CO 2 Fixation, Lipid Production, and Power ... - ACS Publications

Subscriber access provided by UNIV OF CAMBRIDGE

Article

CO2 fixation, lipid production and power generation by a novel air-lift-type microbial carbon capture cell system Xia Hu, Baojun Liu, Jiti Zhou, Ruofei Jin, Sen Qiao, and Guangfei Liu Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 13 Aug 2015 Downloaded from http://pubs.acs.org on August 14, 2015

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 33

Environmental Science & Technology

1

CO2 fixation, lipid production and power generation by a novel air-lift-type

2

microbial carbon capture cell system

3

Xia Hu, Baojun Liu, Jiti Zhou*, Ruofei Jin, Sen Qiao and Guangfei Liu

4

Key Laboratory of Industrial Ecology and Environmental Engineering, Ministry of

5

Education, School of Environmental Science and Technology, Dalian University of

6

Technology, Linggong Road 2, Dalian 116024, China.

7 8 9 10 11 12 13 14 15 16 17 18

* Corresponding author. Tel. /fax: +8641184706252.

19

E-mail address: [email protected]

20 21 22

1

ACS Paragon Plus Environment


23

Abstract

24

An air-lift-type microbial carbon capture cell (ALMCC) was constructed for the

25

first time by using air-lift-type photobioreactor as the cathode chamber. The

26

performance of ALMCC in fixing high concentration of CO2, producing energy

27

(power and biodiesel), and removing COD together with nutrients, was investigated

28

and compared with the traditional microbial carbon capture cell (MCC) and

29

air-lift-type photobioreactor (ALP). The ALMCC system produced a maximum power

30

density of 972.5 mW·m-3 and removed 86.69% of COD, 70.52% of ammonium

31

nitrogen and 69.24% of phosphorus, which indicate that ALMCC performed better

32

than MCC in terms of power generation and wastewater treatment efficiency. Besides,

33

ALMCC demonstrated 9.98 and 1.88 fold increase over ALP and MCC in CO2

34

fixation rate, respectively. Similarly, the ALMCC significantly presented a higher

35

lipid productivity compared to those control reactors. More importantly, the

36

preliminary analysis of energy balance suggested that the net energy of the ALMCC

37

system was significantly superior to other systems and could theoretically produce

38

enough energy to cover its consumption. In this work, the established ALMCC system

39

simultaneously achieved the high level of CO2 fixation, energy recycle and municipal

40

wastewater treatment effectively and efficiently.

41 42 43 44 45 2


Page 2 of 33

Page 3 of 33


46

1. Introduction

47

Global warming induced by a rapid increase of CO2 concentration in the

48

atmosphere has been identified as one of the major worldwide challenges for

49

environmental sustainability1, 2. Microalgae cultivation in municipal wastewater for

50

CO2 fixation is considered as one of the most promising and environmental-friendly

51

approaches.3,

52

ways for biodiesel production and municipal wastewater treatment, and also for

53

reducing the need of chemical fertilizers and algae’s life cycle burden.5 However, the

54

nitrogen concentration in municipal wastewater is significantly lower than that in the

55

medium of microalgae cultivation, which often leads to a relatively low biomass

56

productivity, and thus low CO2 fixation efficiency and overall lipid productivity.6

57

Fortunately, these concerns can be effectively addressed when microalgae are

58

cultivated in the cathode of microbial fuel cells (MFCs), which have been developed

59

as an emerging bioelectrochemical technology for wastewater treatment and electrical

60

energy generation recently. 7-10 In dual-chamber MFCs, the cation species (e.g., Na+,

61

K+, NH4+, Ca2+, and Mg2+) other than protons are primarily responsible for the

62

transport of positive charges across Nafion membrane and their concentrations are

63

typically 105 times higher than the proton concentration, which resulted in

64

accumulation of these cations at the cathode chamber.11, 12 It is most intriguing that the

65

species of NH4+ could be substantially accumulated in the cathode chamber. Therefore,

66

the sufficient nitrogen would be provided for microalgal growth as long as microalgae

67

are cultivated in the cathode of MFCs together with a continuous feeding of municipal

68

wastewater into the anode of MFCs.

4

Apart from CO2 fixation, microalgae cultivation provides possible

3



69

Recently, microbial carbon capture cells (MCCS) emerged as a new sustainable

70

form of MFCs with an algae-assisted cathode, which have attracted much attention in

71

the fields of wastewater treatment, clean electric energy production and CO2

72

sequestration of discharged from anode in MFCs.13, 14 However, those investigations

73

on MCCs generally showed low biomass productivities, which led to low CO2

74

fixation efficiency and biodiesel production6, due to the low mixing efficiency and

75

photosynthetic rate. To address this inefficiency, the air-lift photobioreactor (ALP)

76

may bring a good complement to MCC, owing to its excellent mixing efficiency and

77

best volumetric gas transfer through its liquid cylindrical column. In some previous

78

reports, the microalgae cultivated in the bioreactors yielded the maximum biomass

79

productivity and better specific growth rate.15, 16 In light of the synergetic advantages

80

of MCC and ALP, a system could be established by linking the two devices for the

81

high concentration of CO2 fixation. Thus, an air-lift-type microbial carbon capture cell

82

(ALMCC) could be established by installing the ALP in a MCC as the cathode

83

chamber. In the anode compartment of the ALMCC, the organic matters in municipal

84

wastewater are oxidized to carbon dioxide, producing protons and electrons.

