Next Article in Journal
Water Level Prediction of Emergency Groundwater Source and Its Impact on the Surrounding Environment in Nantong City, China
Previous Article in Journal
Impact of Climate Change on Soil Erosion in the Lam Phra Phloeng Watershed
Article

Comparison of Different Anode Materials to Remove Microcystis aeruginosa Cells Using Electro-Coagulation–Flotation Process at Low Current Inputs

Department of Environmental Science and Technology, Graduate School of Science and Engineering, Saitama University, 255 Shimo-okubo, Sakura-ku, Saitama 338-8570, Japan
*
Authors to whom correspondence should be addressed.
Water 2020, 12(12), 3528; https://doi.org/10.3390/w12123528
Received: 22 October 2020 / Revised: 4 December 2020 / Accepted: 13 December 2020 / Published: 16 December 2020
(This article belongs to the Section Water and One Health)

Abstract

Cyanobacterial blooms are a threat to the drinking water supply owing to their potential toxicity. Microcystins which are the most widespread cyanotoxins, are mainly produced by Microcystis spp. In this study, we cultured Microcystis aeruginosa cells in BG-11 medium at 25 °C to investigate the efficiency of the electro-coagulation–flotation process to remove them. Different anode materials (Fe, Al, Cu, and Zn) along with a graphite cathode were compared separately in the 10–100 mA current range in a 0.025 M Na2SO4 electrolyte. Turbidity, optical density at 684 nm (OD684), OD730, Chl-a concentration, and DOC concentration were analyzed to clarify the mechanism by which M. aeruginosa cells are removed. The Al anode indicated the highest removal efficiencies in terms of turbidity (90%), OD684 and OD730 (98%), and Chl-a concentration (96%) within 30 min at 4.0 mA/cm2 current density and the lowest average electrode consumption of 0.120 ± 0.023 g/L. The energy consumption of the Al electrode was 0.80 Wh/L. From these results, we found that Al was the best among the anode materials evaluated to remove M. aeruginosa cells. However, further studies are required to optimize the Al anode in terms of pH, treatment time, electrode distance, and electrolyte concentration to enhance the removal of M. aeruginosa cells.
Keywords: cyanobacteria removal; Microcystis aeruginosa; electro-coagulation–flotation; anode material cyanobacteria removal; Microcystis aeruginosa; electro-coagulation–flotation; anode material

1. Introduction

Cyanobacterial blooms are one of the major problems worldwide and they can be harmful to the environment, animals, and human health. As a result of rapid oxygen consumption, hypoxic conditions develop, resulting in plant and animal die-off in water bodies [1]. These blooms are a threat to the drinking water supply owing to their potential toxicity and the release of taste and odor compounds such as geosmin and 2-methyl-isoborneol (2-MIB) [2,3]. Generally, cyanobacteria release a large amount of soluble algogenic organic matter (AOM) to the water such as extracellular organic matter (EOM), which is expelled to the water by living algal cells as a product of their metabolic activities, and intracellular organic matter (IOM), which is secreted upon the rupture of cells caused by endogenous or exogenous factors [4,5,6]. IOM is released as a result of cell lysis when cyanobacteria go through water treatment processes, such as ozonation or chlorination and it is a source of precursor materials for the formation of carcinogenic disinfection by-products (DBPs) combining with chlorine [3,7]. Cyanobacteria have been recognized for decades as a potential source of precursor materials for the formation of DBPs such as trihalomethane (THM) and haloacetic acid (HAA) [3]. The dominant AOMs such as hydrophilic polysaccharides and hydrophobic proteins are mainly responsible for the fouling of membrane filtration [4]. Therefore, it is important to remove cyanobacterial cells at the start of the water treatment chain.
Cyanotoxins produced by several species of cyanobacteria are another issue. The most widespread cyanotoxins are the peptide toxins called microcystins. There are at least 80 known microcystins, among which microcystin-LR is generally considered the most toxic. Microcystis spp. and Anabaena spp. are considered the major cyanotoxin-producing cyanobacteria [8,9]. Most of the drinking water guidelines are based on the World Health Organization’s provisional value of 1.0 μg/L microcystin-LR for drinking water [1]. Lake Taihu is the third largest freshwater lake in China, where eutrophication promotes Microcystis spp. blooms that impair drinking water supplies owing to strong odor, taste, and the presence of microcystin [10].
Cyanobacteria have been removed by conventional treatment techniques such as pre-oxidation by ozone or chlorine dioxide, chemical coagulation, sedimentation, flotation, and filtration using combined membrane technologies. However, there are many problems such as high cost, large amounts of sludge produced, huge energy consumption, and the complexity of treatment processes [11,12]. Recently, the electro-coagulation–flotation (ECF) process has been suggested to be a promising alternative option for cyanobacterial removal [13]. A series of reactions occur during the ECF process. Metal ions are generally released at the sacrificial anode by electrolytic oxidation. Simultaneously, hydrogen and oxygen gas microbubbles are generated at the cathode and anode, respectively. Pollutants combine with the released metal ions to form flocs, which are then removed through the lifting force of microbubbles or sedimentation [14].
The key reactions occurring in the ECF process when aluminum (Al) is used as the anode are shown in Equations (1)–(4) [13,15,16,17].
At the anode:
Al Al 3 + + 3 e
2 H 2 O O 2 + 4 H + + 4 e
At the cathode:
2 H 2 O + 2 e H 2 + 2 OH
In solution:
Al 3 + + 3 H 2 O Al ( OH ) 3 + 3 H +
The removal of cyanobacteria through the sedimentation process is challenging because they have a lower density than water owing to gas vacuoles in their cells for regulating the water content [15]. Therefore, the ECF process might be effective and low-cost for cyanobacterial removal.
Only a few studies have focused on the effect of the anode material, mainly Al and/or iron (Fe), on the removal of algae and cyanobacteria by the ECF process. In this research, we compared four anode materials, Fe, Al, copper (Cu), and zinc (Zn), to determine the effect of the anode material on the removal of Microcystis aeruginosa cells.

