Characterization of the enhancement of zero valent iron on microbial azo reduction
© Fang et al.; licensee BioMed Central. 2015
Received: 12 August 2014
Accepted: 27 March 2015
Published: 10 April 2015
The microbial method for the treatment of azo dye is promising, but the reduction of azo dye is the rate-limiting step. Zero valent iron (Fe0) can enhance microbial azo reduction, but the interactions between microbes and Fe0 and the potential mechanisms of enhancement remain unclear. Here, Shewanella decolorationis S12, a typical azo-reducing bacterium, was used to characterize the enhancement of Fe0 on microbial decolorization.
The results indicated that anaerobic iron corrosion was a key inorganic chemical process for the enhancement of Fe0 on microbial azo reduction, in which OH−, H2, and Fe2+ were produced. Once Fe0 was added to the microbial azo reduction system, the proper pH for microbial azo reduction was maintained by OH−, and H2 served as the favored electron donor for azo respiration. Subsequently, the bacterial biomass yield and viability significantly increased. Following the corrosion of Fe0, nanometer-scale Fe precipitates were adsorbed onto cell surfaces and even accumulated inside cells as observed by transmission electron microscope energy dispersive spectroscopy (TEM-EDS).
A conceptual model for Fe0-assisted azo dye reduction by strain S12 was established to explain the interactions between microbes and Fe0 and the potential mechanisms of enhancement. This model indicates that the enhancement of microbial azo reduction in the presence of Fe0 is mainly due to the stimulation of microbial growth and activity by supplementation with elemental iron and H2 as an additional electron donor. This study has expanded our knowledge of the enhancement of microbial azo reduction by Fe0 and laid a foundation for the development of Fe0-microbial integrated azo dye wastewater treatment technology.
KeywordsAzo reduction Shewanella decolorationis S12 Zero valent iron (Fe0)
Azo dyes are widely used in the textiles, leather, plastics, cosmetics, and food industries, with a global annual production of more than 5,000 tons. Approximately 10% of azo products are discharged into the environment, resulting in a negative impact on the environment and human health because most azo dyes are carcinogenic, teratogenic, and highly persistent in the environment [1-3]. Conventional physicochemical methods for treating azo dyes have severe limitations, including incomplete removal, formation of hazardous products, and high operation costs, and biological techniques enable complete mineralization of the azo dye in a more environmentally friendly and cost-effective manner [4,5]. Azo dyes are not readily degraded by biological methods under aerobic conditions, and thus, they are normally decolorized by reductive cleavage of the azo bonds (−N = N-) under anaerobic conditions and then converted to aromatic amines, which are subsequently mineralized aerobically [6,7]. The decolorization process is typically rate-limiting, which hinders the biological treatment of azo dyes .
Zero valent iron (Fe0) can enhance anaerobic microbial azo reduction, but the exact mechanism of Fe0-assisted microbial reduction remains unclear [9-11]. Because azo dyes are decolorized by functional microorganisms, characterizing the Fe0-assisted decolorization of azo dyes using a pure decolorizing bacterium may provide some exact information about the reaction mechanism, and understanding how the microbes interacts with Fe0 will facilitate the elucidation of the mechanisms of enhancement and optimize the biodecolorization process.
Fe2+, OH−, and H2 are the products of the anaerobic corrosion process . The electrode potential of the redox couple Fe2+/Fe0 is −0.44 V, and hydrogen production from corrosion exhibits autocatalytic behavior, attaining a maximum rate of 1.9 mol kg−1 d−1 over 2 d of reaction in a study by Reardon et al. . Based on these knowledge, it is hypothesized that anaerobic Fe0 corrosion may be accelerated in the azo dye biodecolorizing system, then (i) the microenvironmental conditions are altered to produce more favorable redox/pH conditions for the growth of microbes; (ii) the additional electron donor (H2) from Fe0 corrosion facilitates a greater microbial biomass yield; and (iii) the activity of the azo-reducing bacteria is stimulated by the supplementary elemental iron, resulting in the acceleration of the azo bioreduction.