85

Meanwhile, the effluent of the anode containing the residual inorganic nutrients could

86

be used as the medium of microalgae cultivated in the cathode chamber of ALMCC.

87

This system will achieve high biomass concentration to fix high concentration of CO2

88

due to a good mixing in the ALP and constant supplement of nitrogen and minerals

89

into cathode of ALMCC through Nafion membrane. In return, the oxygen

90

continuously produced from microalgae photosynthesis is used as electron acceptor 4


Page 4 of 33

Page 5 of 33


91

for the electricity generation,17 which avoids the use of noble or non-noble catalysts

92

for oxygen reduction, resulting in the enhancement of the economic viability and

93

environmental sustainability.18 Furthermore, CO2 is added to the cathode chamber for

94

CO2 fixation, which also could create a CO2/bicarbonate buffered catholyte system,19,

95

20

96

Through this combination, the high concentration of CO2 could be fixed and

97

bioenergy (bioelectricity and biodiesel) could be produced. At the same time, COD

98

and nutrient in municipal wastewater could be removed without extra cost.

thereby diminishing pH imbalances and increasing power density of ALMCC.

99

In this study, the ALMCC system was constructed for the first time for

100

high-density cultivation of microalgae to fix high level CO2, generate bioenergy and

101

treat municipal wastewater. Its performance was investigated in terms of CO2 fixation,

102

C, N and P removal, power generation and lipid accumulation. To evaluate the

103

advantages of the system, the performance comparison were carried out among the

104

ALMCC, MCC and ALP. Moreover, the energy balance of the three reactors was

105

analyzed for better understanding of the ALMCC system.

106

2. Material and methods

107

ALMCC setup

108

The ALMCC system was comprised of double-chamber and separated by a

109

proton exchange membrane (126 cm2, Nafion 117, Dupont, US). As shown in Figure

110

1, it was constructed by assembling two half-cube structures together with rubber

111

gaskets. The anode chamber was a simple cube with a liquid volume of 600 mL. The

112

cathode chamber of ALMCC was an air-lift-type cubical photobioreactor with a 5



113

centric tube and the liquid volume was 500 mL. The sparger at the bottom of the

114

cathode chamber of ALMCC received continuous aeration of 10% CO2 with 60

115

mL·min-1 during microalgae cultivation to achieve high mass transfer for producing

116

more biomass, although the periodic dosing with CO2 rich microbubbles was reported

117

to be just as effective in growing microalgae.21 A 10 cm long carbon brush (5 cm in

118

diameter) was used as the anode electrode. Prior to usage, the carbon brush was

119

pretreated by heating at 450 °C for 30 min.13 The cathode electrode was carbon fiber

120

cloth (5 cm × 15 cm =75 cm2). Then the anode and cathode electrodes were connected

121

by copper wires and the external resistance was 1000 Ω. Saturated calomel electrode

122

(SCEs; Spsic-Rex Instrument Factory, China) was inserted into anode chamber as a

123

reference electrode. Both a cubical double-chamber MCC and an independent ALP

124

were set up for control experiments.

125

Inoculation and operation

126

The ALMCC system was operated with a synthetic solution at about 30°C. The

127

anode chamber was inoculated with electrochemically active bacteria suspension from

128

a MFC using sodium acetate for more than half a year. The synthetic municipal

129

wastewater contained sodium acetate, 280 mg·L-1; NH4+-N, 39.04 mg·L-1; PO43--P,

130

3.62 mg·L-1; NaHCO3, 600 mg·L-1; NaCl, 12.5 mg·L-1; MgSO4, 6.25 mg·L-1; CaCl2,

131

33.34 mg·L-1 and 1 mL·L-1 of trace elements. The synthetic municipal wastewater

132

was fed into the anode chamber at a flow rate of 0.8 mL·min-1. The anode chamber

133

was covered with tinfoil to avoid illumination and to prevent the growth of algae. The

134

anode effluent was autoclaved at 121 °C, followed by cooling to room temperature, 6


Page 6 of 33

Page 7 of 33


135

and used as medium of microalgae cultivation in the cathode chamber of the ALMCC.

136

The anode effluent was autoclaved to avoid nutrients competition by microbes and

137

achieve isolating the role of microalgae growth.

138

The cathode chamber was inoculated with the green algae Chlorella vulgaris

139

(ESP-6) obtained from National Cheng Kung University previously maintained in

140

axenic culture. Before being added into the cathode chamber, the algal suspension

141

was centrifuged (8000 rpm for 10 min) and washed 2 times using deionized water

142

under sterile conditions to remove residual carbon source for isolating the role of CO2

143

fixation, and then re-suspended in sterilized anode effluent. The cathode chamber was

144

sterilized with 75% alcohol solution and refilled with sterile anode effluent with

145

Chlorella vulgaris (0.1 g·L-1) as inoculum. A continuous illumination of fluorescent

146

lamp (light intensity of 8.9 W·m-2) was employed around the cathode. Evaporated

147

water from the cathode chamber was replenished with sterilized anode effluent.

148

Analysis and calculations

149

The cell voltage was recorded by a data acquisition system (PISO-813, ICP DAS

150

Co., Ltd.) every 30 min. Power density and current density were calculated based on

151

the effective volume of anode chamber according to a previous report.22 After stable

152

voltage outputs, polarization curves were obtained by varying the external resistances

153

from 1000 to 50 Ω.13 The concentrations of COD, NH4+-N, NO3--N, NO2--N, and

154

PO43--P were measured according to the standard method (APHA, 1999).17 The pH

155

value was measured with a pH meter (METTLER TOLEDO FE20K, Switzerland).

