characteristic changes in algal organic matter derived from microcystis aeruginosa in microbial fuel...

Bioresource Technology xxx (2015) xxx–xxx

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Bioresource Technology

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Characteristic changes in algal organic matter derived from Microcystisaeruginosa in microbial fuel cells

http://dx.doi.org/10.1016/j.biortech.2015.06.0140960-8524/� 2015 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel./fax: +86 451 86282098.E-mail addresses: [email protected], [email protected] (F. Cui).

Please cite this article in press as: Wang, H., et al. Characteristic changes in algal organic matter derived from Microcystis aeruginosa in microbial fuBioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.06.014

Huan Wang a, Lu Lu b, Dongmei Liu a, Fuyi Cui a,⇑, Peng Wang a

a State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, PR Chinab Department of Civil, Environmental, and Architectural Engineering, University of Colorado, Boulder, Boulder, CO 80309, United States

h i g h l i g h t s

� Algal organic matter (AOM) wasdegraded in microbial fuel cells(MFCs).� AOM degradation was more

completely by MFC than byfermentation.� Changes in AOM compositions and

structures during MFC treatmentwere characterized.� Several different methods are used in

AOM characterization.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Received 29 April 2015Received in revised form 3 June 2015Accepted 4 June 2015Available online xxxx

Keywords:Algal organic matter (AOM)Microbial fuel cell (MFC)Molecular weight distributionFluorescence EEM spectroscopyFT-IR spectroscopy

a b s t r a c t

The objective of this study was to investigate behavior of algal organic matter (AOM) during bioelectro-chemical oxidation in microbial fuel cell in terms of compositions and structures. Study revealed that theAOM derived from blue-green algae Microcystis aeruginosa could be degraded more completely (82% CODremoval) in microbial fuel cells (MFCs) than by anaerobic fermentation (24% COD removal) in a controlreactor without closed-circuit electrode and electricity was produced simultaneously. A variety of tech-niques were used to characterize the changes in AOM compositions and structures during bioelectro-chemical oxidation. The presence of syntrophic interactions between electrochemical active bacteriaand fermentative bacteria to degrade large molecular organics into small molecular substances, whichcould be oxidized by electrode but not by fermentation. The dominant tryptophan protein-like sub-stances, humic acid-like substances and Chlorophyll a in AOM were highly degraded during MFCtreatment.

� 2015 Elsevier Ltd. All rights reserved.

1. Introduction

Algae, being rich in lipid, protein and carbohydrate, is consid-ered as a promising biomass energy due to its high growth rates,round year production, high bio-fuel yields, small occupied space,and other benefits (e.g. CO2 capture, wastewater nutrientsremoval) (Mata et al., 2010; Scott et al., 2010). To date, algal

biomass has been mainly used to produce bio-fuels (e.g.bio-diesel and bio-ethanol), methane, and hydrogen via variousphysical, chemical and biological methods (Chisti, 2007; Hiranoet al., 1998; John et al., 2011; Nath and Das, 2004; Singh and Gu,2010).

Microbial fuel cells (MFCs) can directly generate electricity byoxidizing organic compounds with the help of bacterial electro-chemical reactions (Logan et al., 2006). Many new technologieshave recently emerged by integrating MFC with algae for renew-able energy production and wastewater treatment. First, algae

el cells.

http://dx.doi.org/10.1016/j.biortech.2015.06.014

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2 H. Wang et al. / Bioresource Technology xxx (2015) xxx–xxx

biomass including living cell, dry mass, algae residue producedfrom other water/wastewater treatment processes can be directlyused as fuels in MFCs for current production (Kondaveeti et al.,2014; Velasquez-Orta et al., 2009; Wang et al., 2012b). In thisway, pretreatment procedures (e.g. alkaline, heat, and microwave)are normally necessary to dissolve algae cell walls for improve-ment of performance (Gadhamshetty et al., 2013; Xiao and He,2014). Second, algae as phototrophic microorganisms can also beused to supply MFC cathode with oxygen for electron reductionas well as to reduce CO2 and produce valuable biomass simultane-ously (Wang et al., 2010; Xiao and He, 2014). Third, MFC can beintegrated with an algal bioreactor with division of labor forremoval of organics (in MFC) and nutrients (in the algal reactor)from wastewaters as well as bio-energy (electricity and biomass)production (Xiao et al., 2012).

