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DOI: 10.1039/D0EW00634C (Paper) Environ. Sci.: Water Res. Technol., 2020, 6, 3262-3275

Emerging investigator series: quaternary treatment with algae-assisted oxidation for antibiotics removal and refractory organics degradation in livestock wastewater effluent†

Waris Khan a, Joo-Youn Nam b, Seokjong Byun c, Sungpyo Kim d, Changseok Han *ef and Hyun-Chul Kim *g
aDepartment of Civil and Environmental Engineering, Sejong University, Seoul 05006, Republic of Korea
bJeju Global Research Center, Korea Institute of Energy Research, Jeju-do 63357, Republic of Korea
cDepartment of Research and Development, Jeollanamdo Environmental Industries Promotion Institute, Jeollanam-do 59205, Republic of Korea
dDepartment of Environmental Engineering, College of Science and Technology, Korea University, Sejong 30019, Republic of Korea
eDepartment of Environmental Engineering, College of Engineering, INHA University, Incheon 22212, Republic of Korea. E-mail: hanck@inha.ac.kr; Tel: +82 32 8607505
fProgram in Environmental and Polymer Engineering, Graduate School of INHA University, Incheon 22212, Republic of Korea
gResearch Institute for Advanced Industrial Technology, College of Science and Technology, Korea University, Sejong 30019, Republic of Korea. E-mail: animaplus@hanmail.net; Tel: +82 10 73731517

Received 6th July 2020 , Accepted 5th November 2020

First published on 6th November 2020

Abstract

In this study, we investigated the combination of algal treatment and subsequent oxidation to improve the antibiotics removal and refractory organics degradation in livestock wastewater effluent. We also proposed a better combination of oxidation processes for robust treatment of recalcitrant wastewater, mainly focusing on the removal of antibiotics. Stand-alone processes of O3, O3/H2O2, ultraviolet C (UVC), and UVC/H2O2 as well as their combined effects were evaluated as a downstream oxidation process. Prior to those oxidation processes, the effluent was treated with microalgae under continuous light illumination, which turned it into alkaline wastewater (pH > 10). The algal treatment was feasible not only to directly remove antibiotics resistant to a specific oxidation method, but also to improve the degradation of antibiotics and effluent organic matter in the alkaline wastewater upon subsequent oxidation. The alkaline wastewater was more favorable for the removal of antibiotics (especially for clopidol) with UVC treatment (UVC and UVC/H2O2). The algal treatment promoted ozonation to some extent for the degradation of florfenicol in the effluent. The removal of antibiotics by ozonation decreased with added H2O2, whereas the UVC performance was improved by adding H2O2. For ozonation followed by UVC treatment, the ozonation dominated the degradation of selected antibiotics.


Water impact

Since a remarkable amount of veterinary antibiotics has been detected even in public water sources, more reliable treatment of livestock wastewater beyond complying with typical discharge goals is increasingly demanded. We propose here an algae-integrated treatment strategy to successfully remove antibiotic residues. This provides further insight into the contributions and roles of microalgae in advanced oxidation of refractory wastewaters.

1. Introduction

Over the past decades, antibiotics have gained much attention as environmental pollutants because their residues are frequently found in surface water bodies and pose a potential risk to public health and aquatic environments even at vestigial concentrations.1–3 Previous studies reported that these trace organic chemicals chronically affected the ecosystem and aquatic species and led to an explosion of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs).4–8 ARB and AGRs are emerging at alarming rates, and the World Health Organization announced that they are major threats to human life in this century.9,10 More than half of all antibiotics around the world are used for animal husbandry, and veterinary antibiotic residues have been frequently observed in aquatic environments, including groundwater, surface water, and terrestrial matrices.11–14 Wide varieties of veterinary antibiotics worldwide are used in concentrated animal feeding operations (CAFOs) to treat infectious diseases and as nutritional supplements in livestock feed. After use, a significant amount of antibiotics as parent compounds and their metabolites are excreted in the urine and feces, since they are not very well adsorbed by the animals' intestines.15 Thus, these compounds are frequently detected in the effluents from livestock manure and CAFOs wastewater treatment facilities,16,17 indicating that conventional technologies for livestock wastewater treatment cannot decompose them effectively.18–20 Because the main purpose of conventional livestock manure treatment is to remove suspended solids, carbonaceous organics, and inorganic nutrients in order to comply with discharge goals, high levels of various antibiotics and the associated ARB and AGRs cannot be effectively eliminated and eventually enter the environment. Considering inter-related water resources, antibiotics-laden surface water can be a source of drinking water supplies; thereby, treatment technologies with high reliability should be applied for robust removal of antibiotic residues in livestock wastewater before it is discharged into the receiving water bodies.21–24

Ozonation is credited as a promising candidate for treating livestock wastewater and is increasingly combined with other techniques. For instance, O3 and ultraviolet C (UVC) can be coupled with H2O2 or other chemicals (e.g., persulfate) to greatly improve the performance of oxidation for the degradation of micropollutants in water and wastewater. Both ozonation and UVC irradiation are well established and operated in full-scale drinking water and water reuse applications.25 A wide variety of advanced oxidation processes (AOPs) have been investigated for removing the emerging pollutants of concern in different types of wastewaters.25–29 The feasibility of AOPs depends on the generation of OH radicals and on the reactivity of target compounds.30 The reactions can be drastically affected by wastewater characteristics, such as pH, organic matter, and alkalinity. In general, degradation rates of organic compounds tend to increase with higher pH in the aqueous phase, as a result of increased generation of OH radicals.28,31–33 Therefore, the treatment of alkaline wastewater with AOPs could be a better option to effectively remove antibiotics remaining after secondary or tertiary treatment of livestock wastewater. Unfortunately, the pH adjustment (pH > 10) of wastewater using caustic chemicals is cost-ineffective and thus unfeasible. In our previous studies, we found that the growth of Scenedesmus quadricauda in reverse osmosis (RO) concentrate significantly increased the pH, effectively reduced alkalinity,34 and removed inorganic nutrients from a wide range of wastewaters.35,36 We also reported the ability of S. quadricauda to remove pharmaceutical residues from RO concentrate in our prior work.37 Microalgae can effectively eliminate several types of micropollutants by means of different mechanisms such as intracellular and extracellular biodegradation, bioaccumulation, and bio-sorption.38,39 To date, some investigations have confirmed the efficiency of algae-mediated removal of emerging pollutants in different types of wastewaters.40–42

The objective of this study was to investigate the effects of algal treatment and subsequent oxidation on the removal of selected antibiotics and organic residues in tertiary livestock wastewater effluent. We evaluated stand-alone processes of O3, O3/H2O2, UVC, and UVC/H2O2 as well as their combined effects as a downstream oxidation process. In our latest work, we demonstrated that H2O2 could be generated on-site through the oxygen reduction reaction during the bioelectrochemical degradation of carbonaceous organic matter.43 Based on this previous observation, the on-site generation of H2O2 was supposed in this study and was integrated with the downstream oxidation processes. As shown in Fig. 1, organic-rich anaerobic digestate could be partially used as a feedstock in the bioelectrochemical system for the on-site generation of H2O2 that can be further used as a mediator for downstream AOPs (O3/H2O2 and UVC/H2O2). In this study, feasible oxidation processes were applied for treatment of tertiary effluent, and the contribution of algal pretreatment to the oxidation processes was also addressed with emphasis on antibiotics removal and refractory organics degradation. A microalga S. quadricauda was employed to increase the pH of wastewater via photosynthesis prior to various oxidation processes. Scenedesmus is a dominant genus of algae commonly found in wastewater ponds.44 To the best of our knowledge, no one has yet reported that microalgae can be used for alkalization of wastewater to improve the performance of AOPs.


image file: d0ew00634c-f1.tif
Fig. 1 Conceptual schematics for quaternary treatment of livestock wastewater using a hybrid system combining (i) bioelectrochemical treatment for on-site H2O2 production, (ii) multi-purpose algal treatment, and (iii) O3 and UVC for advanced oxidation of antibiotics with H2O2 produced on-site. The on-site H2O2 production with bioelectrochemical treatment using anaerobic digestate is out of the scope of this research.