156

Dissolved oxygen (DO) was measured by a DO meter (YSI 550A, America). The 7



157

biomass concentration of Chlorella vulgaris was determined as absorbance23, 24 at 690

158

nm by UV-Vis Spectrophotometer (Jasco V-560) and converted to biomass

159

concentration using the standard curve shown in Supporting Information (SI) Figure

160

S1. The procedures of scanning electron microscopy (SEM) are shown in the SI. CO2

161

fixation rate was calculated according to a previous report25 and the equation is shown

162

in the SI. The oil-droplet of Chlorella vulgaris stained with Bodipy 505/515 was

163

observed by confocal laser scanning microscopy (CLSM, OlympusFV1000).26 The

164

lipid content was determined using the method of FTIR spectroscopy (Bruker

165

VERTEX 70, Germany) and its accuracy has been validated by traditional methods.27,

166

28

167

3. Results and discussion

168

Power generation of ALMCC

The measurements of lipid content and productivity are described in the SI.

169

The ALMCC system was operated for 6 days after the acclimation stage. A MCC

170

as control and the operations was identical to the ALMCC. Figure 2A shows the

171

electricity productions of ALMCC and MCC with an external resistance of 1000 Ω.

172

The maximum voltage output was 0.49 V in the ALMCC, which was higher than that

173

of the MCC (0.42 V). Figure 2B exhibits the polarization and power density curves.

174

The peak power density in the ALMCC reached to 972.5 mW·m-3, which was 46.47%

175

higher than that (520.6 mW·m-3) produced from the MCC. The difference between

176

two systems was mainly ascribed to the performance of cathodes (the anode chambers

177

of ALMCC and MCC were identical), whereas the cathode reaction relied on the

178

dissolved oxygen (DO) produced by algae in the cathode compartment.23 As shown in 8


Page 8 of 33

Page 9 of 33


179

Figure 2C, the DO concentration was 9.74 ± 0.16 mg·L-1, which was 27.31% higher

180

than that in the MCC (7.08 ± 0.19 mg·L-1) at the same operation. The DO levels

181

approached saturation in the current study, which is an inhibitor of higher microalgal

182

metabolic activity. However, such high DO level was then counterproductive. It might

183

be due to that O2 was effectively stripped by dosing with CO2 rich microbubbles.21 It

184

also was demonstrated that the dosing of CO2 and the stripping of O2 were sufficiently

185

fast because CO2 was always in excess (saturated) in the culture medium and O2 was

186

removed as fast as it was produced.29 Actually, the DO generation in the two reactors

187

mainly relied on the photosynthesis reaction of algae in their cathode chambers. The

188

algae concentration was 3.04 ± 0.16 g·L-1 in the ALMCC on the 6th day, and it was

189

about twice higher compared to that in the MCC (Figure 3A), which indicates that the

190

power output is limited by algal photosynthesis.

191

In addition, the difference of electricity production between the ALMCC and

192

MCC was also due to the fact that the internal resistance (152.02 Ω) in the ALMCC is

193

lower than that of MCC (204.05 Ω). The internal resistance was proved to be a key

194

factor on the electricity production of MFCs.22, 30 In the ALMCC, the cultivation of

195

algae in the air-lift-type photobioreactor enhanced the efficient mixing of algal cells,15

196

which reduced the liquid-phase mass transfer resistance. Unlike the ALMCC cell, the

197

substantial amount of algal cells grown on the wall and bottom of the cathode in the

198

MCC increased both mass transfer resistance and internal resistance. Even, a part of

199

algal cells adhering to the carbon cloth may lead to higher mass transfer resistance of

200

proton and oxygen. It is worth noting that, in the ALMCC, the carbon cloth could be 9



201

immobilized by centric-tube in the ALP (cathode chamber) close to proton exchange

202

membrane, which led to the electrode spacing of 1 cm. Such immobilization could not

203

be achieved in the cathode chamber of the MCC, hence the electrode spacing of about

204

2 cm was adopted. It was confirmed again that the power generation of MFC can be

205

enhanced by reducing the electrode spacing.22 The above results indicate that the

206

ALMCC can increase the electricity generation.

207

The pH of the catholyte (the medium of microalgae culture) decreased from 7.72

208

± 0.13 to 6.84 ± 0.02 in the ALMCC and from 7.58 ± 0.09 to 6.79 ± 0.06 in the MCC

209

(Figure 2D) till a stable pH of catholyte (nearly 7) were obtained, which might be due

210

to the combined effect of oxygen reduction and CO2 buffering in cathode.23, 31 It was

211

reported that CO2 can be utilized as pH buffer to replace the expensive and

212

non-sustainable buffer solution which is not practical for large scale application.19, 20

213

In general, the pH can be increased from 6.7-7.4 to 8.0-9.0 during algal

214

photosynthesis because of the consumption of carbon dioxide.32-34 To counteract such

215

change, CO2 is injected into the culture medium as a pH controller. In the present

216

study, 10% CO2 was aerated into the cathode compartments of the ALMCC in

217

response to pH controller and carbon source of algal cultivation. Because the biomass

218

concentration of Chlorella vulgaris was the highest at the 10% CO2, which was

219

23.68%, 29.27% and 48.68% higher than that under CO2 levels of 5%, 15% and 20%,

220

respectively (SI Figure S2). It was also demonstrated that the best algal growth

221

potential could be obtained under 10% CO2.35, 36 Too high concentration of CO2 (>

222

20%) would induce low pH, which may cause the decrease of the activity of carbonic 10


Page 10 of 33

Page 11 of 33


223

extracellular anhydrase37,

38

224

cathode chamber. Therefore, 10% CO2 was continuously added, not only for algal

225

growth as carbon source, but also as the catholyte buffer system and pH regulator of

226

ALMCC.

