Elsevier

Biochemical Engineering Journal

Volume 148, 15 August 2019, Pages 57-64
Biochemical Engineering Journal

Regular article
Deciphering electron-shuttling characteristics of epinephrine and dopamine for bioenergy extraction using microbial fuel cells

https://doi.org/10.1016/j.bej.2019.04.018Get rights and content

Highlights

  • Unveil dual role of epinephrine (EP) and dopamine (DA) as neurotransmitters and electron shuttles.

  • Uncover bioelectrochemical stimulation of EP and DA for power generation in microbial fuel cells.

  • Decipher more significant electrochemical characteristics of EP and DA than vitamin B2, vitamin C and gallic acid.

Abstract

This first-attempt study provided novel electrochemical exploration via microbial fuel cells (MFCs), suggesting why catecholamine hormone-neurotransmitters epinephrine (EP) and dopamine (DA) could effectively trigger acute stress responses for humans. According to bioelectrochemical engineering, EP and DA are ortho-diphydroxyl (o-diOH) substituent(s)-bearing electron shuttles (ESs) that could effectively mediate electron-transfer capabilities for bioenergy extraction. This study quantitatively compared redox-mediating characteristics of EP and DA with other antioxidants and ESs, suggesting possible mechanisms of bioenergy-driven responses to organisms. Although some electrochemical activities of EP and DA were characterized in medical literature, this work clarified that EP and DA were also electrochemically favorable ESs for efficient bioenergy extraction. Compared to vitamin B2 (VB), vitamin C (VC) and gallic acid (GA), quantitative evaluation upon bioenergy-stimulating capabilities of EP and DA were clearly revealed via MFC modules. Apparently, both EP and DA as ESs significantly exhibited stable and reversible redox potential peaks in cyclic voltammetry. Evidently, power density performances of MFCs supplemented with EP and DA considerably increased ca. 127–385%, suggesting that DA and EP would be the most appropriate ESs to effectively stimulate electron-mediating capabilities in multicellular organisms. It was also suspected that highly efficient power-stimulating capabilities of DA and EP could be strongly associated with their electrochemically-steered disease-curative and life-threatening capabilities to humans.

Introduction

Nowadays, with the gradually-increased shortage of non-renewable fossil energy, sustainable renewable and clean energy (e.g., solar, wind, hydroelectric, biomass, tidal, geothermal and oceanic energy) inevitably is top-priority focus for global energy. In fact, new sustainable energy technologies (e.g., hydrogen production and hydrogen fuel cells, building of green buildings, photovoltaics, biofuels, wind turbines, clean coal technology) were popularly mentioned due to significant improvement of energy utilization [1]. In particular, wind power generation and photovoltaics was once considered as the “cleanest” energy with the most significant potential to replace fossil fuel energy [2]. However, due to geological constraints and weather conditions, universal availability of such resources still remained problems to wide-range field applications [3]. Owing to abundance and biodiversity of natural bioresource, biomass-based energy would inevitably be one of the most appropriate renewable energy with environmental friendliness for sustainable development. In recent decades, bioelectric systems have potentially attracted great attentions as promising means for clean energy production. In particular, microbial fuel cells (MFCs) could effectively utilize microbial metabolism to extract energy from organic oxidation, simultaneously stimulating pollutant bioremediation for renewable bioenergy exploitation. In fact, with bioelectricity generation as a driving force, MFCs have been successfully applied to wastewater treatment, biological hydrogen generation, biosensing and bioelectrolysis [[4], [5], [6], [7]]. These all revealed that MFCs owned significant potential for applications to bioenergy and biorefinery. However, problems of scale up (e.g., poor electron transfer capabilities from cells to solid-phase electrode) still limited MFC performance to be in practice [8]. In fact, Logan et al. [9] implemented electrode modification through material replacement to the increase of specific surface area, significantly increasing the power generation of MFCs. That is, alternatives to provide more direct and faster electron transfer should significantly reduce electron transfer resistance for promising biological electricity production. As Liu et al [10] indicated, electrons could be transferred to solid-phase electrode in MFCs at least passed through three main pathways: the outer-membrane cytochromes (c-Cyts) complex, self-contained conductive structures (e.g., nanowire-generating bacteria) and exogenous electron shuttles (ESs). These all controlled overall performance of renewable bioenergy extraction in MFCs.

In fact, exogenous ESs (also known as redox mediators (RMs)) are organic molecules that can be reversibly oxidized and reduced with the ability to potentially act as electron carriers mediating in various redox reactions [11,12]. Exogenous augmentation of ESs could also increase the rate of redox reaction(s) and reduce electron transfer resistance, considerably augmenting power generation in MFCs for effective bioenergy extraction [12,13]. Furthermore, ES compounds could play an irreplaceable role in other fields for applications. Feldt et al. [14] increased the photoelectric conversion efficiency of dye-sensitized solar cells to 6.7% by using a newly designed D-π -A complex of organic sensitizer and cobalt complexes as ESs. Watanabe et al. [15] also reviewed that biotechnologists have attempted to create favorable routes of the electron flow mediating through microbes with aid of artificially-synthesized ESs. Such ES-associated bioprocesses included metal bioremediation, halogenated-organics bioremediation, azo-dye decolorization, and microbial fuel cells (MFCs). Supplementation of artificial ESs (e.g., neutral red, methylene blue and decolorized metabolites of azo dyes) could significantly improve the efficiency of bioelectricity generation in MFCs. However, using chemically-synthesized compounds with high cost and low biocompatibility would lead to concerns of secondary pollution to the environment. Inevitably, seeking naturally-present ESs to replace artificially-synthesized chemicals should be inevitable for effective renewable energy extraction with environmental friendliness. In fact, Watanabe et al. [15] mentioned some naturally-generated organics (e.g., humic substances) as ESs with better water solubility and biocompatibility for bioremediation applications. For example, Velasqnez-Orta et al. [18] implemented supplementation of flavins to successfully stimulate power generation in MFCs. Recently, Chen et al. [16,17] also quantitatively inspected polyphenols-abundant plant bioresource (e.g., extracts of medicinal herbs, Camellia and non-Camellia tea) as possible candidate ESs to effectively stimulate bioenergy generation in MFCs. In particular, these antioxidant polyphenolics-abundant herbs were ubiquitous over the globe. That is, a good grasp of such bioelectrochemical convertibility of antioxidants and ESs from natural polyphenols would provide sustainable alternatives for renewable bioenergy/biorefinery applications.

