Enhancing microalgae growth and landfill leachate treatment through ozonization

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Enhancing microalgae growth and landfill leachate treatment through ozonization Xuejun Quan a, Rui Hu a, Haixing Chang a, *, Xiaoyu Tang a, Xiaoxue Huang a, Chen Cheng a, Nianbing Zhong b, **, Lu Yang c, d a

School of Chemistry and Chemical Engineering, Chongqing University of Technology, Chongqing, 400054, China Chongqing Key Laboratory of Fiber Optic Sensor and Photodetector, Chongqing Key Laboratory of Modern Photoelectric Detection Technology and Instrument, Chongqing University of Technology, Chongqing, 400054, China c Chongqing University of Science & Technology, Chongqing, 400054, China d Chongqing Municipal Solid Waste Resource Utilization & Treatment Collaborative Innovation Center, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 August 2019 Received in revised form 7 October 2019 Accepted 4 November 2019 Available online xxx

Phycoremediation of landfill leachate (LL) with microalgae is a promising approach but the performances are usually inhibited by complex macromolecular organics and high chromaticity of the LL. To realize high-efficiency LL remediation and microalgae biomass production, a technique integrating ozonization and microalgae bioremediation was proposed, in which the LL was first pretreated with ozone to degrade most macromolecular organics and reduce chromaticity. Then the oxidized LL was remediated with microalgae biofilm to reclaim nutrients and produce biomass. Results showed that chromaticity was sharply reduced from 1400 to 45 PteCo and macromolecular organics were significantly reduced from 93.3% in the untreated LL to 54.8% in the oxidized LL via ozonization under 45 mg O3/L for 45 min. The oxidized LL effectively enhanced microalgae growth and nitrogen removal. Then a phosphorus-feeding strategy was adopted to obtain different nitrogen/phosphorus (N/P) molar ratio of 33:1, 16:1; 7:1 and 3:1 for further enhancement of microalgae growth and nitrogen removal. As results, the maximum biofilm density of 28.0 g/m2 and the highest nitrogen removal efficiency of 81.6% under N/P molar ratio of 16:1 were achieved. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: M.T. Moreira Keywords: Biomass Landfill leachate Microalgae Macromolecular organics Ozonization

1. Introduction Landfill leachate (LL), which is generated from landfilling process for solid wastes disposal, is a type of liquid waste containing high quantity of organic and inorganic substances (Colombo et al., 2019). Due to strong toxicity of these matters in the LL, direct discharge of the LL into water system potentially causes severe pollution on water body, like eutrophication and aquatic organism death (Gautam et al., 2019). Therefore, a thorough treatment of the LL before discharge is necessary for sustainable development (Zhu et al., 2018a). Currently, the LL treating methods mainly include membrane separation, advanced oxidation processes (AOPs), active carbon and biological active carbon. But there are still many

* Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (H. Chang), [email protected] (N. Zhong).

problems that barring the application of these techniques. For example, membrane fouling during membrane separation process, difficulties on inorganic salts removal from wastewater during AOPs, high cost on regeneration of active carbon/biological active carbon, are still urging problems that should be addressed (Ghuge and Saroha, 2018; Cheng et al., 2018). Moreover, the aforementioned methods mainly focused on inorganic and organic removal from wastewater but paid little attention on nutrients recycling (Dogaris et al., 2019). In contrast, microalgae can utilize organics and inorganics (nitrogen, phosphorus, etc.) in LL as nutrients and sequestrate CO2 from flue gas as carbon source to produce bioresource, like lipids and carbohydrates (Liao et al., 2018; Sun et al., 2018, 2019; Zhu et al., 2018b). Culturing microalgae with LL can substantially reduce the cost on LL treatment and microalgae biomass production since LL can supply copious nutrients for microalgae growth, simultaneously realizing wastewater remediation and bioresource generation. Thus, microalgae-based bioremediation of LL provides a promising option to alleviate environmental pollution and resource crisis, greatly improving the

https://doi.org/10.1016/j.jclepro.2019.119182 0959-6526/© 2019 Elsevier Ltd. All rights reserved.