2. Materials and methods

2.1. Livestock wastewater effluent

In this study, the tertiary effluent was collected from a local livestock wastewater treatment plant that uses sequential aerobic biological treatment, chemical floatation, and biofiltration for treating farm-generated animal manure. The wastewater sample was collected in sterile plastic containers and transferred to the laboratory to add selected antibiotics. Twenty antibiotics were selected based on their occurrence in livestock wastewater and were supplied by Sigma-Aldrich (St. Louis, MO, USA). Stock solutions of the 20 antibiotics (i.e., amoxicillin, ampicillin, ceftiofur, chlortetracycline, clopidol, enrofloxacin, erythromycin, florfenicol, lincomycin, oxytetracycline, penicillin-G, penicillin-V, sulfadiazine, sulfamethazine, sulfamethoxazole, sulfathiazole, tetracycline, tiamulin, trimethoprim, and tylosin) were individually prepared in HPLC-grade methanol using each of the antibiotics. A diluted mixture was used as a working solution and was spiked into the livestock wastewater sample in order to achieve a final concentration of 20 μg L−1 for each antibiotic. The starting concentration of antibiotics varied widely, and this is more likely due to varying extents of decay during wastewater storage since the recoveries appeared to be fairly consistent for all the antibiotics (see ESI† Table S2). The eventual concentration of total antibiotics ranged between 203 and 253 μg L−1. The characteristics of livestock wastewater effluent are summarized in Table 1. The sample was designated as raw wastewater and stored in a refrigerator at 4 °C in the dark until use in batch experiments. Unless specified otherwise, all experiments addressed in this study were carried out at room temperature.
Table 1 Characteristics of livestock wastewater effluent used in this study
Item Value
a Spiked intentionally.
pH 7.1–8.2
Conductivity (mS cm−1) 0.78–2.24
DOC (mg L−1) 69–86
COD (mg L−1) 262–285
UV254 (cm−1) 0.33–0.35
SUVA (L mg−1 m−1) 0.39–0.51
Color (mg Pt–Co per L) 21–25
TP (mg L−1) 0.04–0.06
TN (mg L−1) 5–16
Alkalinity (mg CaCO3 per L) 25–29
Total antibioticsa (μg L−1) 203–253

2.2. Batch treatment of livestock wastewater effluent

2.2.1. Algal treatment. The raw wastewater sample was divided into two aliquots, one of which was used for algal treatment with S. quadricauda. The stock culture of the S. quadricauda strain (AG 10003) was prepared as described in our prior work.37 The algal biomass in the exponential growth phase was collected via centrifugation (1620g, 10 min), washed with mineral bottled water, and inoculated at an optical density (OD) of 0.4 cm−1 (680 nm) into flasks containing 800 mL of raw wastewater. The flasks were incubated without aeration at 25 °C while shaking at 130 rpm for 12 h. The incubation was conducted twice in duplicate under continuous illumination with fluorescent lamps. The incoming light intensity to the flasks was 150 μmol photons m−2 s−1, which was measured using an MQ-500 quantum meter (Apogee Instruments, Inc., USA). The supernatant was collected from the flasks at the end of the test, filtered with 1.2 μm glass-fiber microfilters (Whatman, Grade GF/C), and mixed uniformly in a single container. The algal-treated wastewater (pH 10.2) was characterized as described in section 2.3 and stored in a refrigerator at 4 °C pending further oxidation treatments.
2.2.2. UVC treatment. The UVC treatment of raw and algal-treated wastewaters was carried out at 254 nm using a collimated beam apparatus with a 20 W low-pressure monochromatic mercury lamp (UVP XX-20S, Analytik Jena Co., Germany). The apparatus and method of UVC treatment have been reported in detail in our prior work.43 Briefly, the batch experiments were conducted in an open crystalline Petri dish containing 40 mL of water samples. The Petri factor (0.863), reflection factor (0.975), and water factors (0.786–0.868 depending on the UV absorbance of the wastewater samples) were applied to correct the UVC intensity, which was measured at the same height as the water level in the Petri dish using a calibrated UVX radiometer (Analytik Jena Co., Germany). The UVC treatment was performed in duplicate at doses of approximately 0, 500, 1000, and 2000 mJ cm−2, which was calculated using the average intensity of 0.404–0.446 mW cm−2 and exposure time.45

We carried out separate UVC treatments to investigate the effects of H2O2 addition on the degradation of antibiotics upon UVC irradiation. Commercially available H2O2 was added to raw and algal-treated wastewaters in a final concentration of 0.5 mM and the UVC irradiation was performed in duplicate as described above. The concentration of H2O2 remaining after the UVC irradiation was measured using the vanadate method.46 If needed, H2O2 remaining in the samples was quenched using bovine liver catalase for further characterizations described in section 2.3.

2.2.3. Ozonation. Ozonation of raw and algal-treated wastewaters was carried out with an O3 generator (Lab-I Ozone Tech Co. Ltd., Korea) using >99.9% O2 and continued for up to 10 min. Tests were performed twice in a glass cylindrical reactor containing 900 mL of wastewater samples. The gaseous ozone exhausted from the reactor was detected and quantified by measuring the absorption of electromagnetic radiation at a wavelength of 254 nm using an ozone analyzer (Model H1, IN USA Inc.). O3 was injected at a rate of 11.4 mg min−1 through a gas diffuser placed at the bottom of the reactor. O3 doses normalized by the dissolved organic carbon (DOC) of the wastewater samples were reported. For some experiments, commercially available H2O2 was added into raw and algal-treated wastewaters in final concentrations of 0.5 and 1.0 mM and subsequent ozonation was performed as described above, in order to investigate the effects of the H2O2 addition on the degradation of antibiotics upon ozonation. After ozonation under the given conditions, residual H2O2 was measured and then quenched as described in the above section prior to the analyses of the water samples.

Separate ozonation was conducted in duplicate to evaluate the pre-ozonation combined with UVC and UVC/H2O2, mainly focusing on the degradation of antibiotics in raw and algal-treated wastewaters. The ozonation was carried out as described above; aliquots were further subjected to UVC treatment (UVC and UVC/H2O2) performed as described in section 2.2.2.