In these algae/MFC systems, algae play a role of fuel or func-tional microorganism to facilitate the reactions in process. In anycase, effluents would be produced and finally enter environment.It is necessary to evaluate their environmental risks before beingdischarged. Because algae biomass has complex chemical composi-tions and cell itself can generate extensive amount of algal organicmatter (AOM), algal toxins, taste and odor compounds with itsmetabolic excretion, decay and autolysis (Henderson et al., 2010;Her et al., 2004). If these compounds can’t be degraded completelyby MFC, they will deteriorate effluents to result in water body pol-lution or affect the performance of subsequent treatment pro-cesses. For example, harmful disinfection byproducts (DBPs) willbe produced after the effluent containing AOMs through tertiarytreatment (e.g. disinfection), and the DBPs toxicity are closelyrelated to the compositions and structures of AOM.Characterization of AOM is necessary to evaluate the risk of efflu-ent discharge. Bioelectricity production from blue-green algae cou-pled algal toxins (MC-RR and MC-LR) removal was achieved in asingle chamber tubular MFC (Yuan et al., 2011). The genotoxicagents in the polluted lake water were almost completely removedin a single-chamber air–cathode MFC (He et al., 2013). Our previ-ous studies showed that precursors of disinfection byproduct (tri-halomethane) were effectively reduced in a two-chamber MFC(Wang et al., 2012a). However, few studies so far have systemati-cally researched on changes in AOM during MFC treatment interms of composition, molecular weight, structures and so on.Hur et al. (2014) have used acidifying dry algae (green algae,Scenedesmus obliquus) powder as MFC substrate to reveal thatAOM compositions would sequentially change with order of pro-teins, acidic functional group, polysaccharides and amino.

This study aimed at examining the changes in the characteris-tics of AOM derived from M. aeruginosa. during MFCs operation,and further exploring the biodegradability of AOM in MFCs. Inaddition, results were compared with those in MFC operated inopen circuit condition, which has not been investigated in previousstudies. Several characterization methods including ultrafiltration,fluorescence EEM spectroscopy, FT-IR spectroscopy and UV–visibleabsorbance were used.

2. Methods

2.1. Preparation of AOM solution

M. aeruginosa (blue-green algae, Collection No. HB909) wereobtained from the Culture Collection of Algae at the Institute ofHydrobiology, Chinese Academy of Sciences, and were grown usingBG11 media in an air-conditioned light incubator at 30 ± 1 �C(GZX-250, Taisite Instruments Inc., China). Algae were extractedon day 33, corresponding to the growth phase of stationary. Thealgae cells in BG11 medium were broken by ultrasound

Please cite this article in press as: Wang, H., et al. Characteristic changes in algaBioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.06.014

(3.5 W/mL) using a sonicator (Sonics Vibracell VCX-130 PB,130 W, 20 kHz) for 20 min at 4 �C. The solution was collected andfiltered through a filter with a pore diameter of 0.45 lm to removethe residual solids. The filtrate was AOM solution including extra-cellular organic matter (EOM) and intracellular organic matter(IOM) with dissolved organic carbon (DOC) of 141 ± 33 mg/L andchemical oxygen demand (COD) of 525 ± 11 mg/L.

2.2. MFC construction and operation

H-type double chambers MFC were constructed as previouslydescribed (Wang et al., 2012a,b). Both the anode and cathodechambers were cuboid (7 cm length � 4.5 cm width � 7 cm height)with a working volume of 200 mL. They were separated by a cationexchange membrane (CEM) (CMI-7000, Membrane InternationalInc., USA) with an effective area of 30.25 cm2. Anode and cathodewere ammonia gas treated graphite brushes (4 cm diame-ter � 4 cm length; fiber: T700–12 K, Toray Industries Co., Ltd.).The distance between anode and cathode was 5 cm. An Ag/AgClreference electrode (+0.2 V versus standard hydrogen electrode)was used to measure the electrode potentials. Two electrodes wereconnected to an external resistor (1 kX) with copper wire.