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economic efficiency of LL treatment. However, the performances of LL treatment and microalgae biomass production were still poor in the existing works attributing to complex property of the LL, especially the nonbiodegradable macromolecular organics and high chromaticity (Sniffen et al., 2018). Although compositions of LL vary with the components of solid wastes and landfill operating conditions, the LL usually contains extremely high content of organics and heavy chromaticity. da Costa et al. (2018) and Paul et al. (2019) analyzed the organic compositions of LL and found more than 70 types of organic pollution in the LL stream, including phenol, aromatic hydrocarbons, chlorinated aliphatics, etc., which were strong toxic to microalgae cells. El Ouaer et al. (2017) showed that microalgae could hardly grow in raw LL, with cell density of only 1
105 cell/ ml for Chlorella sp. The poor growth profile of microalgae in the untreated LL sharply reduced the removal rate of inorganic salts and hindered its application. To reduce the inhibiting effects of LL on microalgae cell, dilution was a most commonly used method to offset the toxic effects of organics and chromaticity on microalgae cells (Chang et al., 2019; Paskuliakova et al., 2018). Khanzada and Ovez (2017) demonstrated that NH þ 4 in the LL was completely removed by diluting the LL to 10% with fresh water, but microalgae exhibited poor growth profile owing to the scare nutrients in 10% diluted LL. A maximum dry biomass concentration of 1.67 g/L could be acquired by controlling proportions of LL to 50%, which provided more sufficient nutrients for microalgae growth than the case of 10% dilution rate. Nevertheless, the large requirement for fresh water during dilution significantly aggravated the fresh water scarcity. In order to reduce the fresh water utilization during dilution, Moreno-Garcia et al. (2019) mixed liquid streams from four various wastewater and obtained a maximum biomass productivity of 22.76 mg/L/d. However, the biomass productivity was still poor and microalgae cells were damaged when the proportion of LL exceed 13.33%. Other methods like isolation of tolerant microalgae strains were also tried to resolve the growth inhibition caused by LL toxicity (Lin et al., 2007; Paskuliakova et al., 2016), which improved microalgae growth and LL treating performances to some extent. But the isolated microalgae strains could not be widely applied to other LL types since compositions (especially the recalcitrant organics) of LL from different positions varied significantly. Until now, a practicable method to offset the inhibiting effects of LL on microalgae growth caused by high chromaticity and toxic organics is lack (Chang et al., 2019; Edmundson and Wilkie, 2013). As one type of the AOPs, ozonization was commonly seen in wastewater treatment (Li et al., 2019; Van Aken et al., 2017), but application of ozonization in resource recovery from LL by combining with microalgae technology was yet to be reported. Herein, an integrated technique containing ozonization followed by microalgae biofilm bioremediation was proposed for highefficiency LL remediation and microalgae biomass production. During ozonization process, the macromolecular organics were degraded by ozone which had strong oxidizing capacity to offset the inhibiting effects of the LL caused by complex macromolecular organics on microalgae cells. Meanwhile, chromaticity of the LL was also greatly reduced since the structure of organic pollutants with chromophore group was destroyed by the ozone, which then enhanced microalgal photosynthesis. Then the oxidized LL was used as culture medium for microalgae Scenedesmus obliquus biofilm cultivation to produce bioresource. Attached mode of microalgae cultivation was chosen in this work attributing to the advantages of stronger resistance to wastewater, easier harvesting of microalgae biomass, and less water requirement when comparing with suspended microalgae cultivation. Results showed that the integrated technique of ozonization and microalgae

remediation had a great potential for industrial application on LL treatment and bioresource production. The aims of this work were to: 1) characterize the effect of ozonization time on LL physicalchemical properties variations; 2) assess the performance of the proposed process integrating ozonization and microalgae remediation, especially on organics and inorganics removal as well as microalgae biomass production; 3) analyze the effects of N:P ratio on inorganics removal and biomass production to enhance the overall performances of the integrated process. 2. Materials and methods 2.1. Landfill leachate sample Biological effluent of LL used in the study was collected from Fengsheng Environmental Protection Co., Ltd. located at Chongqing, China. The detailed physico-chemical parameters were presented in Table 1. The untreated LL contained 733.7 ± 60.0 mg/L of COD, 157.8 ± 11.8 mg/L of NH þ 292.8 ± 20.8 mg/L of NO and 3 4, 3 22.1 ± 1.0 mg/L of PO4 . Besides, the chromaticity and pH were also detected as 1400 ± 200 PteCo and 8.63, respectively. 2.2. Microalgae strain and pre-cultivation The microalgae strain Scenedesmus obliquus adopted in this study was acquired from the Institute of Hydrobiology, Chinese Academy of Sciences (Wuhan, China). The Scenedesmus sp. was selected mainly because that it is easy to settle, which is conducive for microalgae biofilm cultivation. The microalgae strain was precultivated in BG-11 medium according to the previous study (Chang et al., 2018). 2.3. Experimental setup and operation The ozonization treatment of the LL was conducted in a column reactor equipped with an ozone generator (HB03-30, Beijing 322 Water Equipment Co., Ltd., China), as shown is Fig. 1. To ensure full reaction between ozone and macromolecular organics in the LL, a gas-liquid mixing pump (250Y-2DS, Southern Pump Industry Co., Ltd., China) was used in the system to trigger force mixing. During ozonation, 8 L of raw LL was injected into the reactor and ozone with a concentration of 45 mg/L was bubbled into the reactor from the bottom at flow rate of 3 L/min. The operating temperature and pressure of the reactor were set to 25  C and 0.25 MPa. Sampling analysis was conducted at 5 min intervals to monitor the variations of the LL properties during ozonization. The process of microalgae biofilm cultivation for oxidized LL phycoremediation and biomass production was conducted in a rectangular tank made of transparent polymethyl methacrylate (520
200
60 mm, L x W x H) and covered with a transparent glass plate. As shown in Fig. 1, to avoid experimental error caused by sampling, the tank was divided into 6 independent cultivation chambers (60
200
45 mm, L x W x H) and microalgae biofilm Table 1 Physicochemical parameters of leachate in this study. Parameter