To test these hypotheses, S. decolorationis S12, an azo-reducing bacterium isolated from a textile wastewater treatment system [21,22], was used as a model organism to characterize the enhancement of microbial azo reduction by Fe0 in this study. Specifically, we investigated (i) the effect of Fe0 dosage on the decolorization rate, pH change, and H2 release to determine whether Fe0 affects azo reduction by strain S12 indirectly; (ii) the morphology of Fe solids outside and inside the cells to determine whether a direct interaction between microbes and Fe0 occurs in the decolorization process; and (iii) the effect of Fe0 addition on the ratio of live versus dead cells and protein contents to determine whether the addition of Fe0 influences the growth and survival ability of strain S12. This study provides new insights into our understanding of the interactions between Fe0 and microbial cells in the decolorization process and lays a foundation for further optimization of Fe0-microbial integrated processes for efficient azo dye treatment.
Chemicals, organism, media, and cultivation
Amaranth (Am), a typical water-soluble azo dye, was purchased from Sigma (St. Louis, MO, USA). S. decolorationis S12 is a rod-shaped, gram-positive facultative bacterium that was isolated from the activated sludge of a textile-printing wastewater treatment plant by Xu et al. .
Strain S12 was cultivated by transferring a single colony to a 100-mL conical flask containing 50 mL of Luria-Bertani medium (10 g/L peptone, 5 g/L yeast extract, 10 g/L NaCl), which was then incubated in a shaking incubator (160 rpm) at 30°C. The cells were harvested in the middle of exponential growth phase (approximately 8 h) by centrifugation, washed twice with phosphate buffer (0.1 M, pH 7.4), and re-suspended in the buffer prior to inoculation. The cells were inoculated into a defined medium (pH 7.0) containing Na2HPO4, 7.64 g/L; KH2PO4, 3.00 g/L; NH4Cl, 0.50 g/L; NaCl, 1.00 g/L; sodium lactate, 5.00 mM; yeast extract, 0.5 g/L; and amaranth, 1.0 mM. The initial cell density was approximately 107 CFU/ml (the protein mass was approximately 0.023 mg/mL). The cells were statically cultivated at 30°C in an anaerobic workstation (BugBox, Ruskinn Technologies). Standard anaerobic technique was used throughout the study for anaerobic cultivation as previously described . The medium was prepared by adding concentrated stock solutions containing various medium components in O2-free distilled water. The medium was then bubbled with N2 gas for 10 min to remove residual air from the head space. All gases used were passed through a 0.2-μm filter prior to use. All batch experiments were conducted in 100-mL serum bottles with a culture medium volume of 40 mL under anaerobic conditions. Three independent experiments with triplicate bacterial samples were performed in each experiment.
Micrometer-sized iron (Fe0) particles (mean size of 18.51 μm) were obtained from Tianjin Guangfu Technology and Development Co., Ltd., China, and were pretreated by rinsing with 1 M HCl for 3 min, followed by washing with distilled water for 1 min. Different dosages of Fe0 (0, 10, 20, 30, 40, 60 mM) were added to the defined medium (40 mL) to examine the effect of Fe0 dosage on the decolorization reaction. The cell-free abiotic control (no strain S12 cells) received 60 mM Fe0. For the other tests, the dosage of Fe0 particles was maintained at 60 mM. Before and after decolorization (a reaction period of approximately 30 h), the size (hydrodynamic diameter) of the particles was determined using dynamic light scattering in a laser particle size analyzer (Eyetech, Ankersmid, USA).
Growth and activity assays of microbial cells
Cells were grown in medium with and without 60 mM Fe0 for 12 h and then collected for cell yield and activity assays, including protein content and live/dead ratio. The protein content was determined by the Coomassie brilliant blue method  with slight modification. Briefly, NaOH solution (1 M, 40 mL) was added to the serum bottle containing the cell culture in 40 mL of medium, and the mixture was incubated in a water bath for 10 min at 95-99°C with gentle end-over-end inversion every 2 min. After centrifugation at 12,000 × g for 5 min, the supernatant was collected in a new centrifuge tube at room temperature and reacted with Bradford solution containing 0.01% (w/v) Coomassie brilliant blue G-250, 4.7% (w/v) ethanol, and 8.5% (w/v) phosphoric acid for 10 min prior to measuring the absorbance at 595 nm. Bovine serum albumin was used as a protein standard.
A LSM700 laser scanning confocal microscope (Zeiss, Braunschweig, German) was used to examine the activity of S. decolorationis S12 after a 12-h reaction. A rapid fluorescence staining method using the LIVE/DEAD BacLight™ Viability Kit (Molecular Probes Inc., Eugene, Oregon, USA) was applied to estimate both the viable and total counts of bacteria according to the manufacturer’s recommended protocol.