The MFC anode was inoculated with polluted water obtainedfrom a heavily eutrophic lake. The mixed solution of 50 mL pol-luted water and 150 mL AOM solution containing 50 mM nutrientphosphate buffer (Na2HPO4 4.58 g/L, NaH2PO4�H2O 2.45 g/L, KCl0.13 g/L, and NH4Cl 0.31 g/L) was filled into anode chamber forstart-up. The cathode chamber was filled with same 50 mM phos-phate buffered solution and was continuously aerated at100 mL/min to provide dissolved oxygen as the electron acceptorfor the cathode. Once a voltage of >100 mV was obtained, theinoculum was omitted and replaced by AOM solution. The AOMsolution was replaced when the voltage decreased to <50 mV ineach batch cycle. When a reproducible maximum voltage wasobtained for at five batch cycles, the anode was considered fullyenriched with electrochemically active bacteria (EAB).

A MFC with electrochemically active anode but operated atopen circuit (MFC-OC) was served as a control for studying theeffect of other bacteria, except for electrochemically active bacte-ria, on the biodegradation of AOM in MFC. All tests were conductedin fed-batch mode over more than three batch cycles at room tem-perature (21 ± 2 �C).

2.3. Analysis methods

2.3.1. Chemical analysisDissolved organic carbon (DOC) was measured with a TOC/TN

analyzer (TOC-VCPH/TNM-1, Shimadzu, Japan). Chemical oxygendemand (COD) was measured following standard methods. UV254

was measured by an ultraviolet–visible spectrophotometer(UV-2550, Shimadzu, Japan). Specific ultraviolet absorbance(SUVA) was calculated as (UV254/DOC) � 100. Measurements weremade in triplicate.

2.3.2. Electrochemical analysisVoltage (mV) across a external resistor (1 kX) was automati-

cally recorded using a data acquisition system (2700, KeithleyInstruments Inc., USA) connected to a computer. The open circuitvoltage (OCV) (without a circuit load) was obtained by removingthe external load. Voltage was converted to volumetric power den-sity P (W/m3) via the equation P = UI/Va, where U is the voltage (V),I is the current (A), and Va is the net liquid volume (m3) in theanode chamber. The maximum power density was determinedby varying the external resistance (50 X–100 kX).

l organic matter derived from Microcystis aeruginosa in microbial fuel cells.


H. Wang et al. / Bioresource Technology xxx (2015) xxx–xxx 3

2.3.3. AOM fractionation by ultrafiltrationSamples subjected to molecular weight (MW) were first passed

through a 0.45 lm pore size filter. And then fractionation was con-ducted in an Amicon stirred ultrafiltration cell (Model 8050,Millipore Corp., USA) under a constant nitrogen gas pressure of0.1 MPa, employing filters with MW cutoffs of 10 kDa, 3 kDa,1 kDa and 500 Da (YM10, YM3, YM1, YC05, Millipore Corp., USA).The membranes were rinsed with ultrapure water prior to filtra-tion. Sequential ultrafiltration was performed according to thestudy (Hua and Reckhow, 2007). After ultrafiltration separation,the filtrates were analyzed for DOC.

2.3.4. FT-IR spectroscopy analysisLyophilized AOM powder (2–5 mg) was mixed thoroughly with

about 100 mg desiccated KBr under infrared radiation. The mixturewas pressed into a tablet and its infrared spectrum was recordedon a Perkin-Elmer Spectrum One B Fourier Transform Infraredspectrometer (Waltham, MA, USA). The FT-IR spectra wereobtained in a wavenumber range of 4000–400 cm�1, and spectrawere baseline corrected and normalized to 1.0 for the purpose ofcomparison.

2.3.5. Fluorescence spectroscopy analysisFluorescence excitation–emission matrix (EEM) spectroscopy

was measured using a luminescence spectrometry (FP-6500,Jasco, Japan) in a 1 cm quartz cell. Filtered water samples werediluted by more than 15 times in this case to neglect the inner fil-tering effect. The EEM spectra were obtained by scanning the sam-ple over excitation wavelengths from 220 to 700 nm with 5 nmsteps and emission wavelengths from 220 to 750 nm with 2 nmsteps. And the scanning speed was set at 1000 nm/min for all themeasurements (Lu et al., 2012a). The spectrum of Milli-Q waterwas recorded as blank and the equipment was auto-zeroed priorto analysis.