Value

COD (mg/L) NHþ 4 (mg/L) NO 3 (mg/L)

733.7 ± 60.0 157.8 ± 11.8

PO3 4 (mg/L) Cl(mg/L) chromaticity (PteCo) pH

292.8 ± 20.8 22.1 ± 1.0 4807.5 ± 2.5 1400 ± 200 8.63

Please cite this article as: Quan, X et al., Enhancing microalgae growth and landfill leachate treatment through ozonization, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119182

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Fig. 1. Schematic of integrated ozonization and microalgae bioremediation system.

sample in each chamber was detected in sequence day by day. To facilitate detection and reduce settling time of microalgae biofilm, 0.013 g of microalgae biomass was filtered on micro-filtration membrane with working area of 0.002 m2 to make sure the inoculation density was 6.5 g/m2 for each experimental batch. Then the membrane was fixed in the cultivation chamber and the leachate was pumped into each separated cultivation chamber for microalgae growth. During experiments, 100 mL of leachate was circulated with a peristaltic pump (BT100- 1 L, Longer pump Co. Ltd., Baoding, China) for each cultivation chamber. 6% of CO2 enriched gas was controlled with mass flow controller (D07-7 B, Beijing Sevenstar Flow Co., Ltd., China) and supplied into the microalgae cultivation tank from one side. All experiments were carried out in a light incubator (ZGZ-800C-L, China), where temperature and light intensity were kept constant at 25  C and 12000 lux. During experiments, each sample was conducted in triplicates and all medium was sterilized treatment before microalgae cultivation. 2.4. Analytical method 2.4.1. Nutrients and COD concentration 3 Inorganic anions (NO 3 and PO4 ) concentration in the collected LL samples were detected by ion chromatography (ICS-600, Thermo fisher, USA), and the samples were vacuum filtered through a 0.45 mm microporous filter membrane before detection. COD was detected according to fast digestion spectrophotometry method (Huang et al., 2018). NHþ 4 was analyzed using Nessler’s Reagent Spectrophotometry (Wang et al., 2019). 2.4.2. Chromaticity of the LL Chromaticity value of the LL was determined by platinum-cobalt standard colorimetric method (American Society for Testing Materials ASTM D1209-05, 2011). In detail, the platinum-cobalt standard solution with chromaticity of 500 PteCo was first prepared with the following method. 1.245 g of potassium chloroplatinate and 1.000 g of cobalt chloride were dissolved in 100 ml of deionized water, which was then added with 100 ml of hydrochloric acid and diluted to 1000 ml with deionized water. After then, a series of solution with various given chromaticity values were prepared by diluting certain amount of platinum cobalt standard solution into colorimetric tube with total solution volume of 50 mL. A certain amount of the LL sample was diluted to 50 mL with deionized water, and the chromaticity was determined by comparing with the standard chromaticity series. The chromaticity value of LL was calculated according to Eq. (1).

P
50 Chromaticity ðPt  CoÞ ¼ Q

(1)

where P and Q represent the chromaticity of platinum-cobalt standard color series and volume of LL sample, respectively.

3

2.4.3. Macromolecular organics concentration Macromolecular organics in LL were determined by UV-254 and gas chromatography-mass spectrometry (Shimadzu GC/MSQP2010 Plus, Japan). UV-254 was measured with double-beam ultravioletevisible spectrophotometer (TU-1901, Beijing, China) to reflect the content of humic organics in LL sample, like aromatic with C]C double bonds and C]O double bonds. The species of macromolecular organics in LL were determined with GC/MS. Before detection, macromolecular organics contained in LL sample was successively extracted with dichloromethane under acidic, neutral and alkaline conditions. Extraction under each condition was conducted in triplicate and 30 mL of dichloromethane was used as extraction phase for each time. Then the extract was concentrated to about 3 mL by rotary evaporators (RE-52, Shanghai, China) at 40  C for GC-MS analysis. Organics concentration contained in LL was calculated according to Eq. (2) based on organics species and relative percentage detected by GC/MS. Corganic (mg/L) ¼ CCOD
corganic

(2)

where Corganic (mg/L) denotes concentration of a specific type of organic, CCOD (mg/L) denotes concentration of COD and corganic denotes relative percentage of the type of organic according to the result by MC/MS. 2.4.4. Chlorophyll content Chlorophyll in Scenedesmus obliquus cells was extracted with the mixed solution of DMSO/80% acetone (1/2, v/v) according to the method by Liao et al. (2018). Before extraction, biofilm was washed three times with deionized water and then resuspended to 50 mL of water. Optical density of the extract at wavelength of 645 nm and 663 nm was detected with a double-beam ultravioletevisible spectrophotometer. The detected optical density was converted to chlorophyll concentration according to Eq. (3), where Cchl is the concentration of chlorophyll and M is dilution multiple of extract. Then the chlorophyll concentration is converted into the areal chlorophyll density (Achl) according to Eq. (4).