2. Materials and Methods

2.1. Preparation of Microcystis aeruginosa Cultures

To prepare new M. aeruginosa cultures, we obtained samples from a M. aeruginosa monoculture maintained in our laboratory. We used BG-11 medium prepared as described by Rippka et al. [18]. Table 1 shows the ingredients and quantities that were used to prepare the BG-11 medium.
We used twelve 500 mL Erlenmeyer flasks to culture M. aeruginosa. Before inoculation, flasks, rubber stoppers, and the BG-11 medium were sterilized at 121 °C and 0.12 MPa for 20 min in an autoclave (SP300, Yamato Scientific Co., Ltd., Tokyo, Japan) [19]. Each flask was filled with 250 mL of BG-11 medium and closed with a rubber stopper (SILICONE Sterile Stopper, C-40 joint size, AS ONE Corporation, Osaka, Japan) to maintain a proper aeration for their growth. We maintained the cultures in an incubator (LH-55RDS, NK Systems Limited, Tokyo, Japan) at 25 ± 1 °C temperature providing a 12:12 light and dark period and a 60 µmol m−2s−1 photon flux of photosynthetically active radiation [20,21,22]. The flasks with cultures were gently shaken about three times a day to ensure equal exposure of M. aeruginosa cells to the light.
Figure 1a,b show the appearance of M. aeruginosa cultures at the initial stage and after 14 days of growth, respectively. The initial average pH, turbidity, and optical densities at 684 nm and 730 nm (OD684, and OD730) of the culture were 7.40 ± 0.06, 6 ± 1 NTU, 0.0309 ± 0.0012, and 0.0322 ± 0.0018, respectively. Cultures showed an S-shaped growth curve and reached an exponential growth within four days. In the exponential phase of growth (14 days after inoculation), about 2.5 L volume of cultures was harvested and gently stirred to obtain a homogenous sample. Before starting the experiments, the pH and electrical conductivity (EC) of samples were adjusted using 0.1 M NaOH or 0.1 M HCl solution and Na2SO4, respectively. Table 2 shows the characteristics of M. aeruginosa suspensions prepared for the ECF treatment.

2.2. Experimental Setup and Electrode Materials

As shown in Figure 2, all the experiments were carried out at room temperature using 200 mL of M. aeruginosa suspension mixed at a speed of 200 rpm using a magnetic stirrer (PC-320, CORNING, Corning, NY, USA). The electrode distance was maintained at 2 cm for each experiment [13]. The effective areas of the anodes and cathode were 25 cm2 and 30 cm2, respectively. We compared the anode materials along with the graphite cathode separately in the 10 mA–100 mA current range using 0.025 M Na2SO4 electrolyte. The current density was in the range of 0.4–4 mA/cm2. The DC voltage was in the range from 1 to 3.8 V. DC power was supplied by a regulated DC digital power supply unit (PMC35-2A, KIKUSUI, Kanagawa, Japan). After conducting each set of experiments, the electrodes were washed with 0.01 M HCl, thoroughly washed with distilled water to remove residuals on the surface, and then weighed.
Anode materials and a graphite cathode were purchased from Ajax Scientifc Ltd., Scarborough, ON, Canada. Fe, Al, Cu, and Zn electrodes were selected for the study because these metals are less toxic for humans. All electrodes were rectangular in shape. The details of different anodes are shown in Table 3.

2.3. Analytical Methods

All chemicals used in the study were purchased from FUJIFILM Wako Pure Chemical Industries, Ltd., Osaka, Japan. All physicochemical analyses of water samples were carried out in accordance with standard methods for the examination of water and wastewater [23].
Samples for water quality analyses were collected from 2 cm below the surface using a pipette without disturbing the flocs. Turbidity was measured using a laboratory turbidity meter (2100N, HACH Company, Loveland, CO, USA) and pH was measured using a portable digital meter (Orion 3 star, Thermo Fisher Scientific Co., Ltd., Waltham, MA, USA). EC and total dissolved solids (TDS) were analyzed using a portable conductivity meter (AS710, AS ONE Corporation, Osaka, Japan).
Several studies demonstrated that algae show high absorbance at 684 nm and 730 nm. It was shown that there is a linear relationship between cell count and OD at 684 nm for M. aeruginosa (R2 > 0.99) [24,25]. A research carried out by Patel et al. [26] also showed a linear relationship between cell count and OD730 for five cyanobacteria species (R2 > 0.99). Therefore, in this study, ODs at 684 nm and 730 nm were analyzed using a UV-Vis spectrophotometer (UV-1280, Shimadzu, Kyoto, Japan). Dissolved organic carbon (DOC) concentration was measured for samples filtered through a 0.45 µm filter paper by a method based on the catalytic oxidation using a TOC analyzer (TOC-2300, Hiranuma Sangyo Co., Ltd., Ibaraki, Japan). Fluorescence microscopy images of M. aeruginosa cells were obtained before and after ECF treatment (BZ-X810, KEYENCE Corporation, Osaka, Japan).
The chlorophyll-a (Chl-a) concentration of water samples was measured as described by Zavřel et al. [27]. One milliliter each of sample was dispensed into separate Eppendorf safe-lock tubes and the tubes were centrifuged at 15,000× g for 7 min in a refrigerated microcentrifuge (TOMY MX-105, Tomy Seiko Co., Ltd., Tokyo, Japan). After discarding the supernatant, 1 mL of methanol was added and the samples were incubated at +4 °C for 20 min to extract pigments from the cells. The samples were again centrifuged at 15,000× g for 7 min and the absorbance of the supernatant was measured at wavelengths of 665 and 720 nm using a UV-Vis spectrophotometer (UV-1280, Shimadzu, Kyoto, Japan).
Chl-a concentration was determined using Equation (5).
Chlorophyll a ( µ g mL ) = 12.9447 × ( A 665 A 720 )
A665: absorbance at a wavelength of 665 nm
A720: absorbance at a wavelength of 720 nm
Energy consumption was calculated in Wh per L using the Equation (6) reported by Ozyonar et al. [16].
Energy   consumption   ( Wh L ) = V × I × t v
V: Voltage (volt)
I: Current (ampere)
t: Operation time (hours)
v: Volume of the treated solution (L)
The dissociation of ions from the anode follows the Faraday’s law. The theoretical electrode consumption was calculated in g per L using the Equation (7) given by Ozyonar et al. [16].
Electrode   consumption ( g / L ) = I × t × M w z × F × v
t: Operation time (seconds)
Mw: Molar mass of the anode material (g/mol)
z: Number of electrons involved in the reactions (Al, 3; Fe, 2; Cu, 2; Zn, 2)
F: Faraday’s constant (96,485 C/mol)
v: Volume of the treated solution (L).