1

Fig. 1. Molecular weight (MW) distributions of AOM in influent as well as effluentfrom MFCs with closed circuit (MFC-CC) and open circuit (MFC-OC).

3. Results and discussion

3.1. Electricity generated from AOM

After 25 days of start-up, AOM derived from M. aeruginosa witha COD of 525 ± 11 mg/L was fed into the MFC. A maximum voltageof 580 ± 10 mV (1000 X resistor) and the stable voltage around520 mV were obtained during each batch cycle with operating per-iod of around 2 days. The maximum volumetric power densitieswas 4.2 ± 0.1 W/m3. The total COD removal rates were 82 ± 5%and 24 ± 3% for MFC working at closed circuit (MFC-CC) and MFCworking at open circuit (MFC-OC), respectively. The COD removalin MFC-CC was more than the triple of that in MFC-OC, suggestingthe role of electrochemically active bacteria (EAB) in the degrada-tion of AOM. Previous studies have showed that syntrophic inter-actions between different microbial consortia were associatedwith degradation of complex organic matter (Lu et al., 2012b), thatis, large molecular organics (e.g. carbonhydrates, lipid and protein)in AOM were firstly decomposed by fermentative microbes to pro-duce volatile fatty acids, small molecular amino acids and alcohol,which then subsequently oxidized by EAB for current production.On the other hand, the electrochemical oxidation of these smallmolecular organics will facilitate the conversion and degradationof large molecular AOM. In MFC with open circuit, the fermentativeorganic products can’t be consumed by EAB, resulting in low CODremoval.


3.2. Effect of bioelectrochemical oxidation on MW distributions of AOM

The changes in molecular weight (MW) distributions of theAOM after MFC treatment were demonstrated in Fig. 1. For influ-ent, the large molecular AOM with MW >10 kDa was the dominantfractions (35.5%), while fractions with MW 3–10 kDa, 1–3 kDa and<1 kDa were accounted for 19.6%, 28.6% and 16.3% of total AOM,respectively. After bioelectrochemical oxidation in MFC withclosed-circuit, the factions of AOM with MW >10 kDa and 1–3 kDa decreased to 20.4% and 19.8%, respectively, resulting smallmolecular fractions (MW <1 kDa) significantly increased to 33.6%,which was almost twice of that in influent. The MW 3–10 kDa frac-tions slightly increased from 19.6% to 26.2%, part of them should beaccumulated products produced by degradation of AOM fractionswith MW >10 kDa. The similar trend of AOM changes was observedin MFC with open circuit, but less large molecular fractions (MW>10 kDa) were degraded and produced less MW <1 kDa fractions.These results supported the fact that presence of microbial syn-trophic interactions in MFC to facilitate the degradation of complexAOM. These low MW (<1 kDa) fractions may consist of intermedi-ate products of AOM degradation (e.g. amino acids, organic acidsand simple sugars) (Confer and Logan, 1997) and soluble micro-bial products (SMPs) derived from microorganism metabolismsand biomass decay, such as humic acids, antibiotics and extracellu-lar enzymes (Barker and Stuckey, 1999). In addition, the organicsMW distributions can be affected by operation conditions. Forexample, the small MW fractions derived from AOM degradationand SMPs could aggregate into larger MW substances again overa longer operating time (Barker and Stuckey, 1999). Furtherresearches should focus on optimizing operation condition toreduce production of organic factions that prone to subsequentproduction of more harmful materials, such as nitrogenous disin-fection byproducts (N-DBPs).

3.3. FT-IR spectra characterize structure changes of AOM afterbioelectrochemical oxidation

The information of functional groups and special molecularstructures can be obtained by FT-IR spectroscopic analysis. Theinterpretations of the functional groups corresponding to theabsorption bands are listed in Table S1 in Supplementary materials(Jiang et al., 2010; Matilainen et al., 2011).