227

COD and nutrients removal in the ALMCC system

and lead to the imbalance of pH between anode and

228

The organics and nutrients removal was also investigated during electricity

229

generation. The COD decreased to 24.16 ± 7.72 mg·L-1 from 181.45 ± 14.68 mg·L-1

230

in the anode of ALMCC and got the removal efficiency of 86.69% (Table 1), which

231

was higher than that in MCC (82.45%). At the end of operation, no COD was detected

232

in the cathodes of both ALMCC and MCC, which might be assimilated by Chlorella

233

vulgaris because it can grow mixotrophically with high biomass concentration.26 As

234

shown in Table 1, NH4+-N concentrations were reduced to less than half of the initial

235

concentration in both the anode chambers of ALMCC and MCC. It could be ascribed

236

to NH4+ transport into the cathode chamber through the Nafion membrane.11 NO3--N

237

and NO2--N were not observed in the cathode chamber because of the absence of

238

aerobic bacteria and the presence of the DO. The constant supply of NH4+ from anode

239

into cathode increased the removal efficiencies of total nitrogen to 70.52% in the

240

ALMCC and 60.29% in the MCC. The removal rates of PO43--P were 69.24% and

241

65.39% in the ALMCC and the MCC systems, respectively. PO43--P concentrations

242

were decreased due to the bacterial uptake in anode compartment and the algal uptake

243

in cathode compartment. The above results indicate that the removal of carbon and

244

nutrients in the ALMCC was higher than that in the MCC system. 11



245

CO2 fixation and lipid accumulation in the ALMCC

246

To explore the advantages of ALMCC on CO2 fixation and lipid accumulation,

247

the cells growth, CO2 fixation rate and lipid accumulation of Chlorella vulgaris in the

248

ALMCC were investigated and compared with the other two control reactors. As

249

indicated in Figure 3A, Chlorella vulgaris grew better in the ALMCC though the

250

same concentrations (0.1 g·L-1) were inoculated. The biomass concentration reached

251

3.04 ± 0.16 g·L-1 on the 6th day, resulting in the biomass productivity of 482.50 ±

252

20.03 mg·L-1·d-1 and the CO2 fixation rate of 887.81 ± 36.86 mg·L-1·d-1. These results

253

clarify that the CO2 fixation rate was 1.88 and 9.98 fold higher than those of in the

254

MCC and ALP, respectively (Figure 3B). On the one hand, Chlorella vulgaris cultured

255

in air-lift-type photobioreactor as the cathode of ALMCC have the higher mixing

256

efficiency, mass transfer and photosynthetic rate compared with the MCC. These

257

advantages of ALMCC are attributed to the regular circulation of algal cultivation in

258

air-lift-type photobioreactor through the air rising from the centric tube, which makes

259

the circulatory liquid flow out on top of the centric tube and gravitationally forced

260

downward.39 However, the gas rising in the cathode of MCC, was the only driving

261

force for the culture mixing of microalgae. It has been well studied that the regular

262

circulation of the culture could lead to a more effective mixing for microalgae growth,

263

which enhances the biomass productivity of microalgae.16,40 Furthermore, the CO2

264

fixation rate of Chlorella vulgaris cultivated in an independent ALP was significantly

265

lower than that in the ALMCC, which could be due to the cation species (Na+, K+,

266

NH4+, Ca2+, and Mg2+) could be transported to cathode chamber in MFCs by Nafion 12


Page 12 of 33

Page 13 of 33


267

membrane and their concentrations in cathode chamber were several orders of

268

magnitude larger than proton concentration.11, 12 These cation species are essential

269

nutrients and micronutrients for the algae growth and metabolism,41 and especially the

270

nitrogen source as a key factor. Because the synthetic municipal wastewater was fed

271

continuously in the anode of ALMCC, nitrogen and minerals were supplied

272

continuously from anode to cathode of ALMCC, which could provide sufficient

273

nutrients for the algae growth. Comparatively, nitrogen concentration in the ALP from

274

the anode effluent of ALMCC was only (17.06 ± 0.69 mg·L-1) and consumed

275

gradually with algal growth. In addition, no additional nitrogen source was supplied

276

(meaning that Chlorella vulgaris grew under nitrogen deficiency), which led to the

277

low biomass productivity, and moreover the cells were severely broken. Unlikely, the

278

algal cells nearly kept the morphologies (with little variation) in the ALMCC and

279

MCC (Figure 3C). It was demonstrated that nitrogen deficiency or starvation pressure

280

could lead to the increase of the cell morphological complexity.26 Thus, the excellent

281

CO2 fixation ability makes the ALMCC as an efficient and potential candidate for

282

CO2 mitigation.

