Indicators of water biotoxicity obtained from turn-off microbial electrochemical sensors
Graphical abstract
Introduction
Water monitoring is critical to reducing potential risks to the environment and human health due to contamination accidents (Do et al., 2020; Dong et al., 2020; Jiang et al., 2018). Various biosensors have been developed with an appropriate bioreceptor and conductor to estimate the biological response of environmental pollutants (Guo and Liu, 2020; Hao et al., 2020; Yi et al., 2020a). Among these biosensors, microbial electrochemical sensors (i.e., microbial fuel cell-based sensors) have attracted considerable attention in the last decades (Gonzalez-Pabon et al., 2021; Hill et al., 2020), and are expected to provide early warning of the presence of environmental pollutants (Liu and Wang, 2020; Xu et al., 2021a, 2021b). In microbial electrochemical sensors, electroactive microbes use electrodes as the final electron donor or acceptor for respiration (Choudhury et al., 2021; Jiang et al., 2019b; Khoo et al., 2020). The presence of toxic compounds in the aquatic environment can inhibit the extracellular electron transfer (EET) between electroactive microbes and electrodes. This response can be recorded as an electric signal (Chu et al., 2021a). For example, the anodic current can be inhibited by the presence of toxic compounds.
Much effort has been devoted to the fabrication of microbial electrochemical sensors to detect a wide variety of toxic compounds, including heavy metals, pesticides, and antibiotics (Chu et al., 2021a; Hao et al., 2020; Qi et al., 2021). In addition, many studies were conducted to improve the performance of microbial electrochemical sensors, focusing on novel reactors (Chu et al., 2021b; Jiang et al., 2017; Sun et al., 2021; Uria et al., 2020), parameter optimization (Jiang et al., 2015; Li et al., 2021; Xing et al., 2021), model development (Askari et al., 2021), criteria development (Xu et al., 2021a), and bioelectrode design (Chu et al., 2021c; Lazzarini Behrmann et al., 2020; Yi et al., 2020b).
The application of microbial electrochemical sensors is hampered by the lack of an indicator with high response magnitudes, although only a few studies have focused on this aspect. Typically, the current is recorded and used as an indicator in microbial electrochemical sensors (Xing et al., 2020). However, the current is only correlated with the EET rate but does not reflect other characteristics of bioelectrodes for the assessment of the cell status, including conductivity and thickness (Naradasu et al., 2020).
Fortunately, many electrochemical analyses were developed to understand the mechanism of bioelectrodes (Sanchez et al., 2020), and these electric signals could potentially be used as water monitoring indicators. For example, the peak of cyclic voltammetry (CV) has recently been utilized as an indicator of Cr(VI) contamination using microbial electrochemical sensors (Lazzarini Behrmann et al., 2020). The limiting current of the CV curve decreases with the addition of aluminum (Li et al., 2016). The peak of differential pulse voltammetry (DPV) has been used as an indicator of dopamine detection in turn-on chemical sensors and has shown higher sensitivity than the CV method (Xu et al., 2018). The DPV method has also been used to assess the electrochemical characteristics of bioelectrodes for energy generation and conversion (Chu et al., 2020). It is unknown whether the peak of DPV is a better indicator of water biotoxicity than the peak of CV in turn-off microbial electrochemical sensors.
Impedance sensing techniques have been suggested as non-invasive methods to assess the cell status of non-electroactive microbes (Afkhami et al., 2017). Electrochemical impedance spectroscopy (EIS) has also been used in microbial electrochemical reactors to investigate the characteristics of materials, configurations, and microbial interactions (Sanchez et al., 2020). Impedimetric transducers have been used to detect non-electroactive microbes and their metabolites (Brosel-Oliu et al., 2019a); however, their use as biosensors for cellular adhesion has rarely been reported (Brosel-Oliu et al., 2019b). It is unknown whether EIS data can be used as an indicator of water biotoxicity in microbial electrochemical sensors. In addition, it is unclear if real-time impedance analysis of microbial electrochemical sensors can be used for water biotoxicity monitoring with high response magnitudes.
The objective of this study is to select an indicator of water toxicity with high response magnitudes from various electrochemical analyses for use in water monitoring with microbial electrochemical sensors. In this study, several indicators (current, CV peak, DPV peak, and resistance of EIS) are systematically compared for water biotoxicity monitoring using microbial electrochemical sensors. Interdigitated electrode arrays (IDAs) are used for the enrichment of the electroactive biofilm since it has a low double-layer capacitance and a high mass transfer coefficient (Furst and Francis, 2019). The evolution of these indicators is compared during the enrichment of the electroactive biofilm with fixed electrode potentials of −0.3 V and −0.1 V, respectively. The correlation between the current, the most commonly used indicator, and other indicators is analyzed. In addition, the indicators are analyzed and compared in two toxicity assessments with formaldehyde injection. Subsequently, the possibility of using of microbial electrochemical sensors for real-time impedance analysis for water monitoring is evaluated.
Section snippets
Reactor construction and operation
A single-chamber microbial electrochemical reactor (500 mL) was constructed (Fig. S1). It consisted of the IDAs as working electrodes, a platinum plate (10 mm × 10 mm × 0.2 mm) as the counter electrode, and Ag/AgCl (saturated KCl, Gaoss Union Co., Ltd., Wuhan, China) as the reference electrode. The IDAs were obtained commercially (Guangzhou Mecart Sensor Technology Co., Ltd., Guangzhou, China), and each consisted of 25 pairs of microelectrode fingers separated by a 5 μm gap on the silica
Evolutions of indicators during the enrichment of biofilm
The evolutions (Fig. 1) and calculated values (Fig. S3) of the indicators during the enrichment of the electroactive biofilm were evaluated. The amperometric i-t curves indicated that the startup time was 9 d for the bioelectrodes at −0.3 V and −0.1 V (Fig. 1A). However, the maximum current output of the IDAs was 2.3 times higher at −0.3 V (0.025 mA) than at −0.1 V (0.011 mA). A discrepancy in the effect of the anodic potential on the current output was observed in previous studies. Some found
Implications
In the present study, biotoxicity indicators were compared to assess the use of microbial electrochemical sensors for water monitoring. The IR based on the R of EIS was comparable to and even higher than that based on the current. The current was affected by the microbial catalytic turnover of the substrate and the EET (Naradasu et al., 2020). However, the impedance was affected by the conductivity and thickness of the electroactive biofilm (Sanchez et al., 2020). These results suggested that
Conclusions
Indicators from various electrochemical analyses were compared for water monitoring with a microbial electrochemical sensor consisting of IDAs. Only the resistance of EIS provided a comparable response to the current or a higher response. However, no clear response was observed in the real-time impedance analysis for water biotoxicity monitoring. Most of the microbes were in the PI-permeable state, although the current was fully recovered. Hence, further studies are required to ensure that the
Credit author statement
Na Chu: Conceptualization, Investigation, Writing – original draft preparation, Writing- Reviewing and Editing. Jiayi Cai: Writing - Reviewing and Editing. Zhigang Li: Writing - Reviewing and Editing. Yu Gao: Writing - Reviewing and Editing. Qinjun Liang: Writing - Reviewing and Editing. Wen Hao: Writing - Reviewing and Editing. Panpan Liu: Writing - Reviewing and Editing. Yong Jiang: Conceptualization, Methodology, Investigation, Writing – original draft preparation, Supervision. Raymond
Declaration of competing 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.
Acknowledgments
This work was supported by the Fujian Provincial Natural Science Foundation of China (2020J01563), the National Natural Science Foundation of China (51908131).
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