2.4. Statistical Analyses

All experiments were carried out in triplicate. Statistical analyses were carried out using IBM SPSS Statistics 20.0 software. The removal efficiencies in terms of turbidity, OD684, OD730, Chl-a concentration, and DOC concentration achieved after the ECF treatment were compared among different anode materials by one-way ANOVA post-hoc Tukey HSD (Honestly significant difference) tests to identify the best anode material. All statistical analyses used a significance level of 5% (p ≤ 0.05).

3. Results

3.1. Comparison of Treated Water Characteristics

The applied current was as low as 10 mA at the start of each experiment and was gradually increased. There were no significant changes observed during the first 30 min of treatment of M. aeruginosa suspensions until the applied current reached 100 mA. Table 4 shows the results of treated water after the 30 min treatment and 30 min settling time at 100 mA applied current.
The initial pH was adjusted to 7.00 ± 0.01 before the start of each experiment. The highest and lowest average pHs were recorded for the Cu and Fe anodes: 11.46 ± 0.48 and 8.88 ± 0.34, respectively. The initial average EC and TDS were 3893.67 ± 4.73 µS/cm and 3002 ± 2.65 mg/L, respectively, after adding Na2SO4 electrolyte. The treatment carried out using the Al anode showed slight reductions in the average EC and TDS to 3776.67 ± 0.0058 µS/cm and 2890 ± 0.01 mg/L, respectively, but the other anode materials showed slightly higher values than initial values. The Al anode showed the optimal average treated water turbidity, OD684, OD730, and Chl-a concentration: 15.33 ± 1.53 NTU, 0.0168 ± 0.0047, 0.0164 ± 0.0047, and 0.0063 ± 0.0001 µg/mL, respectively. However, the lowest average DOC concentration of 21.85 ± 2.85 mg/L was obtained when the Cu anode was used.
Figure 3 shows the appearance of M. aeruginosa suspensions before and after treatment using different anode materials. As shown in Figure 3c, the ECF treatment carried out using the Al anode showed the clearest water after the treatment. In the case of using the Fe anode (b), the suspension in the beaker turned yellowish-green at the beginning of the ECF treatment and then changed to yellowish-brown with the time. The suspension treated using the Cu anode (d) appeared a light blue at the final stage of the treatment.
Figure 4 shows the turbidity variation at the initial stage, after 30 min treatment, and after 30 min settling. The initial average turbidity was 166.67 ± 2.08 NTU. During the 30 min treatment time, the Al and Cu anodes markedly reduced the turbidity up to 38.34 ± 3.51 NTU and 53.34 ± 4.16 NTU, respectively. After the 30 min settling time, water clarity further improved for both Al and Cu electrodes up to 15.34 ± 1.53 NTU and 37.67 ± 4.04 NTU, respectively.
As shown in Figure 5, the ECF treatment carried out using the Al anode showed the clearest water after the treatment and settling process. In contrast, treatments using Fe, Cu and Zn anodes produced yellowish-brown, light blue, and white cloudy effluents, respectively. Final average EC values were higher than initial EC value in suspensions treated with Fe, Cu and Zn. However, the final EC was 3776.67 ± 0.0058 µS/cm for the suspension treated with Al anode. It was slightly lower than initial EC value.

3.2. Comparison of Removal Efficiency with Respect to Turbidity, OD, Chl-a Concentration, and DOC Concentration among Anode Materials

Figure 6 shows the average removal efficiency as a function of turbidity, OD684, OD730, Chl-a concentration, and DOC concentration for different anode materials. The Al anode showed the highest significant removal efficiency of 91% in terms of turbidity (F(3,8) = 254.210, p < 0.001) and the highest significant OD684 and OD730 reduction of 98% (F(3,8) = 751.252, p < 0.001 and F(3,8) = 1091, p < 0.001, respectively). The Al anode also showed the highest significant Chl-a removal efficiency of 98% (F(3,8) = 62.353, p < 0.001). However, the highest significant DOC removal efficiency of 70.41% was observed for the Cu anode (F(3,8) = 33.751, p < 0.001). The DOC removal efficiency was not significant during the treatment using the Fe, Al, and Zn anodes.