2.3. Analytical methods

The water samples were manually filtered with 0.45 μm microfilters prior to measuring the water quality parameters. Each measurement was carried out at least twice, and the average and standard deviation values were reported. Dichromate, persulfate digestion, and acid persulfate digestion methods were employed to measure the chemical oxygen demand (COD), total nitrogen (TN), and total phosphorus (TP) in the water samples using a DR/5000 spectrophotometer. An identical spectrophotometer was also used to measure the chromaticity, UV254, and OD680. The DOC was determined (TOC-V CPN, Shimadzu, Japan) to obtain the specific UV absorbance (SUVA) value, which is calculated from the UV254 divided by the DOC of the water sample. The pH and conductivity were also measured using a pH meter (Orion Star A215, Thermo Scientific). The alkalinity was measured by titrating 100 mL of liquid sample with diluted sulfuric acid to pH 4.5. The fluorescence spectra were obtained using a Shimadzu RF-5301PC fluorescence spectrometer with a 150 W xenon lamp source. Three-dimensional spectra were obtained by repeatedly measuring the emission spectra within a range of 280–600 nm, with excitation wavelengths from 220 to 400 nm at 10 nm intervals in the excitation domain. The spectra were then concatenated into an excitation–emission matrix. The analytical conditions were reported in detail elsewhere.36

The selected antibiotics were extracted (see ESI† Fig. S1) and analyzed using an Agilent 1200 high-performance liquid chromatograph. The quantification of antibiotics was performed by internal standard calibration using amoxicillin-d4, florfenicol-d3, and sulfamethoxazole-d4. The chromatographic separation was carried out on a Zorbax Eclipse Plus C18 column (2.1 × 150 mm, 3.5 μm particle size) with mobile phase A (0.1% formic acid and 10 mM ammonium formate in water) and mobile phase B (acetonitrile). The elution rate was set at 0.35 mL min−1, and the injection volume of samples was 3 μL. Mass spectrometry detection was performed on an Agilent 6460 triple-quadrupole mass spectrometer equipped with a dual jet stream electrospray ionization source. Quantitative and qualitative analysis for the selected antibiotics were performed by multiple reaction monitoring (MRM). The MRM precursor and product ion pairs were selected at the highest peak intensities with different fragment and collision energies (see ESI† Table S1). Analytical performance was assessed in terms of the limit of detection (LOD), limit of quantification (LOQ), relative recoveries, relative standard deviation (RSD) of recoveries, and correlation coefficients (R2) of calibration curves (see ESI Table† S2). Based on the chromatographic response, the LOD and LOQ for each analyte were determined at signal-to-noise ratio (S/N) of 3 and 10, respectively. The linear regression analysis was performed by plotting the peak area versus the analyte concentration and showed linear responses (R2 ≥ 0.99) to the calibration curves for all detected analytes. Recovery experiments were conducted by spiking tertiary effluent with standard solutions. The average and RSD of relative recoveries during extraction were calculated from triplicate spiking experiments. Spiked recoveries were obtained in the range of 78–127% for the selected antibiotics, with the exception of erythromycin (149 ± 6%). The matrix profiles can be affected by advanced oxidation, and thus a limitation of this study was that the relative recoveries of antibiotics were not evaluated in treated wastewaters.

3. Results and discussion

3.1. Removal of antibiotics by microalgae in livestock wastewater effluent

The algal treatment of livestock wastewater effluent not only increased the pH of wastewater as discussed later, but also removed 29% of total antibiotics for the first 12 h cultivation of S. quadricauda in the light without supplemented CO2 (see Fig. 2). Among the twenty antibiotics examined in this study, nine were removed at over 75% (ceftiofur, penicillin-V, penicillin-G, tetracycline, tiamulin, erythromycin, chlortetracycline, tylosin, and oxytetracycline), eight decreased in concentration but by less than 10% (florfenicol, lincomycin, sulfamethazine, sulfamethoxazole, clopidol, trimethoprim, sulfathiazole, and sulfadiazine), and enrofloxacin was not reduced.
image file: d0ew00634c-f2.tif
Fig. 2 The levels of selected antibiotics in raw nominally neutral and algal-treated alkaline livestock wastewaters. Twenty antibiotics were spiked in the tertiary effluent (which was collected twice on two different days (a) 1st and (b) 2nd from a livestock wastewater treatment plant), and the mixture was designated as raw wastewater. That sample was divided into two aliquots, and algal treatment was conducted using one of those for which S. quadricauda was cultivated in the light for 12 h. The antibiotics are displayed in decreasing order of their removal (c).

The algal treatment almost completely removed ceftiofur (>99%), penicillin-V (>98%), penicillin-G (>98%), and tetracycline (>96%). Amoxicillin and ampicillin are also antibiotics of the penicillin class like penicillin-V and penicillin-G, but they were not detected even in the raw wastewater without added microalgae, likely due to varying extents of decay during wastewater storage. An effective removal was also observed for tiamulin (88%), erythromycin (85%), chlortetracycline (84%), tylosin (79%), and oxytetracycline (77%). The high removal of macrolide antibiotics (erythromycin and tylosin) using microalgae was consistent with previous observations.38,42 The significant removal (p < 0.05) of tetracycline antibiotics (chlortetracycline, tetracycline, and oxytetracycline) also coincided with results reported in previous studies47–49 and could be attributed to photo-degradation, hydrolysis, and bio-sorption during the algal treatment. Zhao et al. (2013)50 reported that the photolytic degradation of oxytetracycline was accelerated with increasing pH even under visible light due to a red shift of the absorption spectrum at high pH. In contrast to the macrolide and tetracycline antibiotics, none of sulfonamide antibiotics (sulfathiazole, sulfamethoxazole, sulfamethazine, sulfadiazine, and trimethoprim) was removed by more than 5%. The tetracycline antibiotics are amphoteric and unstable under strong alkaline and acidic conditions. In this study, the removal of antibiotics was independent of their hydrophobicity during the algal treatment. Sulfamethoxazole and trimethoprim are hydrophilic chemicals like tetracycline, but their removal was much lower than that of tetracycline. Some studies showed a 14–20% reduction of sulfamethoxazole, mostly because of photolysis for a long incubation time.47,49 Similarly, trimethoprim was highly resistant to biodegradation by algae.40 The removal could also differ with algal species, water matrix, initial antibiotics concentration, photolysis, hydrolysis, and operational parameters (e.g., temperature, retention time, and light intensity). This study showed the feasibility of using microalgae to remove certain chemicals during refractory wastewater treatment, although there is little information in the literature about algae-mediated removal of ceftiofur, penicillin-V, or penicillin-G.

