Waste Management 34 (2014) 1035–1040

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Waste Management

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Ultrasound pretreatment of filamentous algal biomass for enhancedbiogas production

0956-053X/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.wasman.2013.10.012

⇑ Corresponding author. Tel.: +82 2 450 3736.E-mail address: kypark@konkuk.ac.kr (K.Y. Park).

Kwanyong Lee a, Phrompol Chantrasakdakul a, Daegi Kim a, Mingeun Kong b, Ki Young Park a,⇑a Department of Civil and Environmental System Engineering, Konkuk University, 120 Neungdong-ro, Gwangjin-gu, Seoul 143-701, Republic of Koreab EPS Solution Ltd., 126-1 Pyeongchon-dong, Dongan-gu, Anyang, Gyeonggi-do 431-755, Republic of Korea

a r t i c l e i n f o

Article history:Available online 22 November 2013

Keywords:AlgaeBiogas productionHydrodictyon reticulatumPretreatmentUltrasound

a b s t r a c t

The filamentous alga Hydrodictyon reticulatum harvested from a bench-scale wastewater treatment pondwas used to evaluate biogas production after ultrasound pretreatment. The effects of ultrasound pretreat-ment at a range of 10–5000 J/mL were tested with harvested H. reticulatum. Cell disruption by ultrasoundwas successful and showed a higher degree of disintegration at a higher applied energy. The range of10–5000 J/mL ultrasound was able to disintegrated H. reticulatum and the soluble COD was increasedfrom 250 mg/L to 1000 mg/L at 2500 J/mL. The disintegrated algal biomass was digested for biogasproduction in batch experiments. Both cumulative gas generation and volatile solids reduction data wereobtained during the digestion. Cell disintegration due to ultrasound pretreatment increased the specificbiogas production and degradation rates. Using the ultrasound approach, the specific methane produc-tion at a dose of 40 J/mL increased up to 384 mL/g-VS fed that was 2.3 times higher than the untreatedsample. For disintegrated samples, the volatile solids reduction was greater with increased energy input,and the degradation increased slightly to 67% at a dose of 50 J/mL. The results also indicate that disinte-gration of the algal cells is the essential step for efficient anaerobic digestion of algal biomass.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

The exhaustion of fossil fuels and the global warming situationare strongly motivating research in alternative energies (Berndeset al., 2003). Many countries are interested in renewable energysources, especially in sustainable forms of energy, i.e., geothermalpower, wind power, small-scale hydropower, solar energy, bio-mass energy, tidal power, and wave power. Biomass energy is gain-ing increasing importance because of its environmentally soundand energy-saving production methods (Zheng et al., 2012). Vari-ous biomasses derived from the carbonaceous waste of humanand natural activities could be utilized as renewable energyresources. Algae have been identified as a promising biomassfeedstock because of their high biomass productivity and theirnon-food-source properties (Mandal and Mallick, 2009).

Algae have attracted increasing attention as a sustainable pro-cess component for nutrient removal and biofuel production, aswell as for mitigation of excessive CO2 production. Biofuel gener-ated from algal treatment of wastewater is a more sustainable fuelwhile using significantly less energy (Rawat et al., 2011; Satyanara-yana et al., 2011; Ehimen et al., 2013). Biogas production from algalbiomass by anaerobic digestion is one of the most environmentallybeneficial technologies, based on both total produced biomass and

the residuals remaining after conversion to biofuel. Anaerobicdigestion is a process wherein anaerobic bacteria convert organicmatter into biogas. Biogas is a mixture of methane gas (CH4) andcarbon dioxide gas (CO2). Natural gas consists of approximately90–95% methane, but biogas is composed of approximately50–65% methane, signifying a low-grade natural gas. This biogas canbe used as a fuel for heating, in gas engines for electricity and heat-ing, or for upgrading to natural gas quality. Thus, biogas productionis an interesting alternative energy because it contributes to notonly energy production but also to reducing organic wastes.