3.3. Comparison of Electrode Consumption and Electrical Energy Consumption among Anode Materials

Figure 7 shows the actual and theoretical anode consumptions of different anode materials. The same applied current of 100 mA was used for each experiment using different anodes. The Al and Cu anodes showed the lowest and highest average anode consumptions of 0.120 ± 0.023 and 0.351 ± 0.170 g/L, respectively. However, the theoretical anode consumptions were lower than the actual anode consumptions for Al and Cu anode materials (Figure 7).
Figure 8 shows the electrical energy consumptions of different anode materials. The Zn and Cu anodes showed the lowest and highest electrical energy consumptions of 0.675 and 0.925 Wh/L, respectively. The electrical energy consumptions of the Al and Fe anodes were 0.750 and 0.800 Wh/L, respectively.

3.4. Appearance of M. aeruginosa Cells before and after ECF Treatment Process

Figure 9a,b show the appearance of M. aeruginosa cells before and after treatment. Figure 9a shows well-matured M. aeruginosa cells after 14 days of incubation with diameters of up to 10 µm. However, cell diameters varied from 5–10 µm. Figure 9b shows the appearance of M. aeruginosa cells after ECF treatment. The cells agglomerated and a sheath formed around them.

4. Discussion

In this study, we conducted comparative experiments using Fe, Al, Cu, and Zn as anode materials under the same operational condition for M. aeruginosa removal. We used indirect measurements such as turbidity, OD, Chl-a concentration, and DOC concentration to measure M. aeruginosa concentrations and AOM at before and after treatment. The Al anode showed the highest removal efficiency in terms of all these parameters except DOC concentration (Figure 6). In this investigation, we started with a current input as low as 10 mA and gradually increased it. There were no any significant changes observed during the first 30 min of treatment in M. aeruginosa suspensions until the applied current reached 100 mA. The Al anode showed the highest removal efficiency of 98% for M. aeruginosa at 100 mA current and 4 mA/cm2 current density for 30 min treatment. A quite similar result was reported by Gao et al. [15]. They demonstrated that 25 min treatment was adequate for 100% M. aeruginosa removal at 5 mA/cm2 current density. According to Faraday’s law, the amount of metal ions released from the anode to the solution increases with increasing current input and electrolysis time. These metal ions incorporated with OH ions promotes the aggregation of cyanobacterial cells to form flocs [28]. Moreover, the density and size of microbubbles increases and decreases with increasing current input, respectively, which promotes flotation [29].
The initial pH is one of the most critical factors affecting the ECF process [17]. In this study, we maintained the initial pH at 7.00 ± 0.01. However, the pH increased to alkaline levels after ECF treatment for all the anode materials investigated. This may be due to OH ions generated at the cathode as a result of metal ion oxidation at the anode. A similar result was reported by Bleeke et al. [30] for the treatment of Scenedesmus acuminatus using the same anode materials. The Cu anode showed the highest final average pH of 11.46 ± 0.48 (Table 4). Tumsri et al. [31] also mentioned that the pH increased markedly during electrolysis when using the Cu anode.
According to Gao et al. [15], at the neutral pH of 7, the amount of aluminum hydroxide is much higher than that of other metal hydroxides. Moreover, a higher current efficiency can be generated by Al electrodes than by Fe, Cu, or Zn electrodes. Owing to hydrolysis reactions, Al ions are hydrolyzed and produce various types of Al species such as monomeric species (e.g., Al(OH)2+ and Al(OH)2+) and polymeric species (e.g., Al13(OH)345+ and Al13O4(OH)247+). These cationic products react with OH ions, which transform into amorphous Al(OH)3 according to complex precipitation kinetics [17,31].
In this study, the Zn anode showed the lowest electrical consumption (0.675 Wh/L); however, its removal efficiency was lower. The electrical consumption of the Al anode was 0.80 Wh/L (Figure 8) with respect to the lowest anode consumption of 0.12 ± 0.023 g/L (Figure 7) at pH 7 for 30 min treatment with 98% M. aeruginosa removal efficiency. Gao et al. [15] reported the electrical consumptions of the Al electrode at different pHs for the complete removal of M. aeruginosa by 75 min treatment. The electrical consumption gradually increased with increasing pH: 0.30 Wh/L from pH 4 to 7, 0.53 Wh/L from pH 7 to 9, and 0.60 Wh/L at the initial pH of 10. An experiment carried out for Chlorella vulgaris showed that the algae removal efficiency was 96–98.1% for 30 min electrolysis at 6–7 initial pH and 2 mA/cm2 current density. The energy consumption was 0.91 Wh/L [31]. At a lower pH, low amount of Al ions is required to remove algal cells owing to charge neutralization. However, when pH is increased, sweep flocculation dominates and a higher amount of Al ions are required to achieve a similar removal efficiency [15]. It is considered that a high efficiency of cyanobacteria/algae removal could be achieved at a low energy consumption under neutral and acidic pH conditions [13,32].