As shown in Fig. S1, strong peaks at 2920–2850 cm�1,1442 cm�1 and 884 cm�1 were all present in the spectrum of influ-ent, indicating the abundance of hydrocarbons in influent. Influentalso contained a significant aromatic C@C peak at 1635 cm�,




indicating presence of aromatic compounds. In addition, the exis-tence of C–O function group in influent was indicated by the peakat 1146 cm�1. The main change after treatment by MFC with orwithout closed circuit was the decrease of peaks number, agreeingwith the organics removal in these reactors. The peak at1442 cm�1 disappeared in the spectra of both effluents, suggestinga prioritized removal of C–H function group by the electrochemicaloxidation in MFC-CC and anaerobic bio-degradation in MFC-OC. Onthe other hand, the effluent of MFC-OC significantly increased theabsorbance of C–O function group at 1078 cm�1 and newly gener-ated O–H vibration of carboxylic group at 1403 cm�1, indicatingthe production of intermediate products such as alcohols, ethers

Fig. 2. Fluorescence EEM spectra of AOM in (a) influent as well as effluent fromMFCs with (b) closed circuit (MFC-CC) and (c) open circuit (MFC-OC).

Table 1Fluorescence EEM spectral parameters of AOM in influent as well as effluent from MFCs withto neglect the inner filtering effect.

Concentration(mg/L-DOC)

SUVA(L/mg�m)

Peaks in Region IEx/Em (Intensity)

Influent 7.32 1.49 300/340 (819), 240/340 (587)Effluent MFC-CC 1.64 0.73 285/340 (211), 230/336 (152)Effluent MFC-OC 5.66 1.20 280/338 (684), 225/336 (482)

SUVA: Specific ultraviolet light absorbance (SUVA) calculated as (UV254/DOC) � 100.


and small molecular carbohydrates. However, this new peak at1403 cm�1 was not found in the effluent of MFC-CC, indicating thata portion of newly generated byproducts could be utilized by elec-trochemical oxidation in MFC-CC. In addition, the peak at1658 cm�1 (C@O amide 1) emerged in the effluent of MFC-CC, sug-gesting the degradation of protein during electrochemical oxidation.

3.4. Fluorescence EEM spectra characterize AOM compositions

3.4.1. Changes in EEM spectra at the end of bioelectrochemicaloxidation

The fluorescence EEM spectra of AOM in influent and effluentsfrom MFC-CC and MFC-OC at the end of MFC treatment wereshown in Fig. 2. EEM spectra were divided in three regions for thisstudy by defining emission boundaries. Rayleigh scatters appearingin the EEM as diagonal lines should be ignored during the spectruminterpretation. The region I at an emission wavelengths of 220–380 nm belongs to the protein-like organic compounds. Otherresearchers have subdivided this region into two sub-regions cor-responding to tryptophan protein-like substances with excitationwavelengths greater than 250 nm (Peak T1) and aromatic proteinswith excitation wavelengths less than 250 nm (Peak T2) throughanalysis with the pure compound in water (Chen et al., 2003).The region II in the EEM is assigned to the humic-like fluorescencewith peaks generally located at emission wavelength of 470 nm.Region II is also separated into two sub-regions according to exci-tation wavelengths. The excitation wavelengths below 250 nm arerelated to fulvic-like substances, and the excitation wavelengthsabove 250 nm are related to humic acid-like substances(Ziegmann et al., 2010). The region III at longer emission wave-lengths (600–750 nm) is assigned to pigments, and it mainly refersto chlorophyll a derived from algae at a 673 nm emission wave-length in this study (Her et al., 2004; Ziegmann et al., 2010).

The peak locations with excitation and emission wavelengths(Ex/Em) and peak intensities were presented in Table 1. The peaksin region I have the highest fluorescence intensities compared tothose in other regions for both influent and effluents, indicatingthe protein-like organic matter are the major components inAOM. The organic matter concentrations are positively correlatedwith the fluorescence intensities if inner filtering effect could beeliminated by appropriately diluting the samples. Compared toinfluent, the fluorescence intensities of peaks in region I werefound to reduce by about 75% in effluent of MFC-CC, while therewas only slight decrease in MFC-OC effluent. This demonstratedthat protein-like substances were efficiently removed by bioelec-trochemical oxidation based on spectral method, which was con-sistent with results by chemical analysis. Interestingly, thelocation of peak T1 and peak T2 in region I were all blue shifted10–20 nm in both effluents. Previous study has showed that a blueshift was associated with the production of small MW components(Coble, 1996), agreeing with the increase of MW <1 kDa fractionsin effluents. The parameter of SUVA is related to amount of aro-matic substances, and the reduction of SUVA in effluents(Table 1) demonstrated the decrease of aromatic constituents or

closed circuit (MFC-CC) and open circuit (MFC-OC). Samples were diluted in EEM test