Methane production from algal biomass has been discussed inthe literature, with an emphasis on anaerobic digestion of single-celled species such as Chlorella spp. (Oswald and Goluke, 1960).However, the practicality of energy generation from algae has beenlimited because of the economic and energy costs associated withcultivating and harvesting unicellular microalgae species (Sialveet al., 2009). Filamentous algae are easier and less expensive toharvest compared with unicellular algae because of their physicalcharacteristics. Low-cost filtration methods could be used toharvest filamentous algae strains described high rate algae bymicrostrainer to retain larger cells and washing out smallernon-filamentous algae (Logan and Ronald, 2011). Thus, the use offilamentous algae could potentially improve the economics of en-ergy generation from algae. There are only a few reports on CH4

production using filamentous algae (Samson and LeDuy, 1983).H. reticulatum is a diverse filamentous alga that can be found in

1036 K. Lee et al. / Waste Management 34 (2014) 1035–1040

almost all aquatic environments, and this alga is usually observedas green, thread-like, mat-forming structures floating close to thesurface of non-turbulent water bodies (Flory and Hawley, 1994).Owing to its widespread availability, H. reticulatum was used asthe biomass in this investigation.

In the case of methane fermentation of solid organic materialssuch as microbial cells, the methane yield is significantly affectedby the mass transfer of each biological step as well as by food avail-ability (Izumi et al., 2010). Up to date, however, the literature onanaerobic digestion of microalgae is limited (Passos et al., 2013a).Anaerobic biogas production from algal biomass is impeded by thehard cell wall of microalgae (Chen and Oswald, 1998). Goluekeet al. (1957) reported that digested sludge provides a noticeablegreen color during anaerobic digestion because of the persistenceof chlorophyll, which is an intracellular material. This observationsuggests that cellular lysis was not completed during digestion,thereby reducing the total biogas production. To improve the overallsubstrate degradability, pretreatment or disintegration of the algalbiomass is required. Various disintegration techniques, includingultrasonography, have been successfully applied as pretreatmentmethods to enhance anaerobic digestibility (Nickel and Neis,2007). Biomass disintegration improves the solubility of the sludgeparticles by disrupting the sludge/flocs in the aqueous phase. Thedissolved components can be readily degraded and utilized as sub-strates in the biological process, thus resulting in increased bioavail-ability (Park et al., 2004; Lee et al., 2005). Recently, sonication wasapplied to break down unicellular algal biomass and improve meth-ane production, achieving up to a 60% increase in methane yield(González-Fernández et al., 2012; Alzate et al., 2012). Passos et al.,(2013a, 2013b) employed microwave irradiation and thermal treat-ment to enhance the disintegration and digestibility of microalgae.However, little information is available regarding filamentous algalbiomass-disintegrating methods for anaerobic digestion.

This technical study aimed at providing preliminary informa-tion on methane yields from the anaerobic digestion of the fila-mentous alga H. reticulatum. An additional aim of this work wasto study the effects of different ultrasound doses to algal feed onanaerobic digestion of the filamentous alga H. reticulatum.

2. Materials and methods

2.1. Biomass sources

The filamentous alga used in this study, H. reticulatum, was sup-plied by the Korean Research Institute of Chemical Technology,Daejeon, Korea, and was cultivated in secondary effluent of treatedwastewater collected from the municipal wastewater treatmentplant in Ansan, Korea (Table 1).

H. reticulatum was cultivated in a bench-scale raceway pondwith secondary wastewater (Fig. 1). The capacity of the racewaypond was 100 L (width, 0.4 m; length, 1.4 m; depth, 0.5 m) andthe pond was constructed and operated under indoor conditionswith agitation using a stainless steel paddle wheel. An artificiallyilluminated raceway reactor was used, and light sources were posi-tioned on both sides of the reactor. Illumination was provided by alight-emitting diode (LED) array. The incident average light inten-sity was 120 ± 20 lmol m2 s with a 12-h light/dark cycle. The

Table 1Secondary effluent composition as an algae growth medium.