In this study, we used EC and color as indirect measurements especially to identify the excess metal ion concentrations in treated suspensions. Final EC values were higher than initial EC value in suspensions treated with Fe, Cu and Zn respective to dissolution of excess metal ions. However, the final average EC of suspension treated with Al anode was slightly lower than initial EC value. It is realized that there were lower excess aluminum ions in treated suspension. In the case of the Fe anode, the suspensions in the beaker turned yellowish-green at the beginning of the ECF process and gradually changed to yellowish-brown (Figure 3 and Figure 5). These color changes happen owing to the presence of Fe2+ and Fe3+ ions [15]. Higher turbidity and ODs of treated water were obtained when using the Fe anode than when using the Al and Cu anodes (Table 4). Fe at 0.3 mg/L causes turbidity, changes color, and stains laundry and plumbing fixtures. However, there is usually no conspicuous taste of water at concentrations <0.3 mg/L [33]. The suspensions treated using the Cu anode appeared light blue at the final stage of treatment (Figure 3 and Figure 5). It could be due to Cu2+ species produced during electrolytic dissolution [31]. Cu produces a bitter taste and changes the color of water when its concentration is higher than 5 mg/L, and stains laundry fixtures at higher than 1 mg/L [33]. The Zn anode showed the lowest removal efficiency in terms of turbidity as the final solutions appeared white and cloudy as a result of Zn(OH)2 formation (Figure 3 and Figure 5). Generally, high pHs enhance the generation of these metal hydroxides [34].
We maintained a 30 min settling time for each experiment and measured the turbidity. During the 30 min settling time, the turbidity decreased for all anodes as a result of the sedimentation of flocs (Figure 4). However, the reduction in turbidity during the settling time was very small for the Zn and Fe anodes owing to Zn(OH)2 precipitation, and of the suspension turned yellowish-brown owing to the oxidation of Fe2+ to Fe3+ in the presence of oxygen [34,35].
Formation of sludge is a crucial problem as it contains metal ions. Aluminum in sludge can be recovered for subsequent reusing purposes using acidic and alkaline extraction methods. Sulfuric acid (H2SO4) is used as the acidification agent in the recovering of the aluminum. This mechanism can also be used to extract other metal ions. Recovery of aluminum in water treatment plant could be a significant approach towards sustainability development [36]. As well as ECF method can use to recover these algae towards the producing of biofuels as a sustainable green energy source.
Regarding the morphology of M. aeruginosa cells before and after ECF treatment, we observed that the cells appeared normal with diameters in the range of 5–10 µm; however, these cells tended to aggregate (Figure 9) after treatment owing to coagulants and the formation of extracellular polysaccharide mucilage around them [37]. In addition, Bakheet et al. [22] reported that more than 30 min electrolysis can disrupt the cell walls and membranes of M. aeruginosa cells, resulting in the release of IOM to the medium [4,5,6]. It is important to remove IOM and EOM precursor materials because they contribute to the formation of carcinogenic DBPs combining with chlorine [3,7]. According to Zhao et al. [38], the EOM and IOM concentrations ranged from very low concentrations to about 100 mg/L depending on the cyanobacterial species. In this research, the initial DOC concentration was 73.85 ± 1.52 mg/L in M. aeruginosa suspensions. The Cu anode showed the highest DOC removal efficiency of 70%, whereas the other anodes did not display a significant removal of DOC (Figure 6). However, the Cu anode exhibited the highest anode consumption and energy consumption (Figure 7 and Figure 8). According to Zhou et al. [39] Cu ions can interact with proteins, intercellular nucleic acids, enzymes, and metabolites microbial cells after uptake by them. In case of Al anode, we obtained only a 40% DOC removal efficiency. Guo et al. [40] reported a 38.7% DOC removal efficiency from the IOM of M. aeruginosa at 5 mg/L alum dosage. The charge neutralization process involves the elimination of AOM during coagulation owing to the occurrence of extremely negative charges on AOM [6]. However, it is important to carry out these ECF experiments considering the maximum M. aeruginosa removal while preventing the release of IOM via cell lysis [41].