3.2. The effects of algal pretreatment on the removal of antibiotics with UV and UV/H2O2

Phototrophs use CO2 and simultaneously release hydroxide ions (OH−) in aqueous medium.51,52 The pH of the livestock wastewater effluent increased from 7.1 to 10.4 for the first 12 h cultivation of S. quadricauda in the light without aeration (see ESI† Fig. S2). We investigated the pH effects on the degradation of selected antibiotics upon various oxidation treatments of the effluent with two different pH values (i.e., raw nominally-neutral and algal-treated alkaline). The UVC removed the selected antibiotics better for algal-treated wastewater (see Fig. 3b). The removal of total antibiotics increased from 51% to 72% as the UVC dose increased (500 to 2000 mJ cm−2), and further increased up to 81% with added H2O2. The highest removal difference between raw neutral and algal-treated alkaline wastewaters for the examined antibiotics was recorded for clopidol (see Fig. 4a). Alkaline UVC treatment achieved >95% removal of clopidol regardless of H2O2 addition, which was much greater than that achieved by neutral UVC treatment (71–74%). Unlike clopidol, enrofloxacin, sulfadiazine, sulfamethoxazole, and sulfathiazole showed a pH-independent removal tendency in both UVC and UVC/H2O2 treatments (see ESI† Fig. S3).
image file: d0ew00634c-f3.tif
Fig. 3 Treatment of raw neutral (a) and algal-treated alkaline (b) livestock wastewater using two different methods (UVC vs. UVC/H2O2). For UVC/H2O2, H2O2 was added to raw and algal-treated wastewater in a final concentration of 0.5 mM just before UVC irradiation (0, 500, 1000, and 2000 mJ cm−2). The percent removals in panel (b) include the removal (27%) achieved by algal-treatment prior to UVC-based treatment of livestock wastewater.

image file: d0ew00634c-f4.tif
Fig. 4 Treatment of livestock wastewater using two different methods (UVC vs. UVC/H2O2) and the effects of algal pretreatment on the removal of clopidol (a), sulfamethazine (b), lincomycin (c), and trimethoprim (d). For UVC/H2O2, H2O2 was added to raw and algal-treated wastewater in a final concentration of 0.5 mM just before UVC irradiation (0, 500, 1000, and 2000 mJ cm−2). For UVC-based treatment of algal-treated wastewater, the percent removals of the selected antibiotics include the removal achieved by algal-treatment.

Fig. 3 also shows that the extent of antibiotics removal was proportional to UVC dose (up to 2000 mJ cm2) applied to the wastewater effluent. When using an identical dose of UVC, the addition of 0.5 mM H2O2 to alkaline wastewater resulted in synergistic effects on the removal of some antibiotics (e.g., lincomycin, sulfamethazine, and trimethoprim). For example, the removal of sulfamethazine ranged from 75 to 79% with a UVC dose of 2000 mJ cm2 regardless of pH values examined (see Fig. 4b). This increased up to 88% when UVC was applied to alkaline wastewater with added 0.5 mM H2O2, but did not increase for neutral UVC/H2O2 treatment. Likewise, the removal of lincomycin (see Fig. 4c) and trimethoprim (see Fig. 4d) was much greater when UVC/H2O2 was applied to alkaline wastewater. These results were consistent with the measurements of H2O2 consumed during UVC treatment. The consumption of H2O2 was higher in alkaline UVC treatment than in neutral UVC treatment (see Fig. 5), suggesting a higher photolytic generation of OH radicals. This result was attributed to a partial dissociation of H2O2 (pKa ≈ 11.6) into hydroperoxide ions (HO2−) at alkaline pH conditions. Some investigators have previously reported similar results.28,31,53,54 In the UVC/H2O2 process, HO2− has about 10 times the UV molar absorptivity at 254 nm that H2O2 has (17.9–19.6 L mol−1 cm−1).30 Therefore, UVC/H2O2 could be more effective at higher pH, especially if the background wastewater matrix absorbs a lot of UVC light.


image file: d0ew00634c-f5.tif
Fig. 5 The H2O2 consumption and the pH change from UVC irradiation (0, 500, 1000, and 2000 mJ cm−2) of raw and algal-treated livestock wastewater with added 0.5 mM H2O2.

Ceftiofur, penicillin-V, and tylosin were easily degraded when raw wastewater was treated with either UVC or UVC/H2O2 (see ESI† Fig. S4), and most of them could also be removed by algal treatment, as discussed in section 3.1. Regarding the necessity of pretreatment with microalgae, it is worthwhile noting that some chemicals (e.g., chlortetracycline, erythromycin, oxytetracycline, penicillin-G, tetracycline, and tiamulin), which showed a moderate to strong resistance toward both UVC and UVC/H2O2, were effectively removed by algal treatment, as discussed earlier (see ESI† Fig. S5). Although the addition of 0.5 mM H2O2 to raw wastewater improved the performance of UVC treatment under the given experimental conditions, about half of those antibiotics still remained. That is, the treatment of livestock wastewater effluent with both UVC and UVC/H2O2 achieved 41–61% removal of chlortetracycline, 15–17% removal of erythromycin, 50–64% removal of oxytetracycline, 25–49% removal of penicillin-G, 57–58% removal of tetracycline, and 40–55% removal of tiamulin; thus, they would mostly remain even after the UVC treatment, unless algal treatment was applied.

3.3. Improved removal of antibiotics using ozonation prior to UVC and UVC/H2O2

In this study, we applied ozonation to the oxidation of livestock wastewater effluent ahead of UVC treatment. UVC treatment was carried out after dissolved O3 was consumed completely; thus, photolytic O3 decomposition was not discussed in this section. The ozonation followed by UVC treatment (O3 + UVC and O3 + UVC/H2O2) removed >99% of total antibiotics in the effluent and the pH effect was negligible (see Fig. 6). Both UVC and UVC/H2O2 further removed antibiotic residues in the ozonated wastewater, but less than 1% of the initial antibiotics. Although the degradation of selected antibiotics was dominated by ozonation, this should be complemented for further removal of accumulated antibiotics resistant to ozone oxidation considering the total mass of antibiotics released to the water environment. For that purpose, subsequent UVC treatment is still considered valid, and O3/H2O2 could be applied as AOPs for process simplicity. However, the removal of antibiotics by ozonation was considerably decreased by addition of H2O2. Fig. 7 shows that the addition of H2O2 (up to 1 mM) to the effluent resulted in decreased removal of antibiotics upon ozonation regardless of pH values examined. The residual concentration of total antibiotics was always higher when ozonating the wastewater effluent with added H2O2; especially, clopidol was highly resistant to the oxidation with O3/H2O2, probably because there were enough organic promoters in the effluent to promote O3 chain reactions. Therefore, H2O2 added as an external promoter could reversely scavenge OH radicals produced in the chain reactions.55,56
image file: d0ew00634c-f6.tif
Fig. 6 Comparison of two different treatment methods (O3 + UVC vs. O3 + UVC/H2O2) in the removal of antibiotics, DOC, and UV254 from raw neutral (a–c) and algal-treated alkaline (d–f) livestock wastewater. Ozonation (1.5 mg O3 per mg C, 10 min) was followed by UVC irradiation (0, 500, 1000, and 2000 mJ cm−2). For O3 + UVC/H2O2, H2O2 was added to raw and algal-treated wastewater in a final concentration of 0.5 mM just before UVC irradiation.

image file: d0ew00634c-f7.tif
Fig. 7 The effects of H2O2 concentrations (0, 0.5, and 1 mM) on the removal of total antibiotics (a) and clopidol (b) upon the ozonation (1.5 mg O3 per mg C, 10 min) of raw neutral and algal-treated alkaline livestock wastewater.