As prior studies [16,17] indicated, Camellia tea extract contained abundant ortho- or para-dihydroxyl substituents-bearing polyphenolic species that may own dual role of antioxidant and ES for electrochemically efficient bioenergy extraction. In fact, ortho-dihydroxyl substituent(s)-bearing chemicals (e.g., catechol, dopamine (DA) and epinephrine (EP)) were the basic essentials for worldwide lives (e.g., sufficient energy supply at daily life and life-threatening situations). For instance, DA is one of the significant catecholamine neurotransmitters in the mammalian central nervous system. It may cause neurological disorders (e.g., Parkinson's disease and schizophrenia) if the concentration of DA was not within appropriate levels [19,20]. In the presence of organic cation(s), EP is another popularly-mentioned neurotransmitter in the nervous system and body fluid, manipulating the nervous system to efficiently trigger serial biological reactions and nervous chemical processes [21]. As many biological reactions are coupled with redox reactions via electron transport chains, corresponding characteristics of electrochemical reactions are likely directly linked to the nervous chemical process for immediate responses/actions [22] (Fig. S-1 for mechanisms of EP and DA). That is, exploring convertibility of electrochemical characteristics of ESs and antioxidants for EP and DA would be of great significance to correlate with the effects of the nervous system (e.g., acute stress responses) for medical and pharmacological applications. In fact, Tsierkezos et al. [23] indicated the excellent synergistic redox capabilities of DA and EP in the presence of uric acid as disrupters. Literature [22,23] also indicated, there were even more than these fingerprint potential peaks exhibited in cyclic voltammetric profiles due to entirely different environments. In suggested that deciphering electrochemical convertibility between species of antioxidants and ESs would be growing concern over the sustainability of bioenergy utilization for the current industrial expansion.

This first-attempt study quantitatively assessed the electrochemical characteristics of EP and DA through systematic comparison of double chamber (DC)-MFCs with supplementation of well-known antioxidants or ESs (e.g., vitamin B2 (VB), vitamin C (VC) and gallic acid (GA)). This study clearly showed that EP and DA could play dual role of electroactive ES and antioxidant to electrochemically catalyze the rate of bioenergy extraction. This finding indicated that due to such highly efficient energy mediation, EP and DA could thus effectively coordinate actions of the nervous system. To have conclusive remarks upon electron-shuttling capabilities of EP and DA as ESs, this study clearly revealed how much of the significant electron-shuttling potential of EP and DA could be provided for sustainable bioenergy extraction in humans.

Section snippets

Cyclic voltammetric (CV) measurement

To determine electrochemical characteristics of antioxidant or ES for DA, EP, GA, VC, VB, cyclic voltammetry of 100 serial cycles of scan was carried out via electrochemical workstation (ALS/DY2325 BI-POTENTIOSTAT, Taiwan). For experimental measurement, a three-electrode system glassy carbon electrode (GCE, ID = 3 mm; model CHI104, CH Instruments Inc., USA) with area of 0.07 cm2 was used as the working electrode. The reference electrode was Hg/Hg2Cl2 electrode filled with saturated KCl(aq) and

Electrochemical feasibility assessment

To classify whether DA and EP exhibited either ES or reductant characteristics, DA, EP, GA, VC and VB were all adopted to quantitatively implement for comparative assessment of cyclic voltammetry. To obtain more detailed electrochemical activities (e.g., reversibility and stability), comparative inspections of 100 cycle-scanned CVs were quantitatively implemented. As indicated in 10th, 50th and 100th cycle CV profiles in Fig. 1(a–b), both DA and EP exhibited significant reductive and oxidative

Conclusion

Cyclic voltammetric analysis upon dopamine (DA), epinephrine (EP), vitamin B2, vitamin C and gallic acid indicated that DA and EP showed significantly stronger redox potential peaks. Power density performance of MFCs with supplemented DA and EP considerably increased ca. 127–385%, suggesting their outstanding electrochemically-stimulating capabilities for bioenergy extraction. As this comparative study revealed, electrochemically catalytic and sustainable ESs seemed to own much higher

Acknowledgements

The authors sincerely appreciate financial supports (MOST 106-2221-E-197-020-MY3, 106-2923-E-197-002-MY3, 107-2621-M-197-001) form the Taiwan's Ministry of Science and Technology for the project of Microbial Fuel Cells (MFCs)sdg conducted in Biochemical Engineering Laboratory, C&ME NIU. This study was completed as part of cooperative achievements for Academic Exchange Program between Yantai University (China) and National I-Lan University (Taiwan). This study is also dedicated to the memory of

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