283

With the efficient microalgae cultivation, the lipid accumulation could be

284

achieved besides the power generation and CO2 fixation in this study. CLSM and

285

FTIR were combined to investigate the lipid accumulation of Chlorella vulgaris.

286

Oil-droplet formation of algal cells stained with Bodipy 505/515 was observed by

287

CLSM. As shown in Figure 4A, the green fluorescence (oil-droplet) intensities of

288

microalgae in the ALP were stronger than those cultivated in the ALMCC and MCC, 13



Page 14 of 33

289

which indicated that the lipid content was higher in the ALP. However, there was little

290

difference of green fluorescence intensities in microalgae between the ALMCC and

291

MCC. To further determine accurately the lipid content of Chlorella vulgaris, FTIR

292

spectroscopic method was chosen for the quantitative analysis of the lipid content,

293

and the peaks in the range of 2800-3000 cm-1 can well characterize the lipid content

294

changes of Chlorella vulgaris (Figure 4B). The lipid contents and productivities were

295

calculated by using the equation in the SI. As shown in Figure 4C, the lipid contents

296

of Chlorella vulgaris were 22.47 ± 2.86 and 20.86 ± 1.93% in the ALMCC and MCC,

297

which were about the half of the results from the previous studies,42,

298

because the microalgae were cultivated in the systems with nitrogen sufficiency.

299

However, we observed the different result when Chlorella vulgaris grew in the ALP,

300

the lipid content of Chlorella vulgaris reached 56.75 ± 0.92%, which was 2.53 fold

301

higher than that in the ALMCC. The recent evidence indicates that the lipid content in

302

Chlorella vulgaris could be doubled or even tripled under nitrogen starvation.44

303

However, the lipid productivity (109.44 ± 5.71 mg·L-1·d-1) in the ALMCC was still

304

2.87 and 1.85 fold higher than those in the ALP and MCC, because the biomass

305

productivity of microalgae in the ALMCC was 9.78 and 1.84 fold higher than that in

306

the ALP and MCC, respectively. The above results again demonstrate that the

307

ALMCC can be used to cultivate microalgae as biodiesel feedstock.

308

The energy balance analysis

43

possibly

309

It is necessary to analyze the energy balance of three different systems since the

310

pumping and aerating consumed additional electric energy. The preliminary analysis 14


Page 15 of 33


311

of energy balance included the processes of energy production and consumption but

312

excluded the processes of upstream. It was demonstrated that the municipal

313

wastewater used as culture medium of microalgae could offset most of the energy

314

consumption derived from upstream processing of the algae cultivation.5 The energy

315

production and consumption of three different systems were evaluated as shown in

316

Table 2. Energy production was comprised of electric energy and biodiesel. Electric

317

energy was derived from the power production of the MFC, while biodiesel came

318

from the lipid accumulation of microalgae with the conversion efficiency of 30%

319

from diesel to electricity.23 Energy consumption consisted of the pumping system

320

(anolyte feeding), aeration system (10% CO2 aeration) and biodiesel producing

321

(dewater, oil extraction and fuel conversion). The energy consumption of the pumping

322

system was estimated according to a previous report.45 The aeration system was

323

calculated based on the aeration efficiency of 1.2 kg O2·kWh-1.46 The biodiesel

324

producing includes dewater, oil extraction and fuel conversion processing, while the

325

energy consumption was 0.17, 0.21 and 0.17 kWh per unit of kWh of biodiesel

326

produced, respectively.47 As shown in Table 2, the energy recovery in the ALMCC for

327

6 days reached 1.034 kWh·m-3 and was significantly superior compared to the other

328

two control systems. The highest energy production in the ALMCC could be ascribed

329

to the significantly apparent energy recovery. With regard to the ALP system, the

330

energy production was the least among the three systems, because the biodiesel

331

production was considered as the only energy source, and the biodiesel productivity

332

was still the lowest compared with the other two systems. In practical, the ALMCC 15



333

system could produce more energy. The energy production can be increased by

334

improving the biodiesel and electric energy production. The lipid productivity of the

335

Chlorella vulgaris can be obviously increased through two-stage cultivation process

336

(First stage: Chlorella vulgaris is cultivated under nutrient sufficiency to improve the

337

biomass productivity; Second stage: after the algae have grown to stationary phase,

338

the culture is transferred to nutrient-deficient condition to increase the lipid content).36,

339

43

340

improved through the optimization of cathode catalyst and operation.49, 50

341

Supporting Information

Importantly, the electric energy production in the MFC can be substantially

342

The methods of calculating CO2 fixation rate, lipid content and productivity,

343

energy consumption of pumping system, and the procedures for SEM of microalgae

344

cells are described in the Supporting Information (SI). The standard curve for

345

calculation of algal biomass concentration and the biomass concentrations of

346

microalgae under different CO2 levels are shown in Figure S 1-2. This information is

347

available free of charge via the Internet at http://pubs.acs.org/.

348

Acknowledgements

349

We wish to thank Professor Jo-Shu Chang in Department of Chemical

350

Engineering, National Cheng Kung University, and Professor Xin-Qing Zhao in the

351

school of life science and biotechnology, Dalian University of Technology for the

352

supply of Chlorella vulgaris, ESP-6 for this study. We wish to extend appreciation to

353

Dr. Qidong Zhao and Dr. Pancras Ndokoye in the school of Environmental Science

354

and Technology, Dalian University of Technology for grammar errors and polishing of 16


Page 16 of 33

Page 17 of 33


355

the manuscript.