Separate ozonation test was conducted and the result of antibiotics removal is illustrated in Fig. 8, in which changes in water quality parameters are also shown as a function of ozonation continued for up to 10 min (equivalent to ∼1.8 mg O3 per mg C). A significant removal (p < 0.05) of selected antibiotics was achieved by algal treatment, as discussed in section 3.1 (see Fig. 2). Regardless of pH values, >90% removal of total antibiotics was achieved by ozonation for 5 min or longer (see Fig. 8a). Florfenicol accounted for the majority of antibiotic residues in the ozonated wastewater (see ESI† Fig. S6), indicating the recalcitrant characteristics of florfenicol toward ozonation. The removal of florfenicol ranged from only 16 to 34% as a function of O3 dose (see Fig. 8b). A similar limitation in the degradation of florfenicol with ozonation has been previously reported.57Fig. 8b also shows a remarkable increase in the degradability of florfenicol when ozonating algal-treated wastewater, achieving 30–51% removal. Although the fate of florfenicol during O3-based oxidation is sparse in the literature, we speculate that the oxidation of florfenicol was improved by the faster generation of OH radicals at elevated pH levels, since pH varied with ozonation. The alkaline ozonation decreased the pH of wastewater to a much greater extent than did that observed for neutral ozonation, indicating a higher consumption of OH− catalyzing the decomposition of O3 under alkaline conditions. In general, the reactions of organic compounds with OH radicals, close to the diffusion-controlled limit (∼1010 M−1 s−1), are much faster than are those with O3 molecules.58 Decrement in the pH of wastewater during alkaline ozonation could thus be greater with accumulated carboxylic acids as oxidation byproducts.31 Considering the concentration of effluent organic matter (5.8–7.2 mM as C) in the wastewater effluent and its reaction with OH radicals (1.4–4.5 × 108 M C−1),59 the radical scavenging of alkalinity (0.5–0.6 mM as HCO3−) could be negligible in this study. Higher degradation of antibiotics during ozonation at alkaline pH has been previously reported.28,32,33


image file: d0ew00634c-f8.tif
Fig. 8 The changes in total antibiotics (a), florfenicol (b), pH (c), SUVA (d), color (e), UV254 (f), COD (g), and DOC (h) upon ozonation. The ozonation of raw and algal-treated livestock wastewater was carried out for up to 10 min (equivalent to ∼1.8 mg O3 per mg C). For ozonation of algal-treated wastewater, the percent removals of antibiotics and organic-related parameters include the removal achieved by algal-treatment.

3.4. The effects of algal treatment on the fate of effluent organic matter by ozonation

The ozonation of livestock wastewater effluent with two different pH values (raw nominally-neutral and algal-treated alkaline, see Fig. 8c) was conducted for up to 10 min (equivalent to ∼1.8 mg O3 per mg C). A slight removal of dissolved organic components was found after the algal treatment alone under autotrophic conditions (see Fig. 6 and 8), which could be associated with a wide variety of non-metabolic processes (physicochemical sorption, ion exchange, complexation, and so forth) on the surface of the algal cells.60,61 Decreases in the SUVA, color, UV254, COD, and DOC were found upon ozonation, and the removal of those parameters was always higher in alkaline ozonation than in neutral ozonation (see Fig. 8d–h). The chromaticity decreased steeply, but was not completely removed, for the given time of ozonation. The UV254 decreased stepwise as the O3 dose was increased, whereas DOC change was negligible under the given ozonation conditions. Effluent organic matter was also determined as COD, and the removal was relatively higher than was the DOC removal, probably because of the oxidation of reduced inorganic species, which could also be oxidized quantitatively under the test conditions for COD measurement.

The reduction of UV254 was associated with the degradation of aromatic compounds and subsequent conversion to low-molecular substances such as ketone, carboxylic acids, and aldehydes.62,63 The low abatement of DOC could be attributed to accumulated low-molecular compounds, which are generally not susceptible to O3 and OH radicals and thus are difficult to completely mineralize. Among the integrated oxidation processes examined in this study, O3 + UVC/H2O2 achieved the greatest removal of the DOC from algal-treated wastewater, but it accounted for only 11% (see Fig. 6f). Numerous studies have shown greater removal of UV-absorbing materials than of effluent organic matter quantified as DOC during ozonation, resulting in a decrease in the level of SUVA.64,65 The observations were also consistent with the results shown for the fluorescence measurements of this study. Fig. 9 shows that the fluorescent moieties of effluent organic matter dramatically decreased with increasing O3 dose regardless of pH values examined. The fluorescence spectra of organic components in livestock wastewater effluent show a typical feature of humic substances, and a negligible change in the fluorescence intensity was found after the 12 h cultivation of microalgae in the effluent. Moreover, tryptophan-like components that are typically associated with microbial activities were found in neither raw nor algal-treated wastewater. The profile of dissolved organic matter can be changed by extracellular polymeric substances formed during biological metabolism and biomass decay,36,66 but there were no observations supporting such changes in this study. The fluorophores originating from humic-like substances are generally enriched with aromatic constituents,67–69 which are preferentially reactive to electrophilic oxidants (e.g., O3).58 The effluent treated by alkaline ozonation showed a relatively lower intensity of the fluorophores, which coincided with a greater reduction in UV-absorbing components than when neutral ozonation was done (see Fig. 8f). This indicates either the degradation or mineralization of the corresponding fluorophores or functional groups that are present in the chemical structure of the fluorescent organic matter.70,71


image file: d0ew00634c-f9.tif
Fig. 9 The fluorescence excitation–emission matrices of effluent organic matter remaining after ozonation of raw neutral (a–c) and algal-treated alkaline (d–f) livestock wastewater effluent at three different doses of 0, 0.9, and 1.8 mg O3 per mg C (equivalent to 0, 5, and 10 min).

For alleviating the burden of receiving water bodies, quaternary-treated wastewater can be further treated with biologically-active processes. Biological treatment following ozone oxidation is a well-established strategy to effectively remove effluent organic matter by converting refractory organic compounds into biodegradable fractions, rather than by completely oxidizing them. We previously determined that pretreatment with proper levels of O3 substantially improves the bioavailability of organic matter for mixotrophic microalgae in the bioremediation of piggery wastewater.64 In the previous study, we also noticed that S. quadricauda performed mixotrophic growth depending on culture conditions, in addition to the common photoautotrophic growth when using CO2 as the sole carbon source. This observation reveals the high adaptability of switchable algal treatment to fluctuating livestock wastewater quality, indicating the operational diversity of algal treatment to remove biodegradable organic components in a single biological reactor.

4. Conclusions

Algal treatment was combined with subsequent ozonation and/or photolytic oxidation to improve the antibiotics removal and refractory organics degradation in livestock wastewater effluent. The algal treatment removed effectively some antibiotics (chlortetracycline, erythromycin, oxytetracycline, penicillin-G, tetracycline, and tiamulin) that were highly resistant to UVC treatment (UVC and UVC/H2O2). In addition to reducing antibiotics directly, the algae-induced alkaline conditions (pH > 10) were synergistic with H2O2 (0.5 mM) in the removal of sulfamethazine, lincomycin and trimethoprim during UVC irradiation (up to 2000 mJ cm−2). Similarly, the removal of clopidol by UVC treatment was always higher in algal-treated alkaline wastewater than in raw neutral wastewater, and the degradation of O3-resistant florfenicol was improved upon ozonation (∼1.8 mg O3 per mg C) in the alkaline wastewater.

This study also corroborated the effectiveness of integrating ozonation and UVC treatment in removing antibiotics from livestock waster effluent. The ozonation dominated the degradation of selected antibiotics, but required further removal of accumulated antibiotics resistant to ozone oxidation. Considering the total mass of antibiotics released to water bodies, subsequent UVC treatment is still considered valid as a promising complementary strategy for robust removal of accumulated antibiotics resistant to ozone oxidation. O3/H2O2 could be applied for process simplicity; however, the removal of antibiotics by ozonation was considerably inhibited by addition of H2O2, whereas UVC performance was generally improved by adding H2O2.