Cchl ðmg=LÞ ¼ ð20:20A645 þ 8:02A663 Þ
M Achl ðg=m2 Þ ¼

Cchl
0:05 0:002
1000

(3) (4)

2.4.5. Determination of Scenedesmus obliquus growth Areal biofilm density of Scenedesmus obliquus was determined with gravimetric method. In detail, the collected microalgae biomass was washed three times with deionized water and dried at 85  C to a constant weight. The growth rate G (g/m2/d) of microalgae biofilm was calculated according to Eq. (5), where X2 (g/m2) and X1 (g/m2) denote the areal biomass density at times t2 (d) and t1 (d), respectively.

Gðg=m2 =dÞ ¼

X2  X1 t2  t1

(5)

3. Results and discussion 3.1. Effects of ozonization on LL physical-chemical properties To investigate the effects of ozonization on LL properties, vari ations of NH þ 4 and NO3 concentration, COD concentration,

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absorbency and chromaticity of the LL were measured every 5 min and results were shown in Fig. 2. It can be observed that the COD concentration and chromaticity of the LL were significantly influenced by ozonation, leading to sharply reduced COD and chromaticity values in the first 45 min (Fig. 2(a) and (b)). But the ozonization pretreatment had no obvious effects on removal of  inorganic salts in the LL, with almost unchanged NH þ 4 and NO3 concentrations during ozonization (Fig. 2(d)). As shown in Fig. 2(a), the COD concentration in the LL was reduced from 733.7 mg/L at initial to 354.5 mg/L at 45 min, which was reduced by 51.7%. The removed COD was mainly degraded by the ozone oxidation, which had strong oxidizing capacity to chemical bonds of the organics. After 45 min, the COD concentration decreased little when the LL was further ozonized. It was probably because that the organics which were easy to be decomposed had been degraded mostly by ozone in the first 45 min. Another possible explanation proposed by researchers was that some intermediates were formed in the LL during organics ozonization and these intermediates could not be oxidized easily, and thus prevented the following ozonization process (Wang and Bai, 2017). Similar to COD, chromaticity of the LL first decreased rapidly from 1400 (PteCo) to 45 (PteCo) within 45 min and then slowly decreased to 10 (PteCo) at 55 min (Fig. 2(b)). It was reported that chromaticity of the LL was mainly caused by humic acids and unsaturated aromatic organics with chromophores such as C]C or C]O double bonds (Cheng et al., 2018). The decrease of the chromaticity was mainly because of structure destruction of these

unsaturated bonds in chromophores attributing to ozone attack. According to previous literatures, absorbency of ultraviolet light at 254 nm (UV254) was usually used to reflect the content of aromatic organics and organic compounds with unsaturated double bonds in liquid (Vakilabadi et al., 2017). Therefore, UVevis spectra (Fig. 2(c)) and UV254 (Fig. 2(b)) of the oxidized LL were measured to quantitatively describe the variations of chromophores organics concentration, like humic acids and unsaturated aromatic organics. As results, absorbency of UV254 monotonously decreased along with the ozonization time and fit well with the trend of chromaticity, demonstrating that ozonization pretreatment substantially reduced chromaticity of the LL by destroying unsaturated bonds in chromophores of the humic acids or unsaturated aromatic organics.  In contrast to COD and chromaticity, NH þ 4 and NO3 concentrations in the LL changed little during ozonization, with value of ca.  160 mg/L for NH þ 4 and ca. 300 mg/L for NO3 throughout the ozonization process, demonstrating that ozonization had no obvious  effects on NH þ 4 and NO3 removal. It is because that for protonated þ amine (NH 4 ), the reduced nucleophilicity toward ozone usually lead to a very low oxidation rate (with rate constant of kO3 ¼ 20 M1s1) (von Gunten, 2003), making the ozone can hardly reacts with NHþ 4 . The oxidation potential provided by ozone in this work was not able to destroy that electron pair on NH þ 4 and thus had little effect on NH þ 4 removal from LL. At the same time, it can be concluded that ozone was the predominant oxidizing agents in the experiments instead of the OH, since the energy provided by OH was capable to destroy NH þ 4 (Nawrocki and Kasprzyk-Hordern,

 Fig. 2. Variations of (a) COD concentration, (b) UV254 and chromaticity, (c) UVevis spectra and (d) NH þ 4 and NO3 concentration of the LL during ozonation.