5. Conclusions

Al was the best anode material among the materials evaluated (i.e., Fe, Cu, and Zn) to remove M. aeruginosa cells at 4.0 mA/cm2 current density for a 30 min treatment period and a 30 min settling time with the lowest anode consumption. Even though the Cu anode showed the highest DOC removal efficiency, its consumption was high. ECF method with Al anode showed to be a highly effective and rapid method for the removal of M. aeruginosa cells. However, further studies are recommended to optimize the Al anode in terms of pH, treatment time, electrode distance, and electrolyte concentration to obtain the maximum removal of M. aeruginosa cells. Moreover, the residual aluminum ion concentration, the effect of halide ions on anode dissolution, usage of dimensionally stable anodes could be recommended as important studies for the application purposes.

Author Contributions

Conceptualization, T.A.O.K.M. and T.F.; methodology, T.A.O.K.M. and T.F.; investigation, T.A.O.K.M.; data analysis, T.A.O.K.M.; writing—original draft preparation, T.A.O.K.M.; writing—review and editing, T.F.; visualization, T.F.; supervision, T.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Research Center for Sustainable Development in East Asia, Saitama University (SU-RCSDEA), V3060SR3, and scholarship donation, KF1T253364 (SU).

Acknowledgments

We are indebted to Senavirathna, M.D.H. Jayasanka (SU) for his cooperation with the incubation of M. aeruginosa cells.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Environmental Protection Agency. Cyanobacteria and Cyanotoxins: Information for Drinking Water Systems; United States Environmental Protection Agency EPA-810F11001; Office of Water: Washington, DC, USA, 2014; pp. 1–11.
  2. Vu, H.P.; Nguyen, L.N.; Zdarta, J.; Nga, T.T.V.; Nghiem, L.D. Blue-Green Algae in Surface Water: Problems and Opportunities. Curr. Pollut. Rep. 2020, 6, 105–122. [Google Scholar] [CrossRef]
  3. Wert, E.C.; Rosario-Ortiz, F.L. Intracellular Organic Matter from Cyanobacteria as a Precursor for Carbonaceous and Nitrogenous Disinfection Byproducts. Environ. Sci. Technol. 2013, 47, 6332–6340. [Google Scholar] [CrossRef] [PubMed]
  4. Zhang, X.; Fan, L.; Roddick, F.A. Influence of the characteristics of soluble algal organic matter released from Microcystis aeruginosa on the fouling of a ceramic microfiltration membrane. J. Memb. Sci. 2013, 425–426, 23–29. [Google Scholar] [CrossRef]
  5. Ghernaout, D. Electrocoagulation Process for Microalgal Biotechnology—A Review. Djamel Ghernaout Electrocoagul. Process Microalgal Biotechnol. Rev. Appl. Eng. 2019, 3, 85–94. [Google Scholar] [CrossRef]
  6. Coral, L.A.; Zamyadi, A.; Barbeau, B.; Bassetti, F.J.; Lapolli, F.R.; Prévost, M. Oxidation of Microcystis aeruginosa and Anabaena flos-aquae by ozone: Impacts on cell integrity and chlorination by-product formation. Water Res. 2013, 47, 2983–2994. [Google Scholar] [CrossRef] [PubMed]
  7. Fang, J.; Yang, X.; Ma, J.; Shang, C.; Zhao, Q. Characterization of algal organic matter and formation of DBPs from chlor(am)ination. Water Res. 2010, 44, 5897–5906. [Google Scholar] [CrossRef]
  8. Li, J.; Li, R.; Li, J. Current research scenario for microcystins biodegradation—A review on fundamental knowledge, application prospects and challenges. Sci. Total Environ. 2017, 595, 615–632. [Google Scholar] [CrossRef]
  9. Pham, T.L.; Utsumi, M. An overview of the accumulation of microcystins in aquatic ecosystems. J. Environ. Manag. 2018, 213, 520–529. [Google Scholar] [CrossRef]
  10. Sakai, H.; Hao, A.; Iseri, Y.; Wang, S.; Kuba, T.; Zhang, Z.; Katayama, H. Occurrence and Distribution of Microcystins in Lake Taihu, China. Sci. World J. 2013, 2013, 1–7. [Google Scholar] [CrossRef]
  11. Dong, Y.; Qu, Y.; Li, C.; Han, X.; Ambuchi, J.J.; Liu, J.; Yu, Y.; Feng, Y. Simultaneous algae-polluted water treatment and electricity generation using a biocathode-coupled electrocoagulation cell (bio-ECC). J. Hazard. Mater. 2017, 340, 104–112. [Google Scholar] [CrossRef]
  12. Xu, Y.; Yang, J.; Ou, M.; Wang, Y.; Jia, J. Study of Microcystis aeruginosa inhibition by electrochemical method. Biochem. Eng. J. 2007, 36, 215–220. [Google Scholar] [CrossRef]
  13. An, J.; Li, N.; Wang, S.; Liao, C.; Zhou, L.; Li, T.; Wang, X.; Feng, Y. A novel electro-coagulation-Fenton for energy efficient cyanobacteria and cyanotoxins removal without chemical addition. J. Hazard. Mater. 2019, 365, 650–658. [Google Scholar] [CrossRef] [PubMed]
  14. Mollah, M.; Morkovsky, P.; Gomes, J.; Kesmez, M.; Parga, J.; Cocke, D. Fundamentals, present and future perspectives of electrocoagulation. J. Hazard. Mater. 2004, 114, 199–210. [Google Scholar] [CrossRef] [PubMed]
  15. Gao, S.; Yang, J.; Tian, J.; Ma, F.; Tu, G.; Du, M. Electro-coagulation-flotation process for algae removal. J. Hazard. Mater. 2010, 177, 336–343. [Google Scholar] [CrossRef] [PubMed]
  16. Ozyonar, F.; Karagozoglu, B. Introduction. Polish J. Environ. Stud. 2011, 20, 173–179. [Google Scholar]
  17. Mouedhen, G.; Feki, M.; Wery, M.D.P.; Ayedi, H.F. Behavior of aluminum electrodes in electrocoagulation process. J. Hazard. Mater. 2008, 150, 124–135. [Google Scholar] [CrossRef]
  18. Stanier, R.Y.; Deruelles, J.; Rippka, R.; Herdman, M.; Waterbury, J.B. Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology 1979, 111, 1–61. [Google Scholar] [CrossRef]
  19. Shirai, M.; Matumaru, K.; Ohotake, A.; Takamura, Y.; Aida, T.; Nakano, M. Development of a Solid Medium for Growth and Isolation of Axenic Microcystis Strains (Cyanobacteria). Appl. Environ. Microbiol. 1989, 55, 2569–2571. [Google Scholar] [CrossRef]