COD T-N Nitrate N

Concentration (mg/L) 12.8 7.7 3.7(1.9)* (0.4)* (0.5)*

* Standard deviation.

growth was manually harvested once daily (7.25 g/m2 d) using asieve. Although the harvested samples contained non-H. reticula-tum biomass because of the wastewater cultivation conditions,the H. reticulatum biomass accounted for more than 99% of the to-tal biomass dry weight due to sifting out of small organisms. Theharvested samples were initially used in the pretreatment processwithout cleaning. Prior to their use in the digestion process, theconcentration of total solids (TS), total suspended solids (TSS), vol-atile solids (VS), volatile suspended solids (VSS), soluble COD, andammonia nitrogen were analyzed (see Fig. 2).

2.2. Pretreatment

Blended H. reticulatum samples were further subjected tomechanical disruption using a low frequency ultrasound homoge-nizer (STH-750S; Sonitopia, Korea). A constant frequency of 20 kHzand an ultrasonic power of 150 W were used. The homogenizerwas equipped with a horn (20 � 123 mm in diameter). The ultra-sound dose is related to the amount of energy supplied per unitvolume of substrate (expressed in J/mL). However, the dose doesnot depend on the TS concentration. The ultrasound dose cannotbe used to compare substrates with different TS contents. Whenthe TS content remains constant, the ultrasound density is a prac-tical method of expressing the energy input for the disintegrationof algal cells on a volume basis. The different ultrasound dosesapplied to 100 mL of H. reticulatum (10,000 mg/L TS) were 10 J/mL,20 J/mL, 30 J/mL, 40 J/mL, 50 J/mL, 500 J/mL, 1000 J/mL, 2500 J/mL,and 5000 J/mL.

Soluble COD release was used as a direct measurement of H.reticulatum cell disintegration. When the H. reticulatum cells weresonicated, the intracellular contents were released into the aque-ous phase. Increased soluble COD after ultrasonic disintegrationwas an indicator of the cell disintegration efficiency. Samples werefiltered through a 0.45 lm membrane and then used for solubleCOD measurements.

2.3. Biochemical methane potential (BMP)

Batch digestion was performed in a series of BMP assays byincubating algal biomass inoculated with anaerobic bacteria. Theactive anaerobic inoculum operating at methophilic conditionswas obtained from the anaerobic digester at the Ansan municipalwastewater treatment plant in Korea. Feed sludge was also takento compare digestibility with algal biomass. The inoculum wasthen filtered by stainless steel filter mesh to prevent inorganic for-eign materials, mixed thoroughly, and used for the digestion trials.A nutrient/mineral/buffer (NMB) medium prepared according toYoung and Tabak (1993). H. reticulatum samples thawed to roomtemperature were used in the BMP assays. The BMP assays wereperformed using sealed 160-mL serum bottles at 35 �C. The pro-duced biogas was measured and was used to represent the BMP.Duplicate units of the digestion setup were used for all pretreat-ment schemes in this study. Biogas production from the inoculumand medium was recorded and used as the blank. Inoculum andsubstrate were used at a ratio of 1:1 using the TS mass. Nutrientsrequired for the growth of anaerobic microorganisms were addedto each BMP serum bottle (NMB medium) at a volume that was

Ammonia N Nitrite N T-P Ortho-phosphate

0.2 0.04 1.1 0.8(0.1)* (0.02)* (0.5)* (0.2)*

Fig. 1. Image of bench-scale raceway pond. (a) Before operation and (b) during operation.

01234567

Conc

entra

tion

(mg/

L)

T-NNitrate NAmmonia NNitrite N

00.10.20.30.40.50.60.7

Conc

entra

tion

(mg/

L)

T-PPhosphate P

Harv

este

d al

gae

(g)

Elapsed time (day)

Harvested algae

00 10 15 25205

4000

2000

6000

8000

10000

(a)

(b)

(c)

Fig. 2. Nitrogen and phosphorus removal and harvested algae during algaltreatment.