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2010; Wang et al., 2017) but the NHþ 4 concentration in the LL was unchanged in the study. It is observed that NO 3 concentration in the LL also changed little during ozonization. This demonstrated  that the oxidation conversion reaction from NH þ 4 to NO3 during ozonization, which was reported as a possible path according to Chen et al. (2018), did not occure in this experiment since NH þ 4 and NO 3 concentrations were basically stable. Besides, the species of major macromolecular organics in the untreated LL and the oxidized LL were investigated with GC-MS, as shown in Fig. 3 and Table 2. The sample at ozonation time of 45 min was chosen because that the COD and chromaticity in the LL at 45 min was overall stable. In Fig. 3 and Table 2, only the macromolecular organics with credibility of 60% was separately listed and the organics with credibility of lower than 60% was counted into the category of other. Fig. 3 shows that 45 min of ozonization greatly reduced the content of macromolecular organics from 93.3% to 54.8%. In addition, the species of macromolecular organics (60% of credibility) was also significantly reduced from 29 in the untreated LL to 3 in the oxidized LL. As seen in Table 2, the top three macromolecular organics with credibility of 60% in the untreated LL were cyclohexasiloxane dodecamethyl (30.0 mg/L), chloroiodomethane (17.1 mg/L) and diethyl carbitol (9.6 mg/L). While, only three species of organics with credibility of 60% were detected in the oxidized LL, which were dibutyl phthalate (18.1 mg/L), cyclotridecane (3.8 mg/L) and phenol-4, 4ʹ-(1-methylethylidene)bis(0.9 mg/L). Other organics with credibility of <60% in the LL were also greatly degraded by ozonization from 557.8 mg/L in the untreated LL to 171.3 mg/L in the oxidized LL, reduced by 69.3%. The reduced macromolecular organics profile and chromaticity in the oxidized LL provided a more appropriate environment for microalgae growth.

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3.2. Effects of ozonization on microalgae scenedesmus sp. growth and nutrients removal Physico-chemical parameters of LL before and after ozonization were investigated in the former section. Obviously, abundant inorganic nutrients (ammonium and nitrate) contained in the leachate could hardly be removed by ozone, but they were potential nutrients for microalgae growth. In the work, untreated and oxidized LL were used as culture medium for microalgae Scenedesmus sp. biofilm growth and results were shown in Fig. 4. It can be seen that microalgae cultivated with oxidized LL had a shorter adaption phase and higher maximum biofilm density (18.9 ± 0.4 g/ m2) than that in the untreated LL with maximum biofilm density of 12.7 ± 0.6 g/m2. The enhanced microalgae growth profile in the oxidized LL triggered nutrients assimilation by microalgae cells and led to much higher nitrogen removal when comparing with the untreated LL (Fig. 5 and Table 3). Fig. 4(a) shows that microalgae in untreated LL grew slowly in the first two days, with biofilm density increased from 6.5 g/m2 to 7.4 g/m2, increasing by only 0.9 g/m2. However, the biofilm density in the oxidized LL increased rapidly to 10.0 g/m2 at day two, which increased by 3.5 g/m2 and was about three times higher than the case in the untreated LL. The shorter adaption phase of microalgae biofilm in the oxidized LL could be attributed to the mild cultivation environment with less macromolecular organics and low chromaticity, as discussed before. It is known that microalgae cells are weak when they are initially inoculated into a new medium, and microalgae need a period to adapt to the new environment, which is called adaption phase. But the adaption phase is desired to be as short as possible for efficient microalgae biomass production. In this work, the existence of vast macromolecular organics (Figs. 2

Fig. 3. Variations of macromolecular organic in LL before and after ozonation under the condition of 45 mg O3/L for 45 min at a flow rate of 3 L/min.

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Table 2 Macromolecular organics in the LL before and after ozonation under the condition of 45 mg O3/L for 45 min at a flow rate of 3 L/min. Serial number

Major organics in untreated LL

Content (%)

Concentration (mg/L)

Credibility Organics in LL after ozonation for Content (%) 45 min (%)

Concentration (mg/L)

Credibility (%)

1 2 3

2-Pentene, 3,4-dimethyl-, (E)Chloroiodomethane Diethyl carbitol

1.114% 2.329% 1.305%

8.2 17.1 9.6

78 78 80

1.058% 5.114% 0.243%

3.8 18.1 0.9

86 90 74

4 5 6 7 8 9 10 11 12 13 14 15

Cyclohexasiloxane, dodecamethyl3-Methyl-3-isopropyldiaziridine Pentadecane Propanoic acid Chloromethyl cyanide Hexadecane Hexanal, 2-ethyl(R)-(þ)-3-Methylcyclopentanone Octadecane Benzene, (2,2-dimethoxyethyl)1,4-Dioxane-2,5-dione, 3,6-dimethyl1,4-Dioxane-2,5-dione, 3,6-dimethyl-, (3 S-ci Cyclopentane, methyl1-Heptene, 2,6-dimethyl2-Ethylthiolane, S,S-dioxide Phenol, 2,4-bis(1,1-dimethylethyl)Methamphetamine acetylated Nikethamide 1,3,5-Triazine-2,4,6(1H,3H,5H)-trione, 1,3,5-tri Urea, triethylnitrosoCarbamic acid, ethyl-, methyl ester Aminorex n-Butyl methacrylate Tri (2-chloroethyl) phosphate Octadecanoic acid 6-Octadecenoic acid, (Z)Other