  20. Islam, M.A.; Beardall, J. Growth and Photosynthetic Characteristics of Toxic and Non-Toxic Strains of the Cyanobacteria Microcystis aeruginosa and Anabaena circinalis in Relation to Light. Microorganisms 2017, 5, 45. [Google Scholar] [CrossRef]
  21. Yuan, R.; Li, Y.; Li, J.; Ji, S.; Wang, S.; Kong, F. The allelopathic effects of aqueous extracts from Spartina alterniflora on controlling the Microcystis aeruginosa blooms. Sci. Total Environ. 2020, 712, 136332. [Google Scholar] [CrossRef]
  22. Bakheet, B.; Islam, M.A.; Beardall, J.; Zhang, X.; McCarthy, D. Effective electrochemical inactivation of Microcystis aeruginosa and degradation of microcystins via a novel solid polymer electrolyte sandwich. Chem. Eng. J. 2018, 350, 616–626. [Google Scholar] [CrossRef]
  23. AWWA-American Water Works Association. Standard Methods for the Examination of Water and Wastewater; American Public Health Association: Washington, DC, USA, 1995. [Google Scholar]
  24. Rajasekhar, P.; Fan, L.; Nguyen, T.; Roddick, F.A. Impact of sonication at 20kHz on Microcystis aeruginosa, Anabaena circinalis and Chlorella sp. Water Res. 2012, 46, 1473–1481. [Google Scholar] [CrossRef] [PubMed]
  25. Zhang, G.; Zhang, P.; Wang, B.; Liu, H. Ultrasonic frequency effects on the removal of Microcystis aeruginosa. Ultrason. Sonochem. 2006, 13, 446–450. [Google Scholar] [CrossRef] [PubMed]
  26. Patel, V.K.; Sundaram, S.; Patel, A.K.; Kalra, A. Characterization of Seven Species of Cyanobacteria for High-Quality Biomass Production. Arab. J. Sci. Eng. 2018, 43, 109–121. [Google Scholar] [CrossRef]
  27. Zavřel, T.; Červený, J.; Sinetova, M.A. Measurement of Chlorophyll. Bio-Protocol 2015, 5, e1467. [Google Scholar] [CrossRef]
  28. Zhu, B.; Clifford, D.A.; Chellam, S. Comparison of electrocoagulation and chemical coagulation pretreatment for enhanced virus removal using microfiltration membranes. Water Res. 2005, 39, 3098–3108. [Google Scholar] [CrossRef] [PubMed]
  29. Holt, P.K.; Barton, G.W.; Wark, M.; Mitchell, C.A. A quantitative comparison between chemical dosing and electrocoagulation. Colloids Surfaces A Physicochem. Eng. Asp. 2002, 211, 233–248. [Google Scholar] [CrossRef]
  30. Bleeke, F.; Quante, G.; Winckelmann, D.; Klöck, G. Effect of voltage and electrode material on electroflocculation of Scenedesmus acuminatus. Bioresour. Bioprocess. 2015, 2, 36. [Google Scholar] [CrossRef]
  31. Tumsri, K.; Chavalparit, O. Optimizing Electrocoagulation-electroflotation Process for Algae Removal. In 2nd International Conference on Environmenta l Science and Technology IPCBEE; IACSIT Press: Singapore, 2011; Volume 6, pp. 452–456. [Google Scholar]
  32. Gonzalez-Torres, A.; Putnam, J.; Jefferson, B.; Stuetz, R.M.; Henderson, R.K. Examination of the physical properties of Microcystis aeruginosa flocs produced on coagulation with metal salts. Water Res. 2014, 60, 197–209. [Google Scholar] [CrossRef]
  33. WHO. Guideline for Drinking-Water Quality; Geneva WHO Press: Geneva, Switzerland, 2008; Volume 1, pp. 335–336. [Google Scholar]
  34. Safwat, S.M. Treatment of real printing wastewater using electrocoagulation process with titanium and zinc electrodes. J. Water Process Eng. 2020, 34, 101137. [Google Scholar] [CrossRef]
  35. Barışçı, S.; Turkay, O. Domestic greywater treatment by electrocoagulation using hybrid electrode combinations. J. Water Process Eng. 2016, 10, 56–66. [Google Scholar] [CrossRef]
  36. Hassan Basri, M.H.; Mohammad Don, N.N.; Kasmuri, N.; Hamzah, N.; Alias, S.; Azizan, F.A. Aluminium recovery from water treatment sludge under different dosage of sulphuric acid. J. Phys. Conf. Ser. 2019, 1349, 012005. [Google Scholar] [CrossRef]
  37. Chen, M.; Tian, L.-L.; Ren, C.-Y.; Xu, C.-Y.; Wang, Y.-Y.; Li, L. Extracellular polysaccharide synthesis in a bloom-forming strain of Microcystis aeruginosa: Implications for colonization and buoyancy. Sci. Rep. 2019, 9, 1251. [Google Scholar] [CrossRef] [PubMed]
  38. Zhao, Z. Effects of Drinking Water Treatment Processes on Removal of Algal Matter and Subsequent Water Quality. Ph.D. Thesis, The University of Western Ontario, London, ON, Canada, 2020. [Google Scholar]
  39. Zhou, J.; Wang, T.; Xie, X. Rationally designed tubular coaxial-electrode copper ionization cells (CECICs) harnessing non-uniform electric field for efficient water disinfection. Environ. Int. 2019, 128, 30–36. [Google Scholar] [CrossRef] [PubMed]
  40. Guo, T.; Yang, Y.; Liu, R.; Li, X. Enhanced removal of intracellular organic matters (IOM) from Microcystic aeruginosa by aluminum coagulation. Sep. Purif. Technol. 2017, 189, 279–287. [Google Scholar] [CrossRef]
  41. Zhao, Z.; Sun, W.; Ray, M.B.; Ray, A.K.; Huang, T.; Chen, J. Optimization and modeling of coagulation-flocculation to remove algae and organic matter from surface water by response surface methodology. Front. Environ. Sci. Eng. 2019, 13, 75. [Google Scholar] [CrossRef]
Figure 1. M. aeruginosa cultures. (a) Initial stage (after inoculation) and (b) after 14 days.
Figure 1. M. aeruginosa cultures. (a) Initial stage (after inoculation) and (b) after 14 days.
Water 12 03528 g001
Figure 2. ECF experimental setup for M. aeruginosa treatment. (a) Schematic experimental setup (scale 1:10, dimensions are presented in mm). (b) Actual experimental setup. The experiments were conducted in 200 mL glass beakers. The electrodes were connected to a DC power supply (PMC35-2A, KIKUSUI, Kanagawa, Japan) and M. aeruginosa suspensions were stirred at 200 rpm using a magnetic stirrer (PC-320, CORNING, Corning, NY, USA).
