjugated atomic carbon [9, 10, 11, 12, 13]. Researchers have demonstrated that incorporating graphenes and other materials (e.g., polypyrrole and gold nanoparticles) together in sensor platform provide biocompatibility, large surface area, ease of functionalization, and significantly improve the reproducibility, sensitivity, and stability. The graphene-based electrochemical biosensors are widely used in the detection of various analysts including bioactive small molecules, peptides, nucleic acids, proteins, enzymes and living cells [9, 10, 11, 12, 13]. In this chapter, the graphene nanocomposite-based electrochemical biosensors for sensing microbial toxins have been discussed and highlighted by the linear ranges, limits of detection (LODs), reproducibilities, and stabilities of these reported biosensors.

2 Sensing Strategies

Based on the sensing strategies, the electrochemical sensors can be mainly divided into three categories including amperometric sensor, voltammetric sensor and impedimetric sensors [14]. Amperometric sensors are detection of analytes based on the electric current or the change of electric current under a specific electrode potential which can be adjusted to maximize the response for the analyte of interest while minimizing the response for the interfering substances. Amperometric immunosensors are considered as a suitable method for the detection of contaminants in food since the sensors exhibit advantage of rapid, sensitive and selective quantification [15]. Voltammetric biosensors are based on electroanalytical chemistry, in which the current is measured by changing the potential and measuring the generated current when the electrochemical reaction occurs between the analyte and the working electrode surface. Differential-pulse voltammetry (DPV) and cyclic voltammetry (CV) are commonly used voltammetric sensing techniques which can be used to detect analytes with high sensitivities and low LODs and quantitatively analyze/fastly characterize reaction processes that take place on the surface of the sensing electrode. For example, based on exonuclease-catalyzed target recycling, Chen and coauthors have developed a voltammetric aptasensor of OTA with LOD of 1.0 pg mL−1 [16]. Electrochemical impedance spectroscopy (EIS) is a sensitive technology for analyzing the interfacial characteristics related to biometric identification, such as biomolecular recognition events, reactions catalyzed by enzymes occurring at the modified surface. In impedimetric biosensors, the binding of biomolecules can form a blocking layer on the electrode surface, resulting in resistance increases. Impedimetric biosensors allow direct detection of biomolecular recognition events without using labels. Chiriaco and coauthors have developed a flow-injection impedimetric immunosensor for direct and label-free detection of cholera toxin with a LOD smaller than 10 pmol L−1 in the buffer solution [17].

3 The Roles of Graphene Nanocomposites in the Electrochemical Biosenors

Based on their inherent natures, the graphene nanocomposites can be used as electrochemical labels for generating electrochemical signal, efficient units for immobilizing biomolecules on electrode surface, and strong enhancers for amplifying detecting signal [19, 20, 21, 22]. For instance, reduced graphene oxide-doped polypyrrole/pyrrole propylic acid nanocomposite (rGO-PPy/PPa) has been used to fabricate impedimetric immunosensor, in which rGO greatly improves the conductivity and stability, PPa provides covalent linkers for probe immobilization and PPy endows the film electroactivity from its inherent electrochemical doping/dedoping property for impedance measurements [18]. Graphene-oxide nanoplatelets (GONPs) are directly used as electroactive labels for aptasensing mycotoxin [19]. After treated with HNO3, the cadmium telluride quantum dots (CdTe QDs)-modified graphene/gold nanoparticle (AuNPs) nanocomposites (GAu/CdTe) can be served as electrochemical probe for ultrasensitive detection of OTA through electroredox of releasing Cd2+ from GAu/CdTe [20]. A novel aptasensor is designed by with the dual amplification of gold nanoparticles (AuNPs) and graphene/thionine nanocomposites (GSTH) for sensitive determination of FB1 [22]. In this case, AuNPs is modified to increase the electrical conductivity at the electrode surface and to produce a FB1-specific recognition interface by hybridization with capture DNA and its aptamer. A great quantity of TH molecules loaded on the graphene surface is served as electroactivating probe to increase its electrochemical signal due to the large surface area and excellent conductivity of graphene sheet.

4 Graphene Nanocomposite-Based Electrochemical Immunosensor

In 2001, the International Union of Pure and Applied Chemistry (IUPAC) defined an electrochemical immunosensor as an integrated device based on an antibody/antigen reaction, which can transform their concentration signals or certain chemical substances into a corresponding electric signal (e.g., current, potential, conductance and impedance) through the sensor element, and realize a specific semi-quantitative or quantitative analysis [14]. Up to date, various types of electrochemical immunosensors based on the graphene nanocomposites, including reduced graphene oxide-conductive polymer nanocomposites, amine-terminated dendrimer (PAMAM)-modified graphene oxide nanosheets, have also been proposed to detect microbial toxins in diverse matrices including foods, freshwater and feeds [18, 23, 24].