356

References

357

(1) Ramanathan, V. The greenhouse theory of climate change: a test by an inadvertent

358

global experiment. Science. 1988, 240 (4850), 293-299.

359

(2) Zeng, X.; Danquah, M. K.; Chen, X. D.; Lu, Y. Microalgae bioengineering: From

360

CO2 fixation to biofuel production. Renew. Sust. Energ. Rev. 2011, 15 (6),

361

3252-3260.

362 363

(3) Lam, M. K.; Lee, K. T. Microalgae biofuels: A critical review of issues, problems and the way forward. Biotechnol. Adv. 2012, 30 (3), 673-690.

364

(4) Christenson, L.; Sims, R. Production and harvesting of microalgae for wastewater

365

treatment, biofuels, and bioproducts. Biotechnol. Adv. 2011, 29 (6), 686-702.

366

(5) Clarens, A. F.; Resurreccion, E. P.; White, M. A.; Colosi, L. M. Environmental life

367

cycle comparison of algae to other bioenergy feedstocks. Environ. Sci. Technol.

368

2010, 44 (5), 1813-1819.

369

(6) Dragone, G.; Fernandes, B. D.; Abreu, A. P.; Vicente, A. A.; Teixeira, J. A.

370

Nutrient limitation as a strategy for increasing starch accumulation in microalgae.

371

Appl. Energ. 2011, 88, (10), 3331-3335.

372 373 374 375 376

(7) Logan, B. E. Simultaneous wastewater treatment and biological electricity generation. Water. Sci. Technol. 2005, 52 (1), 31-37. (8) Rabaey, K.; Verstraete, W. Microbial fuel cells: novel biotechnology for energy generation. Trends. Biotechnol. 2005, 23 (6), 291-298. (9) He, Z.; Minteer, S. D.; Angenent, L. T. Electricity generation from artificial 17



377

wastewater using an upflow microbial fuel cell. Environ. Sci. Technol. 2005, 39,

378

5262-5267.

379 380

(10) Wang, H. M.; Park, J. D.; Ren, Z. J. Practical energy harvesting for microbial fuel cells: a review. Environ. Sci. Technol. 2015, 49 (6), 3267-3277.

381

(11) Rozendal, R. A.;Hamelers, H. V.M.; Buisman, C. J. N. Effects of membrane

382

cation transport on pH and microbial fuel cell performance. Environ. Sci. Technol.

383

2006, 40, 5206-5211.

384

(12) Rinaldi, A.; Mecheri, B.; Garavaglia, V.; Licoccia, S.; Di Nardo, P.; Traversa, E.

385

Engineering materials and biology to boost performance of microbial fuel cells: a

386

critical review. Energy. Environ. Sci. 2008, 1 (4), 417-429.

387

(13) Wang, X.; Feng, Y.; Liu, J.; Lee, H.; Li, C.; Li, N.; Ren, N. Sequestration of CO2

388

discharged from anode by algal cathode in microbial carbon capture cells (MCCs).

389

Biosens. Bioelectron. 2010, 25 (12), 2639-2643.

390

(14) González del Campo, A.; Cañizares, P.; Rodrigo, M. A.; Fernández, F. J.; Lobato,

391

J. Microbial fuel cell with an algae-assisted cathode: A preliminary assessment. J.

392

Power. Sources. 2013, 242, 638-645

393

(15) Chiu, S.Y.; Tsai, M.T.; Kao, C.Y.; Ong, S.C.; Lin, C.S. The air-lift

394

photobioreactors with flow patterning for high-density cultures of microalgae and

395

carbon dioxide removal. Eng. Life. Sci. 2009, 9 (3), 254-260.

396

(16) Ranjbar, R.; Inoue, R.; Katsuda, T.; Yamaji, H.; Katoh, S. High efficiency

397

production of astaxanthin in an airlift photobioreactor. J. Biosci. Bioeng 2008,

398

106, (2) 204-207. 18


Page 18 of 33

Page 19 of 33


399

(17) Zhang, Y.; Noori, J. S.; Angelidaki, I. Simultaneous organic carbon, nutrients

400

removal and energy production in a photomicrobial fuel cell (PFC). Energy.

401

Environ. Sci. 2011, 4 (10), 4340-4346.

402

(18) Clauwaert, P. v. d. H., D.; Boon, N.; Verbeken, K.; Verhaege, M.; Rabaey, K.;

403

Verstraete, W. Open air biocathode enables effective electricity generation with

404

microbial fuel cells. Environ. Sci. Technol. 2007, 41 (21), 7564-7569.

405

(19) Fornero, J. J.; Rosenbaum, M.; Cotta, M. A.; Angenent, L. T. Carbon dioxide

406

addition to microbial fuel cell cathodes maintains sustainable catholyte pH and

407

improves anolyte pH, alkalinity, and conductivity. Environ. Sci. Technol. 2010,

408

44 (7), 2728-2734.

409

(20) Fan, Y.; Hu, H.; Liu, H. Sustainable power generation in microbial fuel cells

410

using bicarbonate buffer and proton transfer mechanisms. Environ. Sci. Technol.

411

2007, 41 (23), 8154-8158.

412 413

(21) Ying, K.; Gilmour, D. J.; Zimmerman, W. B. Periodic CO2 dosing strategy for Dunaliella salina batch culture. Int. J. Mol. Sci. 2015, 16 (5), 11509-11521.