Our results indicate that the oxidation of algal-treated alkaline wastewater could be a better option to effectively remove antibiotics remaining in secondary- or tertiary-treated effluent, depending on the physicochemical characteristics of antibiotics. In contrast to increasing pH of wastewater with caustic chemicals, the alternative strategy proposed in this study could make alkaline oxidation realistic and economically more feasible. Moreover, this algae-induced alkalization is readily convertible to mixotrophic bio-treatment for removal of carbonaceous organic residues in oxidized wastewater effluent. Despite quaternary treatment using oxidation-based processes, effluent organic matter (determined as DOC) mostly remained. In addition to recarbonation of the treated wastewater, a biologically active treatment process should be considered for further removal of the biodegradable organic fraction that was identified by characterizing effluent organic matter.

Conflicts of interest

There are no conflicts of interest to declare.

Acknowledgements

This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A2A2A05022776). This research was also partially supported by the grant (2016000710005) funded by the Korea Ministry of Environment as a part of the project “Environmental Policy Based Public Technology R&D”.

References

  1. M. O. Barbosa, N. F. F. Moreira, A. R. Ribeiro, M. F. R. Pereira and A. M. T. Silva, Occurrence and removal of organic micropollutants: An overview of the watch list of EU Decision 2015/495, Water Res., 2016, 94, 257–279 CrossRef CAS .
  2. F. Kaczala and S. E. Blum, The occurrence of veterinary pharmaceuticals in the environment: A review, Curr. Anal. Chem., 2016, 12, 169–182 CrossRef CAS .
  3. M. Patel, R. Kumar, K. Kishor, T. Mlsna, C. U. Pittman and D. Mohan, Pharmaceuticals of emerging concern in aquatic systems: Chemistry, occurrence, effects, and removal methods, Chem. Rev., 2019, 119, 3510–3673 CrossRef CAS .
  4. F. Baquero, J.-L. Martínez and R. Cantón, Antibiotics and antibiotic resistance in water environments, Curr. Opin. Biotechnol., 2008, 19, 260–265 CrossRef CAS .
  5. N. Hembach, F. Schmid, J. Alexander, C. Hiller, E. T. Rogall and T. Schwartz, Occurrence of the mcr-1 colistin resistance gene and other clinically relevant antibiotic resistance genes in microbial populations at different municipal wastewater treatment plants in Germany, Front. Microbiol., 2017, 8, 1282–1282 CrossRef .
  6. S. Kim, Z. Yun, U.-H. Ha, S. Lee, H. Park, E. E. Kwon, Y. Cho, S. Choung, J. Oh, C. A. Medriano and K. Chandran, Transfer of antibiotic resistance plasmids in pure and activated sludge cultures in the presence of environmentally representative micro-contaminant concentrations, Sci. Total Environ., 2014, 468–469, 813–820 CrossRef CAS .
  7. D. Li, M. Yang, J. Hu, J. Zhang, R. Liu, X. Gu, Y. Zhang and Z. Wang, Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving river, Environ. Microbiol., 2009, 11, 1506–1517 CrossRef CAS .
  8. K. M. M. Pärnänen, C. Narciso-da-Rocha, D. Kneis, T. U. Berendonk, D. Cacace, T. T. Do, C. Elpers, D. Fatta-Kassinos, I. Henriques, T. Jaeger, A. Karkman, J. L. Martinez, S. G. Michael, I. Michael-Kordatou, K. O'Sullivan, S. Rodriguez-Mozaz, T. Schwartz, H. Sheng, H. Sørum, R. D. Stedtfeld, J. M. Tiedje, S. V. D. Giustina, F. Walsh, I. Vaz-Moreira, M. Virta and C. M. Manaia, Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence, Sci. Adv., 2019, 5, eaau9124 CrossRef .
  9. F. Barancheshme and M. Munir, Strategies to combat antibiotic resistance in the wastewater treatment plants, Front. Microbiol., 2018, 8, 2603 CrossRef .
  10. O. L. Davies and S. Bennett, WHO publishes list of bacteria for which new antibiotics are urgently needed, https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed, (accessed November 3, 2020) .
  11. K. D. Brown, J. Kulis, B. Thomson, T. H. Chapman and D. B. Mawhinney, Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico, Sci. Total Environ., 2006, 366, 772–783 CrossRef CAS .
  12. M. S. Díaz-Cruz and D. Barceló, Recent advances in LC-MS residue analysis of veterinary medicines in the terrestrial environment, TrAC, Trends Anal. Chem., 2007, 26, 637–646 CrossRef .
  13. V. Homem and L. Santos, Degradation and removal methods of antibiotics from aqueous matrices – A review, J. Environ. Manage., 2011, 92, 2304–2347 CrossRef CAS .
  14. L.-J. Zhou, G.-G. Ying, S. Liu, R.-Q. Zhang, H.-J. Lai, Z.-F. Chen and C.-G. Pan, Excretion masses and environmental occurrence of antibiotics in typical swine and dairy cattle farms in China, Sci. Total Environ., 2013, 444, 183–195 CrossRef CAS .
  15. A. K. Sarmah, M. T. Meyer and A. B. A. Boxall, A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment, Chemosphere, 2006, 65, 725–759 CrossRef CAS .
  16. M. Y. Haller, S. R. Müller, C. S. McArdell, A. C. Alder and M. J. F. Suter, Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromatography–mass spectrometry, J. Chromatogr. A, 2002, 952, 111–120 CrossRef CAS .
  17. N. T. Malintan and M. A. Mohd, Determination of sulfonamides in selected Malaysian swine wastewater by high-performance liquid chromatography, J. Chromatogr. A, 2006, 1127, 154–160 CrossRef CAS .
  18. L.-Y. He, G.-G. Ying, Y.-S. Liu, H.-C. Su, J. Chen, S.-S. Liu and J.-L. Zhao, Discharge of swine wastes risks water quality and food safety: Antibiotics and antibiotic resistance genes from swine sources to the receiving environments, Environ. Int., 2016, 92–93, 210–219 CrossRef CAS .
  19. Y. He, Q. Yuan, J. Mathieu, L. Stadler, N. Senehi, R. Sun and P. J. J. Alvarez, Antibiotic resistance genes from livestock waste: Occurrence, dissemination, and treatment, npj Clean Water, 2020, 3, 4 CrossRef .
  20. A. J. Watkinson, E. J. Murby and S. D. Costanzo, Removal of antibiotics in conventional and advanced wastewater treatment: Implications for environmental discharge and wastewater recycling, Water Res., 2007, 41, 4164–4176 CrossRef CAS .