0

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400

0 5 10 15 20 25 30

Cum

ulat

ive

met

hane

pro

duct

ion

(mL/

g-VS

)

Elapsed time (day)

Sludge Algae

Fig. 3. Methane production from algae and sludge.

K. Lee et al. / Waste Management 34 (2014) 1035–1040 1037

approximately 3 times the total volume of the added inoculum(Table 1). The serum bottle was then filled to 100 mL with distilledwater.

Data for both cumulative methane generation and volatile sol-ids reduction (VSR) were obtained during the digestion. The gasproduction was measured daily by inserting a needle attached toa frictionless syringe through the septum and allowing the head-space to equilibrate to atmospheric pressure. The composition ofthe headspace was analyzed toward the end of the experimentvia gas chromatography.

2.4. Analytical methods

The concentration of TS, TSS, VS, VSS, Nitrate nitrogen, Nitritenitrogen, Total phosphorus (T-P), ortho-phosphate and COD wereanalyzed following standard methods (APHA, 1998). Total nitrogen(T-N) was determined in H. reticulatum before ultrasonic disinte-gration by Persulfate Digestion Method in HACH methods 10072.To study the release of ammonia nitrogen concentration at differ-ent ultrasonic dose, the ammonia nitrogen (ammonia N) releaseafter ultrasonic disintegration of H. reticulatum cell was deter-mined by salicylate method. To evaluate the effect of ultrasonica-tion on H. reticulatum cell disintegration, sonicated samples wereexamined at the cellular level using light microscope. Cell mor-phology of sonicated samples was compared with that of non-son-icated samples using an optical microscope (DP71-SETModel,Olympus).

The composition of the headspace was analyzed toward the endof the experiment via gas chromatography (HP 5890, PA, USA)using a thermal conductivity detector, by injecting gas samplesinto a packed column (hayesep 3 m 1/8 in. 100/120). The carriergas was Helium in split less mode (column flow: 19 mL/min).The oven temperature was 35 �C with a retention time of1.5 min. Injector and detector temperature were 150 �C and180 �C, respectively. The gas composition was measured towardthe end of the experiment.

3. Results and discussion

3.1. Algal growth

Continuous experiments were conducted to study the growth ofH. reticulatum in secondary effluent of treated wastewater. Theconcentrations of nitrogen and phosphorous species over time dur-ing the experiments are shown in Fig. 3.

Algal treatment offers a cost-effective approach to removingnutrients from tertiary wastewater treatment (Tang et al., 1997).Throughout the experiments, the nitrogen levels of the effluentranged from 1.5 mg/L to 3.5 mg/L given an initial nitrogen concen-tration of approximately 7.7 mg/L. Effluent phosphorus showed avalue of below 0.4 mg/L, with an initial phosphorus concentrationof 1.1 mg/L. The average efficiencies of nitrogen and phosphorus

removal were 70.5% and 62.9%, respectively. The daily harvestedalgal biomass was approximately 7.95 g m�2 d�1. Algal biomass isa potentially important biomass for biofuel production. Algal bio-mass has widely varying lipid contents, and technologies for lipid

0

500

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0 1000 2000 3000 4000 5000 6000

SCO

D a

nd A

mm

onia

N (m

g/L)

TSS

and

VSS

(mg/

L)

Ultrasound dose (J/mL)

TSS VSSSCOD Ammonia N

Fig. 5. TSS and VSS concentrations using different ultrasound doses.

1038 K. Lee et al. / Waste Management 34 (2014) 1035–1040

extraction are still under development (Woertz et al., 2009; Fabi-ana et al., 2013; Alzate et al. 2012). Although relatively few studieshave been published on the anaerobic digestion of filamentousmicroalgae, anaerobic digestion is a promising process that couldsolve waste issues and provide an economical and energy-balancedtechnology (Sialve et al., 2009).