Peaks in Region IIEx/Em (Intensity)

Peaks in Region IIIEx/Em (Intensity)

380/450 (47), 265/440 (61) 615/632 (379), 300/676 (71), 240/674 (50)Non detectable 290/660 (20)385/446 (148), 265/444 (146) 615/630 (167), 280/644 (41), 225/644 (32)



Fig. 3. Changes in fluorescence EEM spectra of AOM during bioelectrochemical oxidation in closed-circuit MFCs with time.

Fig. 4. Changes in fluorescence intensities of T1 and T2 peaks during bioelectro-chemical oxidation in closed-circuit MFCs with time. (T1: Ex/Em = 220–250/300–380 nm; T2: Ex/Em = 250–300/300–400 nm).

H. Wang et al. / Bioresource Technology xxx (2015) xxx–xxx 5

the changes of substance structure (Coble, 1996). The peaks inregion II were found in the influent, however, they disappearedin the effluent of MFC-CC and became more intensive in MFC-OCeffluent, suggesting humic acid-like substances produced during


anaerobic degradation of AOM could be oxidized by using elec-trode as electron acceptors in MFC. Chlorophyll a in region III couldalso be removed in MFC-CC demonstrated by reduction of peaknumbers and intensities, but this degradation was not obvious inMFC-OC.

3.4.2. Changes in EEM spectra during bioelectrochemical oxidation inMFC-CC

In practical, the changes of AOM components in MFC with timecan be easily and timely presented by fluorescence EEM spectradue to its high sensitivity, good selectivity and onlinedetection (Sheng and Yu, 2006). As shown in Fig. 3, the two mainfluorescent groups of AOM were T1: Ex 250–300/Em 300–400 nm(tryptophan protein-like substances) and T2: Ex 220–250/Em300–380 nm (aromatic protein substances), and the former hashigher fluorescence intensity than the latter, suggesting higherconcentration of tryptophan protein-like substances in AOM.There were no new fluorescent groups produced during the degra-dation process. The fluorescent intensities of both peaks gradu-ally decreased with time (Fig. 4). However, the reduction of T1fluorescence intensity was more significant, indicating that thetryptophan protein-like substances might be more easily degradedby MFC.




3.5. UV–vis spectra and UV254 value variations duringbioelectrochemical oxidation

The UV–vis spectra demonstrated a reduced absorbance valueswith increase of wavelengths (Fig. S2a). There are absorbancepeaks at around 260–280 cm�1 and 420–450 cm�1, correspond-ing to protein-like compounds with unsaturated bonds, such astryptophan, tyrosine, phenylalanine, etc. UV254 as a comprehensiveindex of organic matter, mainly related to the aromatic ring, dou-ble bond and hydroxyl functional groups with conjugated struc-ture. The organic matter with intensive ultraviolet absorptionoften have high molecular weight. In the first 10 h, UV254 adsorp-tion rapidly reduced more than 50%, supporting the results men-tioned above that large molecular organics were decomposedinto small molecular weight compositions by the biodegradationin MFC (Fig. S2b). Then, the UV254 adsorption declined slowly withtime. Bacterial metabolisms could also release some soluble micro-bial products into solution, which might result in a slight increaseof UV254 adsorption at time of 20–30 h.

4. Conclusions

Degradation of AOM, mainly including protein-like andhumic-like substances as well as Chlorophyll a, was more com-pletely by bioelectrochemical oxidation in MFC with closed circuitthan anaerobic fermentation in MFC with open circuit. The newlygenerated small molecular byproducts during AOM degradationcould be oxidized by electrode but not by fermentation. The dom-inant tryptophan protein-like substances in AOM were degradedmore quickly than aromatic protein during MFC treatment.

Acknowledgements

The authors would like to thank the Funds for Creative ResearchGroups of China (Grant No. 51121062), the National NaturalScience Foundation of China (No. 50778048), and State KeyLaboratory of Urban Water Resource and Environment (HarbinInstitute of Technology) (No. 2014TS02) for their supports for thisstudy.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.biortech.2015.06.014.

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