414

(22) Cheng, S.; Liu, H.; Logan, B. E. Increased power generation in a continuous flow

415

MFC with advective flow through the porous anode and reduced electrode

416

spacing. Environ. Sci. Technol .2006, 40 (7), 2426-2432.

417

(23) Xiao, L.; Young, E. B.; Berges, J. A.; He, Z. Integrated photo-bioelectrochemical

418

system for contaminants removal and bioenergy production. Environ. Sci.

419

Technol. 2012, 46 (20), 11459-11466.

420

(24) Kokabian, B.; Gude, V. G. Photosynthetic microbial desalination cells (PMDCs) 19



421

for clean energy, water and biomass production. Environ. Sci.: Processes

422

Impacts. 2013, 15 (12), 2178-2185.

423

(25) Ho, S. H.; Chen, C. Y.; Chang, J. S. Effect of light intensity and nitrogen

424

starvation on CO2 fixation and lipid/carbohydrate production of an indigenous

425

microalga Scenedesmus obliquus CNW-N. Bioresour. Technol. 2012, 113,

426

244-252.

427

(26) Zhang, Y. M.; Chen, H.; He, C. L.; Wang, Q. Nitrogen starvation induced

428

oxidative stress in an oil-producing green alga Chlorella sorokiniana C3. PLoS

429

One 2013, 8 (7), e69225.

430

(27) Pistorius, A. M.; DeGrip, W. J.; Egorova-Zachernyuk, T. A. Monitoring of

431

biomass composition from microbiological sources by means of FT-IR

432

spectroscopy. Biotechnol. Bioeng. 2009, 103 (1), 123-129.

433

(28) Meng, Y. Y.; Yao, C. H.; Xue, S.; Yang, H. B. Application of Fourier transform

434

infrared (FT-IR) spectroscopy in determination of microalgal compositions.

435

Bioresour. Technol. 2014, 151, 347-354.

436

(29) Zimmerman, W. B.; Zandi, M.; Hemaka Bandulasena, H. C.; Tesař, V.; James

437

Gilmour, D.; Ying, K. Design of an airlift loop bioreactor and pilot scales studies

438

with fluidic oscillator induced microbubbles for growth of a microalgae

439

Dunaliella salina. Appl. Energ. 2011, 88 (10), 3357-3369.

440

(30) He, Z.; Wagner, N.; Minteer, S. D.; Angenent, L. T. An upflow microbial fuel

441

cell with an interior cathode: assessment of the internal resistance by impedance

442

spectroscopy. Environ. Sci. Technol. 2006, 40 (17), 5212-5217. 20


Page 20 of 33

Page 21 of 33


443

(31) Pandit, S.; Nayak, B. K.; Das, D. Microbial carbon capture cell using

444

cyanobacteria for simultaneous power generation, carbon dioxide sequestration

445

and wastewater treatment. Bioresour. Technol. 2012, 107, 97-102.

446

(32) Han, F.; Huang, J.; Li, Y.; Wang, W.; Wan, M.; Shen, G.; Wang, J. Enhanced

447

lipid productivity of Chlorella pyrenoidosa through the culture strategy of

448

semi-continuous cultivation with nitrogen limitation and pH control by CO2.

449

Bioresour. Technol. 2013, 136, 418-424.

450 451

(33) Chisti, Y. Biodiesel from microalgae beats bioethanol. Trends. Biotechnol. 2008, 26 (3), 126-131.

452

(34) Camacho Rubio, F.; Acień Fernańdez, F. G.; Sańchez Pe´rez, J. A.; Garcıá

453

Camacho, F.; Molina Grima, E. Prediction of dissolved oxygen and carbon

454

dioxide concentration profiles in tubular photobioreactors for microalgal culture.

455

1999, 61 (1), 71-86.

456

(35) Tang, D.; Han, W.; Li, P. L.; Miao, X. L.; Zhong, J. J. CO2 biofixation and fatty

457

acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in

458

response to different CO2 levels. Bioresour. Technol. 2011, 102 (3), 3071-3076.

459

(36) Ho, S. H.; Chen, W. M.; Chang, J. S. Scenedesmus obliquus CNW-N as a

460

potential candidate for CO2 mitigation and biodiesel production. Bioresour.

461

Technol. 2010, 101 (22), 8725-8730.

462 463 464

(37) Martin, C. L.; Tortell, P. D. Bicarbonate transport and extracellular carbonic anhydrase in marine diatoms. Physiol.Plantarum. 2008, 133 (1), 106-116. (38) Rost, B.; Riebesell, U.; Burkhardt, S.; Sultemeyer, D. Carbon acquisition of 21



465

bloom-forming marine phytoplankton. Limnol. Ocenogr. 2003, 48, (1), 55-67.

466

(39) Contreras, A.; Chisti, Y.; Molina, E. A reassessment of relationship between riser

467

and downcomer gas holdups in airlift reactors. Chem. Eng. Sci. 1998, 53 (23),

468

4151-4154.

469

(40) Oncel, S.; Sukan, F. V. Comparison of two different pneumatically mixed

470

column photobioreactors for the cultivation of Artrospira platensis (Spirulina

471

platensis). Bioresour. Technol. 2008, 99 (11), 4755-4760.

472

(41) Li, Y.; Zhou, W.; Hu, B.; Min, M.; Chen, P.; Ruan, R. R., Integration of algae

473

cultivation as biodiesel production feedstock with municipal wastewater

474

treatment: strains screening and significance evaluation of environmental factors.

