Elsevier

Science of The Total Environment

Volume 644, 10 December 2018, Pages 1152-1159
Science of The Total Environment

Oxygen exposure deprives antimonate-reducing capability of a methane fed biofilm

https://doi.org/10.1016/j.scitotenv.2018.07.047Get rights and content

Highlights

  • Bio-reduction of Sb(V) to Sb2O3 precipitates was achieved in a CH4-based membrane biofilm reactor (MBfR).

  • 8 mg/L of O2 in the influent irreversibly inhibited Sb(V) reduction.

  • 8 mg/L of O2 suppressed key biological metabolisms of the biofilm, but stimulated growth of methanotrophs.

Abstract

This work is aiming at achieving antimonate (Sb(V)) bio-reduction in a methane (CH4) based membrane biofilm reactor (MBfR), and elucidating the effect of oxygen (O2) on the performance of the biofilm. Scanning electron microscope (SEM), energy dispersive X-ray (EDS) and X-ray photoelectron spectroscopy (XPS) confirm Sb2O3 precipitates were the main product formed from Sb(V) reduction in the CH4-fed biofilm. Illumina sequencing shows Thermomonas may be responsible for Sb(V) reduction. Moreover, we found 8 mg/L of O2 in the influent irreversibly inhibited Sb(V) reduction. Metagenomic prediction by Reconstruction of Unobserved State (PICRUSt) shows that the biofilm lacked efficient defense system to the oxidative stress, leading to the great suppress of key biological metabolisms such as TCA cycle, glycolysis and DNA replication, as well as potential Sb(V) reductases, by O2. However, methanotrophs Methylomonas and Methylosinus were enriched in the biofilm with O2 intrusion, in accordance with the enhanced abundance of genes encoding aerobic CH4 oxidation. These insights evoke the theoretical guidance of microbial remediation using CH4 as the electron donor towards Sb(V) contamination, and will give us a strong reference with regard to wastewater disposal.

Introduction

Antimony (Sb) is associated with variety of industries like the production of semiconductor, tracer bullets, antifriction alloys, batteries, mordant, glass decolouriser, and flame-proof retardant of textiles and papers (Filella et al., 2002a). This heavy metal draws great attention due to its carcinogenicity, genotoxicity, and cardiovascular and dermal effects, which lead to great damage to human health (Sundar and Chakravarty, 2010). 6 μg/L is the maximum contaminant level (MCL) for Sb in drinking water set by U.S. EPA (2009).

Pentavalent antimonate (Sb(V)) and trivalent antimonite (Sb(III)) are the main valent state of Sb occurring in natural water, in the form of Sb(OH)6 and Sb(OH)3 (Sb2O3), respectively (Filella et al., 2002b). Although both of Sb(V) and Sb(III) are toxic, transferring Sb(V) to Sb(III) is a feasible method for Sb removal, as Sb(V) is highly soluble while Sb(III) easily hydrolyzes into Sb2O3 precipitates that can be removed by centrifugation or filtration (Lai et al., 2015; Xiao et al., 2013). Sb treatment technologies include adsorption by metallogels, calcined hydrotalcite, or nanomaterials, and electrochemical methods (Constantino et al., 2018; Lan et al., 2014; Luo et al., 2017; You et al., 2018). Compared with these physicochemical methods, biological transformation of Sb(V) to Sb(III) has aroused researchers' interest due to its high sustainability and environment friendly pattern.

Traditional Sb bio-remediation processes usually are involved in electron donors such as acetate and lactate (Abin and Hollibaugh, 2014; Kulp et al., 2014; Nguyen and Lee, 2014). Bio-reduction of oxidized contaminants using CH4 as electron donor and carbon source has many advantages compared with that using organics and hydrogen, since CH4 leaves less electron residues, has lower cost, being generated directly from anaerobic digestion (Alexeev et al., 2004; Luostarinen et al., 2009; Meyer et al., 2010; Modina et al., 2007). More importantly, the oxidation of CH4 is beneficial for alleviating global greenhouse effect, as CH4 has much high valuer of GWP (global warming potential) than that of carbon dioxide (CO2) (Hu et al., 2014).

