Efficient reduction of antimony by sulfate-reducer enriched bio-cathode with hydrogen production in a microbial electrolysis cell
Graphical abstract
Introduction
With the expansion of industrialization and globalization, widespread wastewater containing heavy metals were released into the environment. Heavy metal contamination always shows serious environmental and human health issues. Therefore, it is very much needed and essential to process this highly toxic pollutant from the wastewater environments efficiently. Antimony (Sb) is one such highly dangerous heavy metal that is more prevalent in China (Ali et al., 2019; He et al., 2012). Sb and its compound are highly toxic pollutants and considered as hazardous heavy metal pollutants by the United States Environmental Protection Agency (USEPA) and European Union (EU). Even though the occurrence of Sb is a natural process in the earth's crust, intensive anthropogenic activities (mining or smelting) lead to an increased Sb contamination in the environment (Filella and He, 2020; He et al., 2012). China produces 88% of the world's total antimony, then Bolivia, Russia and Tajikistan, South Korea, USA, and France (Zeng et al., 2015; Zhou et al., 2019a). Pilot-scale mining and smelting have produced a massive amount of Sb contamination in the Xikuangshan (XKS) mine (Lengshuijiang, Hunan province, Southwest China) (Sun et al., 2016; Tang et al., 2019). The average Sb contamination in XKS mine surrounding agricultural soil, water, and plants is 235.8 mg/kg, 7.3 μg/L, and 54 mg/kg, respectively (He et al., 2012; Zhou et al., 2019b). The maximum allowed Sb level in drinking water is 5 μg/L (China) (Filella and He, 2020), 20 μg/L (World Health Organization) (WHO, 2003), and 2 μg/L (Japan) (Zheng et al., 2000). In many circumstances, chlorine is used as a disinfectant in water; if the antimony is exposed to chlorine-containing water, it will readily react with chlorine to form tri-chloride (SbCl3), which is very toxic for human health (Mantha et al., 2018; McCallum, 2005). The contamination level of Sb is rapidly increasing every year and may result in serious health threats to the local inhabitant in China (Chen et al., 2019; Gu et al., 2020).
In the past decades, research on antimony reduction by the chemical or biological method was increased rapidly because the toxicity of the Sb is increased in water, food, and soil, which leads to mutagenic, carcinogenic, and teratogenic risks (Barragan et al., 2020; Gu et al., 2020; Jin et al., 2020; Silva and Cesarino, 2020; Singkiburin et al., 2020; Y. Zhang et al., 2020). Sb has two main valence states in the environment (+3 and +5) (M. Li et al., 2020; Xi et al., 2020). Thus, the reduction process of Sb (V) to Sb (III) and subsequent insoluble form (Sb2S3) has been considered as an innovative remediation strategy in Sb contaminated sites (Wang et al., 2013). Developing a simple technology to achieve complete remediation of emerging contaminants is highly credited. Bio-reduction or bioremediation is a renowned favourable economic method to remediate the toxic heavy metals in the environment, in which microorganisms play an energetic role in the catalytic process (Medfu Tarekegn et al., 2020). Additionally, various advanced technology has been proposed for the remediation of Sb contamination like adsorption (Deng et al., 2017), membrane filtration (Mubarak et al., 2015; Seelajaroen et al., 2020), coagulation-flocculation-sedimentation (Mantha et al., 2018), chemical precipitation (Guo et al., 2018; Mubarak et al., 2015), ion exchange (Arnold et al., 2019) and electrochemical methods (Wang and Wang, 2019). Their high cost, complicated preparation process, inherent membrane fouling, excessive use of chemicals, and the possibility of secondary pollution confines their pervasive applications (Vareda et al., 2019).
Recently, an inexpensive bio-precipitation method for heavy metals reduction like Sb, Se, and As by sulfate-reducing bacteria (SRB) under anoxic conditions were proved to be efficient in removing the toxic contamination in the environment (Briones-Gallardo et al., 2016; Hockin and Gadd, 2003; Wang et al., 2013). SRB plays a vital role in the global carbon and sulfur cycle to remove a secondary hazardous contaminant called sulfate in the environment and produce biogenic dissolved sulfide (Biswas et al., 2014). This biogenic dissolved sulfide produced by SRB can react with the aqueous form of heavy metals and convert the contaminants into an insoluble form, which is an attractive way to remove the heavy metals from the environment (Xu and Chen, 2020). SRB has great potential ability to survive at a various range of pH and temperature, and have significant features like complete sulfate reduction, sulfide production, the competence of hydrogen evolution reaction, and bio-precipitation of heavy metals (Ayangbenro et al., 2018; Kushkevych et al., 2019a). Biogenic sulfide production by SRB is a natural process, and comparably it is very low in cost, and thus the biological precipitation of heavy metals by sulfide is easy and efficient. Since antimony (a chalcophile element) has a great affinity towards sulfur compounds to form the primary precipitate of Sb called stibnite (Sb2S3) under anoxic conditions. Therefore, SRB precipitation is considered a promising method for the complete reduction of Sb in the environment.