TEM and SEM analyses
Transmission electron microscopy (TEM) and scanning electron microscopy (SEM) with energy dispersive X-ray spectroscopy (EDS) were used to observe the structures of the bacterial cells and the iron precipitates. Bacterial cell samples were collected for TEM analysis after a 12-h incubation, and Fe0 samples for SEM analysis were collected after a 30-h incubation. The suspended bacterial cells and Fe0 samples were collected separately. The cell pellet was separated from the medium by centrifugation at 12,000 × g for 5 min, and the pellet (containing cells and Fe0) was washed twice with 0.1 M phosphate buffer before fixation in 3% glutaraldehyde for 5 h. Then, the pellet was washed twice with phosphate buffer and dehydrated in a gradient series of ethanol solutions from 30 to 100% by incubation at each ethanol concentration for 15 min. For TEM analysis, the sample was treated with acetone and embedded in epoxy resin. Thin sections (80–90 nm) were cut with a diamond knife mounted on a Leica EM UC6 ultramicrotome and collected on carbon-coated Cu grids. TEM observation was performed with a JEOL JEM-2010HR TEM at 200 kV or a Hitachi H-7650 TEM at 80 kV. For SEM observation, the sample was treated with tert-butanol and then freeze dried. After sputtering with gold, the sample was deposited on the Cu carrier and observed with either a Hitachi H-3000 N SEM or a FEI Quanta 400 F SEM. The EDS measurement was performed with an Oxford INCA EDX spectrometer coupled with a JEOL JEM-2010HR TEM or an FEI Quanta 400 F SEM.
Chemical analysis and calculation
The pH of the solution was measured using a digital multi-parameter 3430 meter (WTW, Germany). The Fe2+ concentration in the aqueous phase was measured using the HCl extraction ferrozine assay method as previously described . The H2 concentration in the medium after a 12-h reaction was examined by hydrogen microelectrodes (model H2-50, Unisense A/S, Denmark) polarized at +1000 mV.
where A is the initial absorbance, B is the absorbance after the reaction, C is the initial concentration of amaranth (1 mM), and t is the decolorization reaction time (12 h). All assays were performed in triplicate.
Statistical analysis was conducted with Office Excel 2010, Origin V8.0, and SPSS V17.0 (SPSS Inc. Chicago, IL, USA) software. Treatment P values < 0.05 were considered significant.
Results and discussion
Effects of Fe0 on azo dye decolorization by strain S12
To determine if the H2 evolved from Fe0 can serve as an electron donor for strain S12 during the decolorization process, the concentration of H2 in the experimental systems after 12-h reactions with different Fe0 dosages was determined. As shown in Figure 1b, the H2 concentration increased with Fe0 dosage in both the presence and absence of strain S12 (from 36 to 93 μmol L−1 and from 129 to 148 μmol L−1, respectively), indicating that H2 was generated from the anaerobic corrosion of Fe0. However, the H2 concentrations in the presence of strain S12 were significantly lower than those measured in the cell-free tests (P < 0.001), suggesting that the produced H2 was consumed as an electron donor by strain S12 during azo reduction. In addition, as shown in Figure 1b, the dosage of Fe0 was a rate-limiting parameter for azo reduction when the dosage of Fe0 was less than 40 mM, which could be due to the limited H2 supply for strain S12. However, when the dosage of Fe0 was greater than 40 mM, the supply of H2 became adequate, and the decolorization efficiency reached a steady state. This study thus confirmed the presence of a dosage threshold for Fe0 (40 mM) for strain S12 in azo reduction. Previous study of the effect of Fe0 dosage on hexavalent chromium and carbon tetrachloride removal also reported a dosage threshold for Fe0 due to the H2 supply .