  21. Y. Ben, M. Hu, X. Zhang, S. Wu, M. H. Wong, M. Wang, C. B. Andrews and C. Zheng, Efficient detection and assessment of human exposure to trace antibiotic residues in drinking water, Water Res., 2020, 175, 115699 CrossRef CAS .
  22. S. Jia, K. Bian, P. Shi, L. Ye and C.-H. Liu, Metagenomic profiling of antibiotic resistance genes and their associations with bacterial community during multiple disinfection regimes in a full-scale drinking water treatment plant, Water Res., 2020, 176, 115721 CrossRef CAS .
  23. D. Simazaki, R. Kubota, T. Suzuki, M. Akiba, T. Nishimura and S. Kunikane, Occurrence of selected pharmaceuticals at drinking water purification plants in Japan and implications for human health, Water Res., 2015, 76, 187–200 CrossRef CAS .
  24. H. Wang, N. Wang, B. Wang, Q. Zhao, H. Fang, C. Fu, C. Tang, F. Jiang, Y. Zhou, Y. Chen and Q. Jiang, Antibiotics in drinking water in Shanghai and their contribution to antibiotic exposure of school children, Environ. Sci. Technol., 2016, 50, 2692–2699 CrossRef CAS .
  25. D. B. Miklos, C. Remy, M. Jekel, K. G. Linden, J. E. Drewes and U. Hübner, Evaluation of advanced oxidation processes for water and wastewater treatment – A critical review, Water Res., 2018, 139, 118–131 CrossRef CAS .
  26. C. Han, M. Pelaez, V. Likodimos, A. G. Kontos, P. Falaras, K. O'Shea and D. D. Dionysiou, Innovative visible light-activated sulfur doped TiO2 films for water treatment, Appl. Catal., B, 2011, 107, 77–87 CrossRef CAS .
  27. C. Han, V. Likodimos, J. A. Khan, M. N. Nadagouda, J. Andersen, P. Falaras, P. Rosales-Lombardi and D. D. Dionysiou, UV–visible light-activated Ag-decorated, monodisperse TiO2 aggregates for treatment of the pharmaceutical oxytetracycline, Environ. Sci. Pollut. Res., 2014, 21, 11781–11793 CrossRef CAS .
  28. G. Boczkaj and A. Fernandes, Wastewater treatment by means of advanced oxidation processes at basic pH conditions: A review, Chem. Eng. J., 2017, 320, 608–633 CrossRef CAS .
  29. E. M. Cuerda-Correa, M. F. Alexandre-Franco and C. Fernández-González, Advanced oxidation processes for the removal of antibiotics from water. An overview, Water, 2020, 12, 102 CrossRef CAS .
  30. J. C. Crittenden, R. R. Trussell, D. W. Hand, K. J. Howe and G. Tchobanoglous, in MWH's Water Treatment: Principles and Design, John Wiley & Sons, Inc., 2012, ch. 18, pp. 1415–1484,  DOI:10.1002/9781118131473 .
  31. W. Li, X. Xu, B. Lyu, Y. Tang, Y. Zhang, F. Chen and G. Korshin, Degradation of typical macrolide antibiotic roxithromycin by hydroxyl radical: Kinetics, products, and toxicity assessment, Environ. Sci. Pollut. Res., 2019, 26, 14570–14582 CrossRef CAS .
  32. R. F. Dantas, S. Contreras, C. Sans and S. Esplugas, Sulfamethoxazole abatement by means of ozonation, J. Hazard. Mater., 2008, 150, 790–794 CrossRef CAS .
  33. J. Wu, Y. Jiang, L. Zha, Z. Ye, Z. Zhou, J. Ye and H. Zhou, Tetracycline degradation by ozonation, and evaluation of biodegradability and toxicity of ozonation byproducts, Can. J. Civ. Eng., 2010, 37, 1485–1491 CrossRef CAS .
  34. S. K. Maeng, W. Khan, J. W. Park, I. Han, H. S. Yang, K. G. Song, W. J. Choi, S. Kim, H. Woo and H.-C. Kim, Treatment of highly saline RO concentrate using Scenedesmus quadricauda for enhanced removal of refractory organic matter, Desalination, 2018, 430, 128–135 CrossRef CAS .
  35. H.-C. Kim, W. J. Choi, J. H. Ryu, S. K. Maeng, H. S. Kim, B.-C. Lee and K. G. Song, Optimizing cultivation strategies for robust algal growth and consequent removal of inorganic nutrients in pretreated livestock effluent, Appl. Biochem. Biotechnol., 2014, 174, 1668–1682 CrossRef CAS .
  36. H.-C. Kim, W. J. Choi, A. N. Chae, J. Park, H. J. Kim and K. G. Song, Evaluating integrated strategies for robust treatment of high saline piggery wastewater, Water Res., 2016, 89, 222–231 CrossRef CAS .
  37. S. K. Maeng, S. H. You, J.-Y. Nam, H. Ryu, T. C. Timmes and H.-C. Kim, The growth of Scenedesmus quadricauda in RO concentrate and the impacts on refractory organic matter, Escherichia coli, and trace organic compounds, Water Res., 2018, 134, 292–300 CrossRef CAS .
  38. J.-Q. Xiong, M. B. Kurade and B.-H. Jeon, Can Microalgae remove pharmaceutical contaminants from water?, Trends Biotechnol., 2018, 36, 30–44 CrossRef CAS .
  39. Y. Yu, Y. Zhou, Z. Wang, O. L. Torres, R. Guo and J. Chen, Investigation of the removal mechanism of antibiotic ceftazidime by green algae and subsequent microbic impact assessment, Sci. Rep., 2017, 7, 4168 CrossRef .
  40. X. Bai and K. Acharya, Removal of trimethoprim, sulfamethoxazole, and triclosan by the green alga Nannochloris sp, J. Hazard. Mater., 2016, 315, 70–75 CrossRef CAS .
  41. A. de Wilt, A. Butkovskyi, K. Tuantet, L. H. Leal, T. V. Fernandes, A. Langenhoff and G. Zeeman, Micropollutant removal in an algal treatment system fed with source separated wastewater streams, J. Hazard. Mater., 2016, 304, 84–92 CrossRef CAS .
  42. G.-J. Zhou, G.-G. Ying, S. Liu, L.-J. Zhou, Z.-F. Chen and F.-Q. Peng, Simultaneous removal of inorganic and organic compounds in wastewater by freshwater green microalgae, Environ. Sci.: Processes Impacts, 2014, 16, 2018–2027 RSC .
  43. W. Khan, J.-Y. Nam, H. Woo, H. Ryu, S. Kim, S. K. Maeng and H.-C. Kim, A proof of concept study for wastewater reuse using bioelectrochemical processes combined with complementary post-treatment technologies, J. Environ. Sci. Water Resour., 2019, 5, 1489–1498 RSC .
  44. S. R. Lyon, H. Ahmadzadeh and M. A. Murry, in Biomass and Biofuels from Microalgae: Advances in Engineering and Biology, ed. R. N. Moheimani, P. M. McHenry, K. de Boer and A. P. Bahri, Springer International Publishing, Cham, 2015, pp. 95–115,  DOI:10.1007/978-3-319-16640-7_6 .
  45. J. R. Bolton, S. E. Beck and K. G. Linden, Protocol for the determination of fluence (UV dose) using a low-pressure or low-pressure high-output UV lamp in bench-scale collimated beam ultraviolet experiments, IUVA News, 2015, vol. 17, pp. 11–16 Search PubMed.
  46. R. F. P. Nogueira, M. C. Oliveira and W. C. Paterlini, Simple and fast spectrophotometric determination of H2O2 in photo-Fenton reactions using metavanadate, Talanta, 2005, 66, 86–91 CrossRef CAS .