Figure 2. ECF experimental setup for M. aeruginosa treatment. (a) Schematic experimental setup (scale 1:10, dimensions are presented in mm). (b) Actual experimental setup. The experiments were conducted in 200 mL glass beakers. The electrodes were connected to a DC power supply (PMC35-2A, KIKUSUI, Kanagawa, Japan) and M. aeruginosa suspensions were stirred at 200 rpm using a magnetic stirrer (PC-320, CORNING, Corning, NY, USA).
Water 12 03528 g002
Figure 3. Appearance of suspensions before and immediately after treatment. (a) M. aeruginosa suspension before treatment. Suspensions after treatment using (b) Fe anode, (c) Al anode, (d) Cu anode, and (e) Zn anode.
Figure 3. Appearance of suspensions before and immediately after treatment. (a) M. aeruginosa suspension before treatment. Suspensions after treatment using (b) Fe anode, (c) Al anode, (d) Cu anode, and (e) Zn anode.
Water 12 03528 g003
Figure 4. Variation of average turbidity of M. aeruginosa suspensions treated using different anode materials at different treatment stages. Error bars represent the standard deviation (n = 3).
Figure 4. Variation of average turbidity of M. aeruginosa suspensions treated using different anode materials at different treatment stages. Error bars represent the standard deviation (n = 3).
Water 12 03528 g004
Figure 5. Appearance of suspensions before treatment and after 30 min settling time. (a) M. aeruginosa suspension before treatment. Suspensions after settling after treatment using (b) Fe anode, (c) Al anode, (d) Cu anode, and (e) Zn anode.
Figure 5. Appearance of suspensions before treatment and after 30 min settling time. (a) M. aeruginosa suspension before treatment. Suspensions after settling after treatment using (b) Fe anode, (c) Al anode, (d) Cu anode, and (e) Zn anode.
Water 12 03528 g005
Figure 6. Removal efficiency as a function of turbidity, optical density, Chl-a concentration, and dissolved organic carbon concentration for different anode materials. Error bars represent the standard deviation (n = 3). Different superscripts in bars for each parameter indicate a significant difference at 0.05 significant level for different anodes.
Figure 6. Removal efficiency as a function of turbidity, optical density, Chl-a concentration, and dissolved organic carbon concentration for different anode materials. Error bars represent the standard deviation (n = 3). Different superscripts in bars for each parameter indicate a significant difference at 0.05 significant level for different anodes.
Water 12 03528 g006
Figure 7. Actual and theoretical anode consumption of different anode materials. Error bars represent the standard deviation (n = 3).
Figure 7. Actual and theoretical anode consumption of different anode materials. Error bars represent the standard deviation (n = 3).
Water 12 03528 g007
Figure 8. Electrical energy consumptions of different anode materials.
Figure 8. Electrical energy consumptions of different anode materials.
Water 12 03528 g008
Figure 9. M. aeruginosa cells. (a) before and (b) after treatment using Al electrode. The scale bar is 10 µm (captured using a BZ-X810 fluorescence microscope at 44.4× magnification).
Figure 9. M. aeruginosa cells. (a) before and (b) after treatment using Al electrode. The scale bar is 10 µm (captured using a BZ-X810 fluorescence microscope at 44.4× magnification).
Water 12 03528 g009
Table 1. Composition of BG-11 medium [18].
Table 1. Composition of BG-11 medium [18].
IngredientNaNO3K2HPO4·3H2OMgSO4·7H2OCaCl2·2H2OCitric AcidFerric Ammonium CitrateEDTA Na2CO3Trace Metal Mix *
Quantity in 1 L of deionized water1.5 g0.04 g0.075 g0.036 g0.006 g0.006 g0.001 g0.02 g1 mL
* Trace metal mix contains (g/L): H3BO3, 2.86 g; MnCl2·4H2O, 1.81 g; ZnSO4·7H2O, 0.222 g; Na2MoO4·2H2O, 0.390 g; CuSO4·5H2O, 0.079 g; Co(NO3)2·6H2O, 0.0494 g.
Table 2. Characteristics of M. aeruginosa suspensions prepared for electro-coagulation–flotation treatment (n = 3).
Table 2. Characteristics of M. aeruginosa suspensions prepared for electro-coagulation–flotation treatment (n = 3).
ParameterpHTemp, °CEC, µS/cmTDS, mg/LTurbidity, NTUOD684OD730DOC, mg/LChl.-a, µg/mL
Average (S.D.)7.00 (0.01)25 (1)3893.67 (4.73)3002 (2.65)166.67 (2.08)0.9129 (0.0004)0.8520 (0.0002)73.85 (1.52)0.157 (0.013)
Table 3. Details of different electrodes used for ECF process.
Table 3. Details of different electrodes used for ECF process.
ElectrodeOxidation Potential (E0), VArea (W × L), cm2Breadth, mmWeight, g
Fe0.4465 (25 × 127)0.514.6
Al1.6665 (25 × 127)0.54.3
Cu−0.5265 (25 × 127)0.513.9
Zn0.7665 (25 × 127)0.514.3
Graphite-83.5 (135 × 25)5.025.1
Table 4. Characteristics of M. aeruginosa suspensions treated using different anode materials (n = 3).
Table 4. Characteristics of M. aeruginosa suspensions treated using different anode materials (n = 3).
ElectrodepHEC, µS/cmTDS, mg/LTurbidity, NTUOD684OD730DOC, mg/LChl.-a, µg/mL
Fe8.88 (0.34)4283.34 (0.0058)3266.67 (0.0116)69.00 (3.61)0.3945 (0.0171)0.3578 (0.0113)45.06 (2.54)0.0514 (0.0018)
Al9.77 (0.32)3776.67 (0.0058)2890 (0.01)15.33 (1.53)0.0168 (0.0047) 0.0164 (0.0047)44.39 (3.84)0.0063 (0.0001)
Cu11.46 (0.48)3913.34 (0.0153)3013.34 (0.0153)37.67 (4.04)0.0601 (0.0077)0.0554 (0.0056)21.85 (2.85)0.0208 (0.0011)
Zn10.75 (0.36)4250 (0.01)3243.34 (0.0153)115 (6.56)0.2160 (0.0098)0.1915 (0.0090)43.52 (2.57)0.0452 (0.0023)
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Back to TopTop