4.1 Detection Bacterial Toxins

The latest example is the impedimetric immunosensor for the label-free and direct detection of bacterial toxin [i.e., botulinum neurotoxin serotype A (BoNT/A)] using gold nanoparticles/graphene–chitosan composite (termed as, Au–Gr–Cs nanocomposite) [25]. The Au–Gr–Cs nanocomposites are prepared by directly growing AuNPs on chitosan (Cs)-coated graphene. The fabrication process of impedimetric immunosensor is shown in Fig. 1. The relationship of the impedance changes and the concentration of BoNT/A are well fitted into a simple linear regression in range of 0.27–268 pg mL−1. The LOD for the immunosensor is determined to be 0.11 pg mL−1, which is obtained based on the signal/noise ratio of three. Good recoveries and relative standard deviations (RSDs) are obtained for BoNT/A from serum and milk samples without any sample pretreatment. The obtained results fabricated immunosensor and ELISA method which are in good agreement without significant difference for 100.0 pg mL−1 of analyte. The results suggest that the immunosensor offers good precision and accuracy, low LOD and wide linear range, which are especially suitable for routine detection of BoNT/A in different samples. Similarly, Sharma and coauthors develop antibody-attached Au–Gr–Cs-modified glassy carbon electrode-based voltammetric immunosensor which can be used to detect 5 ng mL−1 staphylococcal enterotoxin B in practical sample within 35 min [26].
Fig. 1

a Immunosensor construction process, b SEM image of Au–Gr–Cs nanocomposite, and c comparison of performance of the impedimetric immunosensor for determination of BoNT/A in various samples. Reprinted with permission [25]

4.2 Detection of Mycotoxins

Using PPy-electrochemically-reduced graphene oxide (ErGO) and AuNPs nanocomposite film-coated disposable screen-printed carbon electrode (SPE) as sensing platform, Gunasekaran and coauthors report a voltammetric immunosensing method (as shown in Fig. 2) for rapid, selective and sensitive (LOD of 8.6 ppb for DON and 4.2 ppb for FB1) detection of two mycotoxins, DON and FB1 in co-existing toxins environment (i.e., spiked corn samples) [27]. In addition, the immunosensor exhibits good stability over 12 days [RSD of 5.8% (n = 3)]. The authors believe that, with specific antibodies, the sensing scheme is suitable for simultaneous detection of multiple co-contaminant mycotoxins individually. Tang and coauthors develop an impedimetric immunosensor for the fast detection of OTA in food samples through co-immobilization of amine-terminated dendrimer (PAMAM) and anti-OTA antibody on the graphene oxide nanosheets (termed as, anti-OTA–GO–PAMAM) which are used as the affinity support for the loading of Mn2+, and then functionalized on the electrode after a competitive-type assay format [28]. The anti-OTA–GO–PAMAM–Mn2+ can induce the formation of MnO2 in situ via classical redox reaction between KMnO4 and Mn2+ on the immune-sensing platform. Furthermore, the produced MnO2 nanoparticles as effective catalyst can catalyze the 4-chloro-1-naphthol (4-CN) oxidation without H2O2 to generate an insoluble precipitation on the platform. In the introduction of the target OTA, a competitive immune response is actualized between the analyte and the OTA–BSA immobilized on electrode for the anti-OTA antibody on the graphene oxide nanosheets labels. The as-prepared impedimetric immunosensor has wide dynamic working range (from 0.1 pg mL−1 to 30 ng mL−1) and low LOD (0.055 pg mL−1), and can be used to detect OTA in the red wine samples.
Fig. 2

a Illustration of step-by-step fabrication of the immunosensor, b electrochemical immunosensing employed for the detection of mycotoxins, and c stability of the immunosensor stored in 1× PBS at 4 °C over 12 days. Error bars are standard deviations of three independent measurements. Reprinted with permission [27]

5 Graphene Nanocomposite-Based Electrochemical Aptasensor

Nucleic acid aptamers are nucleic acid species with appropriate secondary structures containing 10–50 variable bases that have been engineered through repeated rounds of in vitro selection or equivalently, SELEX (systematic evolution of ligands by exponential enrichment) to bind to various molecular targets such as nucleic acids, small molecules, proteins, and even cells, tissues and organisms [29, 30, 31]. Due to their low cost production, ease to be labelled with different reporter molecules and coupling with different transduction systems, nucleic acid aptamers are ideal reagents for the development of biosensors. As earlier as 2002, Bruno and Kiel selected ssDNA aptamer against cholera toxin [29]. In 2008, Penner and Cruz-aguado evaluated the aptamer sequence (5′-GATCGGGTGTGGGTGGCGTAAAGGGAGCATCGGACA-3′) for OTA using in vitro process SELEX [30, 31]. During past decade, various aptasensors with different sensing strategies including fluorescence and electrochemistry have been developed for detection of multiple microbial toxins [1, 2, 32, 33, 34].