  47. A. Garcia-Rodríguez, V. Matamoros, C. Fontàs and V. Salvadó, The influence of light exposure, water quality and vegetation on the removal of sulfonamides and tetracyclines: A laboratory-scale study, Chemosphere, 2013, 90, 2297–2302 CrossRef .
  48. S. Jiao, S. Zheng, D. Yin, L. Wang and L. Chen, Aqueous photolysis of tetracycline and toxicity of photolytic products to luminescent bacteria, Chemosphere, 2008, 73, 377–382 CrossRef CAS .
  49. P. Xie, S.-H. Ho, J. Peng, X.-J. Xu, C. Chen, Z.-F. Zhang, D.-J. Lee and N.-Q. Ren, Dual purpose microalgae-based biorefinery for treating pharmaceuticals and personal care products (PPCPs) residues and biodiesel production, Sci. Total Environ., 2019, 688, 253–261 CrossRef CAS .
  50. C. Zhao, M. Pelaez, X. Duan, H. Deng, K. O'Shea, D. Fatta-Kassinos and D. D. Dionysiou, Role of pH on photolytic and photocatalytic degradation of antibiotic oxytetracycline in aqueous solution under visible/solar light: Kinetics and mechanism studies, Appl. Catal., B, 2013, 134–135, 83–92 CrossRef CAS .
  51. I. M. Power, S. A. Wilson, D. P. Small, G. M. Dipple, W. Wan and G. Southam, Microbially mediated mineral carbonation: Roles of phototrophy and heterotrophy, Environ. Sci. Technol., 2011, 45, 9061–9068 CrossRef CAS .
  52. R. Xiao and Y. Zheng, Overview of microalgal extracellular polymeric substances (EPS) and their applications, Biotechnol. Adv., 2016, 34, 1225–1244 CrossRef CAS .
  53. X. Duan, X. He, D. Wang, S. P. Mezyk, S. C. Otto, R. Marfil-Vega, M. A. Mills and D. D. Dionysiou, Decomposition of iodinated pharmaceuticals by UV-254 nm-assisted advanced oxidation processes, J. Hazard. Mater., 2017, 323, 489–499 CrossRef CAS .
  54. A. Dulov, N. Dulova and M. Trapido, Photochemical degradation of nonylphenol in aqueous solution: The impact of pH and hydroxyl radical promoters, J. Environ. Sci., 2013, 25, 1326–1330 CrossRef CAS .
  55. B. H. Diya'uddeen, W. M. A. W. Daud and A. R. Abdul Aziz, Treatment technologies for petroleum refinery effluents: A review, Process Saf. Environ. Prot., 2011, 89, 95–105 CrossRef .
  56. J. P. Pocostales, M. M. Sein, W. Knolle, C. von Sonntag and T. C. Schmidt, Degradation of ozone-refractory organic phosphates in wastewater by ozone and ozone/hydrogen peroxide (peroxone): The role of ozone consumption by dissolved organic matter, Environ. Sci. Technol., 2010, 44, 8248–8253 CrossRef CAS .
  57. Y. Zhang, Y. Shao, N. Gao, W. Chu, J. Chen, S. Li, Y. Wang and S. Xu, Chlorination of florfenicol (FF): Reaction kinetics, influencing factors and by-products formation, RSC Adv., 2016, 6, 107256–107262 RSC .
  58. D. Gerrity, F. L. Rosario-Ortiz and E. C. Wert, in Advanced Oxidation Processes for Water Treatment: Fundamentals and Applications, ed. M. I. Stefan, IWA Publishing, London, UK, 2017,  DOI:10.2166/9781780407197_0123 .
  59. P. Westerhoff, S. P. Mezyk, W. J. Cooper and D. Minakata, Electron pulse radiolysis determination of hydroxyl radical rate constants with suwannee river fulvic acid and other dissolved organic matter isolates, Environ. Sci. Technol., 2007, 41, 4640–4646 CrossRef CAS .
  60. P. Chakravarty, K. Bauddh and M. Kumar, in Algae and Environmental Sustainability, ed. B. Singh, K. Bauddh and F. Bux, Springer, India, New Delhi, 2015, pp. 97–106,  DOI:10.1007/978-81-322-2641-3_8 .
  61. Z. Aksu and S. Tezer, Biosorption of reactive dyes on the green alga Chlorella vulgaris, Process Biochem., 2005, 40, 1347–1361 CrossRef CAS .
  62. A. Azaïs, J. Mendret, G. Cazals, E. Petit and S. Brosillon, Ozonation as a pretreatment process for nanofiltration brines: Monitoring of transformation products and toxicity evaluation, J. Hazard. Mater., 2017, 338, 381–393 CrossRef .
  63. S. Van Geluwe, C. Vinckier, L. Braeken and B. Van der Bruggen, Ozone oxidation of nanofiltration concentrates alleviates membrane fouling in drinking water industry, J. Membr. Sci., 2011, 378, 128–137 CrossRef CAS .
  64. H.-C. Kim, W. J. Choi, S. K. Maeng, H. J. Kim, H. S. Kim and K. G. Song, Ozonation of piggery wastewater for enhanced removal of contaminants by S. quadricauda and the impact on organic characteristics, Bioresour. Technol., 2014, 159, 128–135 CrossRef CAS .
  65. H.-C. Kim, W. M. Lee, S. Lee, J. Choi and S. K. Maeng, Characterization of organic precursors in DBP formation and AOC in urban surface water and their fate during managed aquifer recharge, Water Res., 2017, 123, 75–85 CrossRef CAS .
  66. L. O. Villacorte, Y. Ekowati, T. R. Neu, J. M. Kleijn, H. Winters, G. Amy, J. C. Schippers and M. D. Kennedy, Characterisation of algal organic matter produced by bloom-forming marine and freshwater algae, Water Res., 2015, 73, 216–230 CrossRef CAS .
  67. L. Fu, C. Wu, Y. Zhou, J. Zuo, G. Song and Y. Tan, Ozonation reactivity characteristics of dissolved organic matter in secondary petrochemical wastewater by single ozone, ozone/H2O2, and ozone/catalyst, Chemosphere, 2019, 233, 34–43 CrossRef CAS .
  68. H.-C. Kim, S. H. Park, J. H. Noh, J. Choi, S. Lee and S. K. Maeng, Comparison of pre-oxidation between O3 and O3/H2O2 for subsequent managed aquifer recharge using laboratory-scale columns, J. Hazard. Mater., 2019, 377, 290–298 CrossRef CAS .
  69. M. Li, Q. Wen, Z. Chen, Y. Tang and B. Yang, Comparison of ozonation and UV based oxidation as pre-treatment process for ultrafiltration in wastewater reuse: Simultaneous water risks reduction and membrane fouling mitigation, Chemosphere, 2020, 244, 125449 CrossRef CAS .
  70. H.-C. Kim, M. J. Yu and I. Han, Multi-method study of the characteristic chemical nature of aquatic humic substances isolated from the Han River, Korea, Appl. Geochem., 2006, 21, 1226–1239 CrossRef CAS .
  71. T. Liu, Z.-L. Chen, W.-Z. Yu and S.-J. You, Characterization of organic membrane foulants in a submerged membrane bioreactor with pre-ozonation using three-dimensional excitation–emission matrix fluorescence spectroscopy, Water Res., 2011, 45, 2111–2121 CrossRef CAS .

Footnote

† Electronic supplementary information (ESI) available. See DOI: 10.1039/d0ew00634c
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