Conversely, Sulfate reduction and H2S production in Microbial fuel cell (MFC) for the generation of bioelectricity have gained more attention from many researchers (Abbas et al., 2018; Agostino and Rosenbaum, 2018; Blazquez et al., 2016; Coma et al., 2013; Isosaari and Sillanpää, 2016; Jabeen and Farooq, 2015). Furthermore, the attention of SRB has gained much more in terms of first value product (H2) production by Microbial electrolysis cell (MEC), since the sulfate reduction potential is closely conjugated with the hydrogen production rate with an applied voltage (Agostino and Rosenbaum, 2018; Lim et al., 2018). MEC technology is a type of bio-electrochemical system which involved in a wide range of applications on wastewater treatment with different elegant value-added end products (H2, CH4, and H2O2, etc.) (Jain and He, 2020; Seelajaroen et al., 2020; Sim et al., 2018). Consequently, H2 production through MEC using SRB have more advantage over the conventional H2 production technology in which it does not require a precious catalyst, need only less energy input, and the cost of H2 production is significantly less with sulfide concentration (Beegle and Borole, 2017; Martins and Pereira, 2013). To avoid the use of the expensive catalyst for the H2 production, a cheap carbon material containing bacterial population on its surface is termed as “bio-cathode,” was developed, which have a tremendous prospective catalytic role in the hydrogen evolution rate (Croese et al., 2011; Wang et al., 2017). In comparison, direct utilization of SRB in terms of sulfate reduction and sulfide production for heavy metals precipitation with H2 evolution in the bio-cathode MEC reactor will be a more robust bioremediation technology (Dominguez-Benetton et al., 2018). However, bio-precipitation of Sb driven by SRB with H2 production in bio-cathode MEC technology is mostly unknown.
The novelty of the present study is to reduce high strength sulfate contaminant with bio-precipitation of Sb (V) to Sb (III) through subsequent yield precipitate (Sb2S3) carried by sulfide (HS−) produced in the same bio-cathode MECs at an applied voltage. The objective of this research work as follows (i) to develop SRB bio-cathode MEC by reversing the polarity of the anode to cathode. (ii) to analyze the sulfate reduction potential and sulfide production in MEC reactor (ii) to investigate the effectiveness of Sb bio-reduction from Sb (V) to Sb (III) by biogenic sulfide. (iv) utilization of SRB on H2S production for bio-precipitation of Sb with concurrent hydrogen production. (v) Finally, bio-precipitation was analyzed by X-Ray Diffraction (XRD) and X-ray photon spectroscopy (XPS) to confirm the conversion of Sb (V) to the insoluble form of stibnite (Sb2S3). Moreover, this research work presents for the first time an elegant route for the successful bio-precipitation of hazardous heavy metals with a valuable product (H2) in the MEC reactor, which is the main advantage of SRB bio-cathode MECs.
Section snippets
Enrichment and optimization of SRB for Sb precipitation
Previously isolated two different types of active sulfate-reducing bacteria of strain BY7 (Yan et al., 2018a) and SR10 (Zhang et al., 2017) were used in this study to investigate the bio-reduction of Sb. These SRB strains of BY7 and SR10 were also available in Guangdong Microbial Culture Collection Center, with accession a number GDMCC1.1349 and GDMCC1.1031. To enrich the SRB for Sb treatment, BY7 and SR10 were repeatedly sub-cultured in serum bottles for five times in 100 mL of modified
Optimization of Sb (V) reduction by SRB
SRB strains of Enterococcus avium (BY7) and Citrobacter freundii (SR10) used in this study are non-traditional sulfate reducers isolated previously from the up-flow anaerobic sludge bed for treating acid mine drainage. Both BY7 and SR10 are rod-shaped flagellated bacteria, and the phylogenetic information of both SRB strains was depicted in Figs. S2 and S3. Both the strains have high efficient track of sulfate reduction with simultaneous heavy metal removal and precipitation like Cr, Ni, Pb,
Conclusion
An SRB rich bio-cathode MEC was developed successfully for the purpose of clean hydrogen production and Sb reduction with an applied voltage (0.8 V). SRB strains of BY7 and SR10 show an efficient way for the utilization of dissolved sulfide produced in the sulfate reduction reaction for the enhanced Sb reduction. The data obtained in this research work provides a proof of concept applied to reduce Sb contamination in the wastewater. Among the two SRB strains, Citrobacter freundii (SR10) is
CRediT authorship contribution statement
Samuel Raj Babu Arulmani: Conceptualization, Methodology, Writing – original draft, Writing – review & editing. Junxi Dai: Writing – review & editing, Validation, Data curation. Han Li: Data curation, Methodology. Zhenxin Chen: Writing – review & editing, Visualization. Hongguo Zhang: Supervision, Conceptualization, Validation, Writing – review & editing. Jia Yan: Conceptualization, Writing – review & editing. Tangfu Xiao: Formal analysis. Weimin Sun: Formal analysis.
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
The work was supported by the National Natural Science Foundation of China (nos. 51208122, 51778156, 51708142), Pearl River S&T Nova Program of Guangzhou (201806010191), Science and Technology Program of Guangzhou (No. 201707010256).
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