475

Bioresour. Technol. 2011, 102 (23), 10861-10867.

476

(42) Harwati, T. U.; Willke, T.; Vorlop, K. D. Characterization of the lipid

477

accumulation in a tropical freshwater microalgae Chlorococcum sp. Bioresour.

478

Technol. 2012, 121, 54-60.

479

(43) Jiang, L.; Luo, S.; Fan, X.; Yang, Z.; Guo, R. Biomass and lipid production of

480

marine microalgae using municipal wastewater and high concentration of CO2.

481

Appl. Energ. 2011, 88 (10), 3336-3341.

482

(44) Converti, A.; Casazza, A. A.; Ortiz, E. Y.; Perego, P.; Del Borghi, M. Effect of

483

temperature and nitrogen concentration on the growth and lipid content of

484

Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem

485

Eng Process. 2009, 48 (6), 1146-1151.

486

(45) Kim, J., Kim, K.; Ye, H.; Lee, E.; Shin, C.; McCarty, P. L.; Bae, J. Anaerobic 22


Page 22 of 33

Page 23 of 33


487

fluidized bed membrane bioreactor for wastewater treatment. Environ. Sci.

488

Technol. 2011, 45, 576-581.

489 490

(46) Force, J. T., Design of munnicipal wastewater treatment plants: WEF manual of practice No.8; Water Environment Federation:Alexandria,. 1998.

491

(47) Batan, L.; Quinn, J.; Willson, B.; Bradley, T., Net energy and greenhouse gas

492

emission evaluation of biodiesel derived from microalgae. Environ. Sci. Technol.

493

2010, 44 (20), 7975-7980.

494 495

(48) Kadam, K. L., Environmental implications of power generation via coal-microalgae cofiring. Energy. 2002, 27 (10), 905-922.

496

(49) Wang, Z.; Cao, C. L.; Zheng, Y.; Chen, S. L.; Zhao, F. Abiotic oxygen reduction

497

reaction catalysts used in microbial fuel cells. ChemElectroChem 2014, 1 (11),

498

1813-1821.

499

(50) Qiu, Z. Z.; Su, M.; Wei, L. L.; Han, H. L.; Jia, Q. B.; Shen, J. Q. Improvement of

500

microbial fuel cell cathodes using cost-effective polyvinylidene fluoride. J.

501

Power. Sources. 2015, 273, 566–573.

502

23



Page 24 of 33

503 504

Table 1. Characteristics of the synthetic solution in the ALMCC and MCC (mg·L-1)

Anode influent of ALMCC Anode effluent of ALMCC Cathode effluent of ALMCC Anode influent of MCC Anode effluent of MCC Cathode effluent of MCC

COD

NH4+-N

PO43--P

181.45 ± 14.68 24.16 ± 7.72 N/D 181.45 ± 14.68 32.03 ± 3.76 N/D

39.04 ± 1.23 17.06 ± 0.69 11.51 ± 0.99 39.04 ± 1.23 17.89 ± 0.74 15.50 ± 0.70

3.62 ± 0.19 2.14 ± 0.15 1.11 ± 0.08 3.62 ± 0.19 2.31 ± 0.2 1.25 ± 0.12

505

24


Page 25 of 33


506 507

Table 2. Energy production and consumption in the ALMCC, MCC and ALP ALMCC

Input

Output

Net

MCC

ALP

-3

-3

(kWh·m )

(kWh·m )

(kWh·m-3)

pump

-0.000018

- 0.000018

N/A

aeration

-0.082

-0.082

-0.082

biodiesel production

-1.192

-0.619

-0.382

electricity

0.140

0.075

N/A

biodiesel

2.168

1.126

0.695

total

1.034

0.501

0.231

508

25



509 510

A

511 512

B

513 514

C

515 516 517

Figure 1. Structure (A), photo (B), and schematic illustration of the functional principles (C) of ALMCC. 26


Page 26 of 33

Page 27 of 33


518 519

A

520 521

B

522 523 524

C

525 27



526 527

D

528 529

Figure 2. Performance of the ALMCC and MCC: (A) Voltage outputs with time; (B)

530

Polarization and power density curves; (C) Changes of dissolved oxygen with time;

531

(D) pH changes with time. Control: MCC.

532

28


Page 28 of 33

Page 29 of 33


533 534

A

535 536

B

537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 29



553 554

C

555 556

Figure 3. The performance of cell growth and CO2 fixation efficiency: (A) Biomass

557

concentration with time; (B) CO2 fixation rate; (C) SEM images and photo of algae in

558

three reactors. a: ALMCC, b: MCC, c: ALP d: the microalgae suspension in three

559

reactors. Control 1: MCC and control 2: ALP.

560

30


Page 30 of 33

Page 31 of 33


561

A

562 563

B

564 565

C

566 567

Figure 4. Lipid accumulation: (A) CLSM images of algae labeled in vivo with

568

Bodipy 505/515. a: ALMCC, b: MCC, c: ALP; (B) Expanded part of infrared spectra 31



569

showing the band around 3000-2800 cm-1 of algae. (C) Lipid content and productivity

570

of algae in three reactors. Control 1: MCC and control 2: ALP.

32


Page 32 of 33

Page 33 of 33


84x47mm (300 x 300 DPI)


CO 2 Fixation, Lipid Production, and Power ... - ACS Publications

Recommend Documents