5.1 Detection Bacterial Toxins

Yuan and coauthors have developed a signal-on voltammetric aptasensor for the hypersensitive detection of Endotoxin, also known as LPS by combining the three-way DNA hybridization process and electroactive toluidine blue–graphene–gold nanoparticles (termed as, Tb–Gra–AuNPs) nanocomposite-based amplification [35]. With the cascade signal amplification, the proposed voltammetric aptasensor provides an ultrasensitive electrochemical detection of LPS down to the femtogram level (8.7 fg mL−1) with a linear range of six orders of magnitude (from 10 fg mL−1 to 50 ng mL−1). Zhang and coauthors reported a voltammetric aptasensor which is based on a competitive reaction between free FB1 in the sample and GS-TH nanocomposite, for an immobilized FB1 DNA aptamer (S2)/capture DNA/AuNPs at electrode surface [22]. The constructed aptasensor was applied successfully employed to detect FB1 in feed samples.

5.2 Detection of Mycotoxins

Zhao and coauthors have developed a visible-light-driven photoelectrochemical (PEC) aptasensor with high sensitivity and selectivity for cyanobacterial toxin Microcystin-LR (MC-LR) through immobilization of MC-LR aptamer onto vertically-aligned titanium dioxide nanotube (TiO2 NTs) photoanode substrate with the aid of graphene via ππ stacking interactions between the nucleobases of the DNA and the graphene hexagonal cells (as shown in Fig. 3) [36]. The functionalization of graphene further gives the visible light response activity of the aptasensor. The PEC aptasensor shows a linear relationship between the photocurrent increment and the MC-LR concentration ranging from 1.0 to 500 fmol L−1 and the LOD is determined as 0.5 fmol L−1. In addition, the aptasensor exhibits high selectivity towards detecting 100-fold concentration other several potential coexisting interferents. Amazingly, Pumera and coauthors has developed a voltammetric aptasensor for OTA by utilizing GONPs as electroactive label [19]. In this case, the GONPs are conjugated to OTA aptamers (OTA-apt) immobilized on the electrode surface through ππ interactions. The principle of detection relies on the ability of these nanoplatelets to be electrochemically reduced, leading to produce a well-defined reduction peak that can be used as the analytical signal (as shown in Fig. 4). The fabricated aptasensor shows the detection range of OTA in the concentration from 310 fmol L−1 to 310 pmol L−1, and good selectivity against common interferences. Additionally, the fabricated aptasensor has reasonable reproducibility (RSDs = 11.8%).
Fig. 3

Illustration for the construction of MC-LR PEC aptasensor. Reprinted with permission [36]

Fig. 4

Representation of the application of GONPs as inherently electroactive labels for the aptasensing of OTA. In the absence of OTA, the GONPs are adsorbed onto immobilized OTA-apt through ππ interactions. In the presence of OTA, OTA-apt binds specifically to OTA and lead to the partial removal of immobilized OTA-apt from the electrode surface, owing to conformational changes. GONPs then adsorb onto the remaining immobilized OTA-apt. Inset: molecular structure of OTA. Reprinted with permission [19]

6 Summary and Outlook

The graphene-based nanocomposites have already demonstrated great successes in the development of electrochemical biosensors for sensing microbial toxins. These biosensors exhibit outstanding performance which leads to develop miniaturized electronic and electrochemical devices for the practical or commercialized applications including real-time monitoring of food/feed quality and analysis of clinical samples. Due to the lack of facile methods for controllable, scalable, and reproducible, preparation of graphene materials with defined structures and properties, the development and widespread application of grapheme nanocomposite-based sensors are largely hindered. For example, extensively used graphene synthesis method (Hummers method) will produce acid wastes, and it is still a challenge for the preparation of pure single-layer graphene without residual oxygen groups on the surface. The electrical/chemical properties of reduced graphene-based nanocomposites may differ significantly since the morphology and chemical structure of reduced graphene are very sensitive to the method used for exfoliation and reduction. To move forward, it is, therefore, necessary to collaborate between different disciplines and technologies.


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Copyright information

© The Nonferrous Metals Society of China 2018

Authors and Affiliations

  • Girma Selale Geleta
    • 1
    • 2
  • Zhen Zhao
    • 1
    • 2
  • Zhenxin Wang
    • 1
  1. 1.State Key Laboratory of Electroanalytical Chemistry, Changchun Institute of Applied ChemistryChinese Academy of SciencesChangchunChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

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