Furthermore, we also measured the Fe2+ concentrations in the absence and presence of strain S12 cells in the presence of 60 mM Fe0 (no rate limitation of azo reduction was observed at this dosage, as described above) because Fe2+ is one of the products of anaerobic Fe0 corrosion. After a 30-h incubation, the Fe2+ concentration in the experiments with strain S12 was 13.0 ± 0.5 μmol L−1, which was significantly higher than that of the abiotic control (2.1 ± 0.1 μmol L−1) (P = 0.03), suggesting that strain S12 promoted the dissolution of Fe0 particles. The same phenomenon was also observed by De Windt et al.  for anoxic Fe0 corrosion coupled with nitrate reduction by S. oneidensis MR-1. The mechanism of Fe0 consumption remains unclear. There were two likely explanations: (i) the consumption of H2 released from the Fe0 surface by strain S12 allowed the reaction described in Equation (1) to occur and shift to the right, or (ii) strain S12 reacted with Fe0 directly (such as from the uptake of iron discussed below) and accelerated the transformation of iron. The data in this study indicate that both explanations are correct and complementary, but more work is needed to clarify the exact mechanism.
Shifts in the size distribution pattern of Fe0 particles during biodecolorization
Effects of Fe0 on cell morphology and viability
The TEM/EDS images demonstrated differences in cell morphology in the Fe0-supplemented culture (Figure 5d,e) and the control (Figure 5f). In the Fe0-supplemented culture, extracellular and/or intracellular fine-grained Fe precipitates or clusters formed outside and/or inside the cell membrane (with mean sizes of 80.52 ± 15.82 nm and 25.90 ± 6.53 nm, respectively) (Figure 5d,e). These results indicated direct interactions between Fe0 and strain S12, providing good evidences for microbial-driven biogeochemical cycling. These direct interactions promoted the transformation of iron as well as the removal of contaminants. First, for contaminant removal, Fe precipitates provided more Fe sources for the synthesis of enzymes and thus enhanced microbial activity. Elemental iron assimilated by strain S12 was an active ingredient for multiple dehydrogenases and hydrogenases (such as [Fe-S] cluster-containing lactate dehydrogenase and [Ni–Fe] and [Fe–Fe] catalytic site-containing hydrogenases), ensuring higher cell physiological and azoreductive activities [14,34,38]. Second, strain S12 cells, which were attached to the surface of Fe0, coupled the consumption of H2 (released from Fe0 corrosion) and the reduction of azo dye by azo respiration. For iron transformation, the process included several steps as follows: (i) Fe2+ released from Fe0 corrosion and reversibly adhered to the surface of Fe0 or strain S12 cells; (ii) Fe2+-containing precipitates formed (e.g., Fe(OH)2, Fe3(PO4)2, FeCO3) when anions presented, and (iii) the small size and high surface-to-volume ratio of fine-grained particles (Fe0-Fe2+ [solid]) enabled significant adsorption of Fe precipitates to the outer membrane of strain S12 cells and the intracellular uptake of Fe precipitates to the cytoplasm of strain S12 cells. Fe0 corrosion was accelerated because the concentration of Fe2+ [aqueous] was diluted by strain S12 through steps (i) and (iii), suggesting that strain S12 contributed to the transformation of iron, although a quantitative analysis could not be performed here. The biosorption of Fe precipitates has also been observed for other Shewanella spp.  and Dehalococcoides spp.  involved in Fe0-assisted bioremediation, revealing universal direct interactions between bacteria and minerals during containment removal .
Mechanisms of Fe0-assisted biodecolorization
The results of batch experiments of azo decolorization by combining the use of Fe0 and the azo-reducing bacterium S. decolorationis strain S12 expanded our knowledge of the enhancement of microbial azo reduction by Fe0. A conceptual model for Fe0-assisted microbial azo reduction was established based on the direct and indirect interactions between microbes and Fe0 after characterizing the changes in the morphology of the Fe0 particles, the physiological activities of the bacteria, and the physicochemical properties of the azo reduction system. This model will facilitate the development of azo dye remediation technology. However, to further elucidate the mechanisms underlying these processes, transcriptomic and proteomic analyses should be performed to track the dynamics and adaptive responses of strain S12 during Fe0-assisted azo reduction processes.
We thank Yinghua Cen for the suggestions during manuscript preparation. This research was supported by the National Basic Research Program of China (973 Program) (2012CB22307), the National Natural Science Foundation for Outstanding Young Scholars of China (51422803), the National Natural Science Foundation of China (21207019), Guangdong Provincial - Chinese Academy of Sciences Strategic Cooperation Projects (2013B091500081), the Natural Science Foundation of Guangdong, China (2014A030308019), and the Special Fund for Agro-scientific Research in the Public Interest (201503108).
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