Fig. 3 shows that batch digestion, using the alga H. reticulatumas feed, was not effective in producing methane, compared withwastewater sludge feed. In this experiment, the methane yield pro-duced by H. reticulatum was 170 mL/g of VS fed, which was lowerthan that from wastewater sludge. The earliest work on this topiccompared the digestion of domestic wastewater sludge and greenmicroalgal biomass, Scenedesmus spp. and Chlorella spp. harvestedfrom wastewater ponds (Golueke et al., 1957), and this early studyshowed a 32% lower yield from the microalgal biomass comparedwith the wastewater sludge.

3.2. Effect of ultrasound pretreatment on disintegration of H.reticulatum

Ultrasound disintegration technologies focus on H. reticulatumto improve anaerobic digestion in this study. Sonication of H. retic-ulatum prior to anaerobic digestion significantly enhanced the bio-degradability of these cells. Figs. 4 and 5 show the effects ofultrasound pretreatment of filamentous algae: Fig. 4 is a photo-graph of the microalgae with pretreatment, before (a) and after(b) ultrasound application. A microscopic image of the microalgaeshows significant disruption of the H. reticulatum cells.

We used 10 different ultrasound doses: 0 J/mL, 10 J/mL, 20 J/mL,30 J/mL, 40 J/mL, 50 J/mL, 500 J/mL, 1000 J/mL, 2500 J/mL, and5000 J/mL. The concentration of algae used for the sonicationwas approximately 10,000 mg/L of TS (8700 mg/L of VS). Both TSand VS of each sample followed a similar trend with differentultrasound doses. The results showed that the concentrations of to-tal suspended solids (TSS) and volatile suspended solids (VSS) de-creased by sonication (Fig. 5). When an ultrasound dose of 5000J/mL was used, the TSS concentration was decreased to 6200 mg/L.These results prove that the insoluble particulate organic matteris transformed into a soluble state by ultrasonic disintegration.

The relationship between the ultrasound dose and soluble CODconcentration is shown in Fig. 5. The soluble COD concentration in-creased until an ultrasound dose of 2500 J/mL was used, and theconcentration then decreased when the highest dose (5000 J/mL)was applied. This result shows that the concentration of solubleCOD increases by sonication and proves that intracellular organicmatter is released because of algal cell wall disruption by ultra-sound, and then soluble COD destroyed to inorganic at the higherdose of sonication. Ammonia nitrogen released from H. reticulatumwas analyzed during sonication. The effects of the ultrasoundtreatment on the concentration of ammonia N released at differentultrasound doses are shown in Fig. 5. The results show that theammonia N concentration increases with an increase in the

Fig. 4. Image of algae with sonication. (a) Before and (b)

ultrasound dose. For ultrasound doses of 0 J/mL and 5000 J/mL,the concentrations of ammonia nitrogen released were 80 mg/Land 110 mg/L, respectively.

3.3. Effects of ultrasound pretreatment on the biochemical methanepotential

The BMP experiment was performed at 35 �C in 160 mL serumbottles. BMP assays were conducted to determine the specific con-ditions required for optimal methane production of filamentous al-gae using different ultrasound doses. The 1% TS (8700 mg/L VS) ofH. reticulatum was subjected to ultrasound pretreatment before theBMP assay was performed. The inoculum and substrate added toeach serum bottle were at a 1:1 ratio based on the TS mass.Fig. 6 shows the methane generation of H. reticulatum. In the first3 days of the BMP assay, the methane generation rate was lowfor all tested ultrasound doses because of the lag phase of anaero-bic digestion. The rate of biogas generation increased exponentiallyfrom the initial day until the generation slowed. At 10 days, theaccumulated methane generation was maximal and methane wasthereafter produced at a steady generation rate. When theultrasound dose in range from 10 J/mL to 5000 J/mL, methane gasaccumulated up to 313–384 mL/g-VS fed, which is approximately1.9–2.3 times higher than that obtained with the non-sonicatedsample (0 J/mL). Most disintegration technologies focus on sludgepretreatment to increase the overall biodegradability of thesubstrate. The relative improvement by ultrasound disintegrationwith respect to gas production from sludge varies from 0% to60% (Palmowski et al., 2006), and indicates that compared withwastewater sludge, it is easy to decompose H. reticulatum usingultrasound pretreatment.