In our previous research, we achieved chromate (CrO42−) and selenate (SeO42−) reduction in a CH4 based membrane biofilm reactor (MBfR), the concentration of surrounding O2 was very low (less than 0.2 mg/L of dissolved O2 (DO)) (Lai et al., 2016a, Lai et al., 2016b; Luo et al., 2015). O2 might have multiple effects on the CH4-fed biofilm. The et al. (2005) reported that the O2 availability has strong effect on CH4 oxidation, the rate of CH4 oxidation increased with increasing O2 concentration. However, intrusion of O2 into biofilm might cause oxygenic stress on the microbial cells: oxygen might be transformed into harmful superoxide and hydroxyl radicals such as superoxide anion radical (O2) and hydrogen peroxide (H2O2), and impose great damage to proteins, DNA, and lipids (Cabiscol et al., 2000). Luesken et al. (2012) reported that O2 exposure gave overall detrimental effects on anaerobic methane oxidizing bacteria Candidatus Methylomirabilis oxyfera. Besides, O2 is a common competitive electron acceptor with high redox potential, thus impairing microbial capability for respiration of other oxyanions. However, how does the O2 affect the performance of CH4 fed biofilm reactor and the biofilm components remained unclear.

Phylogenetic investigation of communities by reconstruction of unobserved state (PICRUSt) is a powerful bioinformatics tool that has been applied to predict metagenomic information for microorganism (Metcalf et al., 2016; Langille et al., 2013; Ward et al., 2017). Metcalf et al. (2016) successfully elucidated the key principles controlling metabolic function during decomposition of mouse and human corpses by using PICRUSt piplines. Ward et al. (2017) used PICRUSt to reveal seasonality in microbial metabolic pathways involving photosynthetic proteins, carbohydrate metabolism, and transporters, in marine ecosystems.

In this study, we tested the feasibility of Sb(V) reduction in a CH4 based MBfR when the influent concentration of O2 was 0.2 mg/L, and studied the effect of O2 on Sb(V) reduction. In order to understand the microbial mechanisms, we characterized the microbial communities by using illumine sequencing targeting bacterial 16S rRNA gene, and predicted metagenomic information by using PICRUSt piplines.

Section snippets

Reactor setup and operation

Detailed information about the CH4 based MBfR configuration has been given by Lai et al. (2016a). In brief, the MBfR was made up of two columns containing composite hollow fibers (280-μm OD and 180-μm ID, model MHF-200TL, Mitsubishi, Ltd., Japan). The total surface area of the fibers was 58 cm2, and the total volume of the MBfR was 65 mL. A peristaltic pump was used for internal recycle at 100 mL/min.

We inoculated the MBfR with 1 mL of culture that performed nitrate dependent micro-aerobic

Sb(V) reduction kinetics

Fig. 1A presents the influent and effluent Sb(V) concentrations of the CH4 based MBfR, while Fig. 1B showed the Sb(V) removal percentage. The comparison between maximum CH4 flux and the actual CH4 flux demonstrated that all stages have sufficient CH4 supply, as was shown in Table 1. In Stage 1, when the MBfR was fed with medium containing 4 mg/L of Sb(V) and 1.8 mg/L of DO, the removal percentage of Sb(V) attained to ~30%, with 150 mg/m2-day of Sb(V) removal flux. In Stage 2, when the influent

Conclusion

This work demonstrated Sb(V) bio-reduction in a CH4-based MBfR, and Sb2O3 precipitates were the final products. Thermomonas, an anaerobic denitrifier, might be the major genus performing Sb(V) reduction, while its abundance had positive correlation with Sb(V) flux. However, the introduction of 8 mg/L of O2 significantly impaired Sb(V)-reducing capability of the biofilm. Metagenomic prediction analysis suggest the biofilm suffered great oxidative stress, as the genes associated with key

Acknowledgments

Authors greatly thank the “National Key Technology R&D Program (2017ZX07206-002)”, the “National Natural Science Foundation of China (Grant No. 21577123)”, the “Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001)”, and the “Fundamental Research Funds for the Central Universities (2016QNA6007, 2017XZZX010-03)” for their financial support.

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