4.086% 0.996% 0.694% 0.540% 0.700% 0.477% 0.592% 0.067% 0.295% 0.203% 0.158% 0.439%

30.0 7.3 5.1 4.0 5.1 3.5 4.4 0.5 2.2 1.5 1.2 3.2

90 83 64 83 78 72 72 89 72 72 96 78

48.400%

171.3

<60

0.139% 0.211% 0.145% 0.346% 0.171% 0.223% 0.237%

1.0 1.6 1.1 2.5 1.3 1.6 1.7

96 64 64 97 95 72 72

0.254% 0.116% 0.242% 0.312% 0.071% 0.175% 0.099% 76.60%

1.9 0.9 1.8 2.3 0.5 1.3 0.7 557.8

72 90 64 95 97 72 98 <60

16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

and 3 and Table 2) and high chromaticity (1400 PteCo, Fig. 2) in the untreated LL hindered microalgae growth and prolonged the adaption phase. For instance, high chromaticity of the untreated LL was not conducive to light transfer in the culture medium and hindered microalgae photosynthesis, which could be verified by the lower chlorophyll concentration in microalgae biofilm than that in the oxidized LL (Fig. 4(c)). As results, the growth rate in the untreated LL was much low, with values of 0.25 g/m2/d at day one and 0.65 g/m2/d at day two (Fig. 4(b)), resulting in poor biofilm density of 7.4 g/m2 at day two. Comparing with the untreated LL, chromaticity and macromolecular organics in the oxidized LL were mostly removed by ozonization (Figs. 2 and 3). It resulted in much higher microalgae growth rate, which were 1.00 g/m2/d at day one and 3.05 g/m2/d at day two (Fig. 4(b)) and led to a much higher biofilm density of 10.0 g/m2 at day two (Fig. 4(a)), increasing by more than three times than that in the untreated LL. After two days, the biofilm in both cases exhibited good growth trends with linear increase of biofilm density, but the biofilm density in the untreated LL was lower than that in the oxidized LL throughout the cultivation process. The maximum growth rate in the oxidized LL was 4.7 g/m2/d while the value was only 3.3 g/m2/ d for the untreated LL. The higher growth rate of microalgae in the oxidized LL led to a great improvement of the maximum biofilm density from 12.7 g/m2 in the untreated LL to 18.9 g/m2 in the oxidized LL (Fig. 4 (a)). The robust microalgae growth in the oxidized LL also enhanced removal of inorganics and organics. As  shown in Table 3, removal efficiencies of COD, NH þ 4 and NO3 in the oxidized LL were improved by 113.4%, 58.4% and 60.5% comparing with that in the untreated LL. Fig. 5 shows that there was little  difference on NHþ 4 and NO3 between the untreated LL and the oxidized LL in the first three days. After the third day, the NH þ 4 and

CyclotridecaneDibutyl phthalate Phenol,4,4’-(1-methylethylidene) bisOther

NO 3 concentration in the oxidized LL were further reduced to a great extent, while they were almost unchanged for the untreated LL. It was probably because that poor microalgae growth in untreated LL after three days decreased the nutrients requirements by microalgae growth and metabolism. It is worth mentioning that microalgae biofilm possibly grew under mixotrophic mode attributing to direct contact of microalgae cells with LL. This can be verified by Fig. 5 and Table 3 that both COD and inorganic salts were removed by microalgae cultivation. However, it can be seen from Table 3 that COD removal efficiencies in untreated LL and oxidized LL were only 27.6% and 59.1%, respectively. It demonstrated that a large quantity of residual organics was remained in the LL, which was likely nonbiodegradable. Besides, there were large amounts of residual ammonium (37.1 mg/ L) and nitrate (192.0 mg/L) in the oxidized LL at final time of microalgae cultivation, but the phosphorus was already exhausted at day two. This suggested that phosphorus was insufficient in the oxidized LL, which limited microalgae growth and nitrogen removal. 3.3. Effect of phosphorus feeding on microalgae growth and nitrogen removal Phosphorus plays an important role on microalgae Scenedesmus sp. growth. In detail, adequate phosphorus in culture medium can enhance microalgae growth and nitrogen removal from the LL. Considering the scarce phosphorus in the LL (Table 1 and Fig. 5), additional phosphorus was added to the oxidized LL to obtain different N/P molar ratio of 33:1, 16:1; 7:1 and 3:1. Microalgae biofilm growth under different N/P ratio was presented in Fig. 6. In general, microalgae biofilm density in experimental groups with P

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(a)

(b)

(c) Fig. 4. Growth profile of Scenedesmus sp. in the untreated LL and in the oxidized LL. In specific, (a)biofilm growth curve, (b) growth rate and (C) chlorophyll concentration of microalgae biofilm in the untreated LL and in the oxidized LL.