Graph fitting was performed to investigate the BMP and esti-mated parameters using the modified Gompertz Eq. (1).

M ¼ P � exp � expRm � e

Pk� tð Þ þ 1

� �� �ð1Þ

after application of an ultrasound dose of 5000 J/mL.

Elapsed time (days)0 10 20 30 40 50

Cum

ulat

ive

met

hane

pro

duct

ion

(mL-

CH

4/g-V

S)

0

100

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400

500 0 J/mL10 J/mL20 J/mL30 J/mL40 J/mL50 J/mL500 J/mL1,000 J/mL2,500 J/mL5,000 J/mL

Fig. 6. Accumulated biogas production profile with different ultrasound doses.

Table 2Effect of ultrasound pretreatment on BMP.

Ultrasound dose (J/mL)

0 50 500 1000 2500 5000

P 165.9 348.3 326.2 318.9 313.5 333.2Rm 8.0 21.3 20.9 18.7 16.8 20.5k 6.2 5.1 4.9 5.5 6.1 5.2

⁄P = methane production potential, Rm = methane production rate, k = lag-phasetime.

50

55

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0 1000 2000 3000 4000 5000 6000

VS re

duct

ion

(%)

Met

hane

yie

ld (m

L/g-

VS)

Ultrasound dose (J/mL)

Methane YieldVS reduction

Fig. 7. Effects of ultrasound pretreatment of VS reduction.

K. Lee et al. / Waste Management 34 (2014) 1035–1040 1039

where M = cumulative methane production, k = lag-phase time,P = methane production potential, Rm = methane production rate,and e = exp(1).

To compare the progression of digestion of different samples,the determined biogas volume was calculated by non-linearregression analysis using the modified Gompertz equation and Sig-maPlot 10.0 (Table 2). The curves showed a good fit between theexperimental data and calculated values in all cases (R2 was be-tween 0.984 and 0.997, and p-value was below 0.0001). The cumu-lative methane production showed that sonication at 40–50 J/mLwas adequate for H. reticulatum in terms of maximum methaneproduction potential and methane production rate. These 2 param-eters increased by approximately 2-fold while the lag time wasshortened. The VS reduction data were also obtained during thedigestion (Fig. 7). For the disintegrated samples, VS reductionincreased according to the energy input, from 60% to 67%. These

results indicate that pretreatment of filamentous algal cells needto optimize anaerobic digestion efficiency of algal biomass.

4. Conclusions

Methods that use algae have attracted increasing attention assustainable processes for nutrient removal and biofuel productionas well as for mitigation of CO2 generation. Biogas production fromalgal biomass is one of the most environmentally beneficial tech-nologies, whether using the total produced biomass or the residualfraction remaining after biofuel production. However, biogas pro-duction from anaerobic processes is impeded by the rigid algal cellwall. In this study, the alga H. reticulatum was used to treat second-ary wastewater and was harvested as a residual. Ultrasonic pre-treatment was successfully used for improving the disintegrationand anaerobic biodegradability of H. reticulatum. The effect ofultrasonic pretreatment at doses from 10 J/mL to 5000 J/mL ap-plied to H. reticulatum was investigated.

The cell disruption efficiency in terms of disintegration degreeincreased as the applied energy increased. The methane formationefficiency was improved by up to 2.3 times when the ultrasoundchanged the chemical composition and enhanced the substrate sol-ubility at an energy dose of 40 J/mL. The VS reduction data werealso obtained during the batch digestion. The VS reduction ob-served for the digester using a feed of disintegrated samples wasgreater than in the control reactor without biomass pretreatment,and the reduction reached up to 67% at an energy dose of 50 J/mL.

Acknowledgements

This study was supported by the Korea Ministry of the Environ-ment (MOE) as an ‘‘Eco-Innovation Project’’ (Project No.: E212-40005-0035-0). This work was supported by the Waste to Energyand Recycling Human Resource Development Project (YL-WE-12-001)funded by the Korea MOE.

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