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(a)

(b)

(c)  3 Fig. 5. Variations of (a) NHþ 4 , (b) NO3 and (c) PO4 concentration in the untreated LL and the oxidized LL.

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Table 3 Nutrients and COD removed amount and removal efficiencies in untreated LL and oxidized LL.

COD NH þ 4 NO 3 COD NH þ 4 NO 3

removed amount (mg/L) removed amount (mg/L) removed amount (mg/L) removal efficiency (%) removal efficiency (%) removal efficiency (%)

Untreated LL

Oxidized LL

202.3 76.1

433.6 120.7

62.8 27.6 48.2

100.8 59.1 76.5

21.4

34.5

feeding were overwhelmingly higher than the biofilm density in control group with no additional P feeding, demonstrating that more P nutrients in the LL substantially enhanced microalgae growth. However, excess P adding in the leachate under N/P ratio of 7:1 and 3:1 presented inhibiting effects on microalgae growth, resulting in slight decrease of biofilm density comparing with the maximal biofilm density of 28.0 g/m2 under N/P ratio of 16:1. In accordance with microalgae biofilm density, the maximal COD removal efficiency of 64.3% and nitrogen removal efficiency of 81.6% were obtained under N/P ratio of 16:1 (Table 4). Fig. 6(a) shows that there was little difference on microalgae biofilm density between control group and experimental groups with various N/P ratio in the first three days, but the biofilm density in the control group at day four and day five were much lower than that in the experimental groups. It was because that phosphorus was sufficient for all batches in the first three days (Figs. 5(c) and Fig. 6(c)), leading to similar growth trends between control group and experimental groups. However, P was totally used up for the control group after the third day, as shown in Fig. 5(c), resulting in limiting effect on microalgae growth. The possible reason for limiting effects caused by P scarce was that P availability in culture medium was closely associated with microalgae intracellular energy transduction (Chu et al., 2014). Insufficient P nutrients in the control group reduced the production and transduction of metabolic energy, leading to slower microalgae growth rate than experimental groups. As a result, the maximum biofilm density of the control group was 18.9 g/m2. Comparing with the control group, additional P feeding ensured the P availability in leachate. As shown in Fig. 6(c), P was totally used up at the third day for the control group, but P was exhausted at day four for N/P ratio of 33:1 and at day five for 16:1. More sufficient P nutrients enhanced the maximum microalgae biofilm density to 27.6 g/m2 and 28.0 g/m2, which was ca. 48.0% higher than that in the control group. But when further more P was added to the LL, denoting that the N/P ratios decreased to 7:1 and 3:1, the maximum biofilm density was slightly reduced to 27.3 g/m2 and 25.6 g/m2. It suggested that excess P feeding in the LL caused a minor inhibiting effect on microalgae growth, which could be attributed to P-toxicity effect caused by P over-assimilation. Intracellular carbon flow was induced to store energy-related macromolecule (like lipid) instead of biomass.

(a)

(b)

Table 4 Nutrients and COD removed amount and removal efficiencies in the different N/P ratio. N/P molar ratio

COD removed amount (mg/L) N removed amount (mg N/L) P removed amount (mg P/L) COD removal efficiency (%) N removal efficiency (%) P removal efficiency (%)

Control

3/1

7/1

16/1

33/1

433.6 116.6 7.2 59.1 61.8 100

395.6 117.6 116.6 53.9 61.9 79.4

418.1 136.4 64.5 57.0 71.8 96.3

471.6 155.1 33.5 64.3 81.6 100

460.4 138.9 19.9 62.8 73.1 100

(c) Fig. 6. Effect of phosphorus feeding on (a)biofilm growth curve, (b)N concentration and (c) P concentration in the oxidized LL.

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Table 5 Performance comparisons of various wastewater treatment methods. Approach

Wastewater type

Nitrogen removal (%)

Phosphorus removal (%)

Biofilm density (g/ m2)

Reference

ozonization

Drink

0

e

e

microbubble catalytic ozonization and biological process ozonization/autotrophic nitrogen/activated carbon ozonization/Fe2þ-BAF microalgae (C. vulgaris) ozonization/microalgae (C. vulgaris)

bio-treated coal chemical wastewater Landfill leachate petrochemical secondary effluent Hog manure Landfill leachate

52.9

e

e

von Gunten (2003) Liu et al. (2018)

93.8 e 69.55 81.6

e 77.1 64.40 100

e e 7.37 28.0

Gao et al. (2015) Wu et al. (2017) Wu et al. (2019) This work

Variations of nitrogen and COD removal were illustrated in Fig. 6(b) and Table 4. It was shown that the removal of nitrogen and COD was consistent with the trend of maximum microalgae biofilm, which first increased and then decreased with the decrease of N/P ratio. The Optimum nitrogen and COD removal efficiencies were achieved as 81.6% and 64.3% under N/P ratio of 16:1. There was little difference on COD removal efficiency between control group and experimental groups under various N/P ratios, which was possibly because that the residual organics in the oxidized LL were mainly nonbiodegradable matters and additional P feeding had little effects on enhancement of COD removal. While the nitrogen removal efficiency was significantly improved from 61.5% in the control group to 81.6% in experimental group with N/P ratio of 16:1 (Table 4). It was because that nitrogen assimilation and conversion process by microalgae cells mainly experienced three steps, i.e. (1) nitrogen transport across cytomembrane from the leachate to inside of the cell, (2) reduction of nitrate to ammonium catalyzed by successive action of nitrate and nitrite reductase, and (3) incorporation of ammonium into intracellular component, like protein and chlorophyll, in which step 2 and step 3 are energy consuming (Vega et al. (1991)). Phosphorus is closely associated with energy production and transduction in the microalgae cell, and additional P feeding provided more sufficient energy for nitrogen metabolism, which enhanced nitrogen removal and resulted in higher nitrogen removal efficiency especially under N/P ratio of 16:1. To evaluate the performance of the proposed method, main parameters including nitrogen removal, phosphorus removal and biofilm density were compared with the previous studies and techno-economic of the proposed method was conducted. As shown in Table 5, it was reported that ozonization alone had no effect on ammonia nitrogen removal attributing to the very low reaction rate of k ¼ 20 M1s1 between ozone and ammonia nitrogen (von Gunten, 2003). To remove nitrogen or phosphorus from wastewater, ozone-based integrated process was proposed. Liu et al. (2018) proposed an integrated technique of microbubble catalytic ozonation and biological process. But removal efficiency of nitrogen was poor, with the maximum nitrogen removal efficiency of 52.9% for the integrated system. To improve inorganic salts removal, Gao et al. (2015) proposed an ozonization/autotrophic nitrogen/activated carbon technique with the highest removal efficiency of 93.8% for nitrogen. Wu et al. (2017) constructed an integrated technique containing ozonization/Fe2þ and biological aerated filter (ozonization/Fe2þ-BAF) and found that 77.1% of phosphorus was removed. But the aforementioned methods mainly focused on nitrogen and phosphorus removal from wastewater stream and paid little attention on nutrients reclamation. It led to resources waste and reduce the economic efficiency. To reclaim nutrients from wastewater for bioresource production, Wu et al. (2019) obtained a maximum microalgae biofilm density of 7.37 g/ m2 in hog manure and removed 69.55% of nitrogen and 64.40% of phosphorus from the wastewater stream. Obviously, microalgae

showed a promising strategy for wastewater treatment since it achieved dual function of wastewater treatment and bioresource production, significantly enhancing economic efficiency than the methods without nutrients recycling. But toxicity and chromaticity of wastewater seriously limited microalgae growth, leading to poor nutrients removal and biomass production. To realize highefficiency LL treatment and nutrients reclamation, the integrated technique containing ozonization and nutrients reclamation with microalgae was proposed in this work and realized high-efficiency COD, nitrogen and phosphorus recycling to produce high-value microalgae-based bioresources (like biolipid and carbohydrates). As results, a maximum nitrogen removal of 81.6% and phosphorus removal of 100% were achieved. Comparing with the biofilm density (7.37 g/m2) reported by Wu et al. (2019), the biofilm density in this work was greatly improved to 28.0 g/m2. The obtained microalgae biomass is superior feedstocks for bioenergy (biolipid, biohydrogen, etc.) production, significantly enhancing economic feasibility when comparing to previous methods. 4. Conclusion LL contained high chromaticity and complex macromolecular organics, which were toxic to microalgae growth. Ozonization under 45 mg O3/L for 45 min greatly reduced the chromaticity from 1400 to 45 PteCo by destructing the chromophores on unsaturated aromatic organics. The complexity and concentration of macromolecular organics in the LL were also sharply reduced via ozonization. As results, microalgae biofilm density was improved from 12.7 g/m2 in untreated LL to 18.9 g/m2 in oxidized LL. By adding additional P nutrients, the biofilm density and nitrogen removal efficiency were further improved to 28.0 g/m2 and 81.6%, which were overwhelming higher than the untreated LL. However, further studies on comprehensive optimization of microalgae growth, nutrients recycling and bioenergy production should be addressed. In addition, outdoor exploration of the integrated technique should be conducted for large-scale application. Declaration of competing interest The authors declare no declaration of interest and the authors don not have any copyright issues with the publication of this article. Acknowledgments The authors are grateful for the financial support provided by the National Natural Science Funds for Young Scholar (No. 51806026), Chongqing Municipal Solid Waste Resource Utilization & Treatment Collaborative Innovation Center (Shljzyh2017-003), National Natural Science Foundation of China (51876018), Foundation and Frontier Research Project of Chongqing of China

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