You are on page 1of 7

RSC Advances

Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

View Article Online


PAPER View Journal | View Issue

Effect of algal species and light intensity on the


performance of an air-lift-type microbial carbon
Cite this: RSC Adv., 2016, 6, 25094
capture cell with an algae-assisted cathode†
Xia Hu, Jiti Zhou* and Baojun Liu

The performances were investigated for air-lift-type microbial carbon capture cells (ALMCCs) with Chlorella
vulgaris and Chlorella sp. as cathodic microorganisms. The two ALMCC systems showed differences in CO2
fixation, lipid production and power generation. The ALMCC system with Chlorella vulgaris produced
a maximum power density of 558.22 mW m3, a CO2 fixation rate of 223.68 mg L1 d1 and lipid
productivity of 21.75 mg L1 d1, indicating that Chlorella vulgaris performed better than Chlorella sp. By
conducting further experiments with Chlorella vulgaris under different light intensities (2.4, 5.0, 8.9 and
11.4 W m2), the ALMCC was found to be sensitive to light intensities. The maximum power outputs and
CO2 fixation rate were observed under light intensity of 8.9 W m2 (972.5 mW m3 and 887.8 mg L1
Received 9th December 2015
Accepted 28th February 2016
d1, respectively). The lipid productivity was increased with the light intensity from 2.4 to 11.4 W m2.
However, there was no difference in lipid productivities between light intensities of 8.9 and 11.4 W m2
DOI: 10.1039/c5ra26299b
(p > 0.05). These results suggested that 8.9 W m2 was the optimal light intensity for CO2 fixation, lipid
www.rsc.org/advances production and power generation of the ALMCC with Chlorella vulgaris.

biodiesel productivity because of the low mixing efficiency and


1. Introduction photosynthetic rate.10 Fortunately, this inefficiency has been
The concern about global warming and the energy crisis has addressed by the air-li-type microbial carbon capture cell
encouraged researchers to nd the solution for CO2 capture and (ALMCC) which was constructed for the rst time using the air-
alternative sources of energy.1,2 Microalgae cultivation for li-type photobioreactor (ALP) as the cathode chamber of
photosynthetic CO2 xation and biodiesel production is MCC.11 Owing to the ALP with the excellent mixing efficiency
considered to be a promising approach that is energy-saving and best volumetric gas transfer through its liquid cylindrical
and environment-friendly, due to the fact that microalgae column, the microalgae can yield the maximum biomass
have high photosynthetic efficiency, biomass productivity and productivity with a better specic growth rate.12,13 It was also
lipid content.3,4 Besides, oxygen is generated simultaneously demonstrated that the ALMCC perform better than MCC in
when microalgae convert sunlight, water and CO2 to algal terms of power generation, CO2 xation efficiency, municipal
biomass through the photosynthesis process, and this oxygen wastewater treatment efficiency and lipid productivity. In
can be used as the electron acceptor for microbial fuel cells addition, the preliminary analysis of energy balance suggested
(MFCs).4 Therefore, microalgae have been cultivated in the that the net energy of the ALMCC system was signicantly
cathode chamber of MFCs for the oxygen production to superior to other systems (MCC and ALP) and this reactor could
decrease the over-potential of the oxygen reduction reaction.5,6 theoretically produce enough energy to cover its consumption.11
The microbial carbon capture cell (MCC) as a new sustainable In the ALMCC, the synthetic municipal wastewater is
form of MFCs with an algae-assisted cathode, was constructed continuously fed into the anode chamber for a continuous
for CO2 capture of discharged from anode in MFCs with generation of electricity, and the anode effluent is used to
simultaneous wastewater treatment and electricity genera- cultivate microalgae in the cathode chamber, thereby reducing
tion.7–9 However, MCCs generally exhibit low biomass produc- the need of chemical fertilizers and algae's life cycle burden.14
tivities of microalgae, resulting in low CO2 xation rate and The microalgae cultivated in municipal wastewater have a long
history especially the Chlorella genus because they could grow
mixotrophically with high biomass accumulation in municipal
Key Laboratory of Industrial Ecology and Environmental Engineering, Ministry of wastewater with organic carbon.15,16 Additionally, Chlorella
Education, School of Environmental Science and Technology, Dalian University of species are very common to be used as CO2 sequestration and
Technology, Linggong Road 2, Dalian 116024, China. E-mail: jitizhou502@163.com;
biodiesel production because it has high photosynthetic effi-
Fax: +86 41184706252; Tel: +86 41184706252
† Electronic supplementary information (ESI) available. See DOI:
ciency to x CO2 and their lipids are mainly composed of C16
10.1039/c5ra26299b and C18 (C16:0, C18:0, C18:2 and C18:3), which are appropriate

25094 | RSC Adv., 2016, 6, 25094–25100 This journal is © The Royal Society of Chemistry 2016
View Article Online

Paper RSC Advances

fatty acids for biodiesel synthesis.15,17 It was also found that


Chlorella vulgaris and Chlorella sp. have the highest tolerances
for municipal wastewater, xation efficiency to high CO2
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

concentration (10% CO2) and lipid content among ten Chlorella


strains. However, to the date, few studies have been investigated
for comparing the performances of MFCs with different Chlor-
ella strains cultivated in the cathode chamber. Furthermore,
light intensity is one of the most important environmental
factors that would affect the photosynthesis efficiency, meta-
bolic pathway, CO2 xation and electricity generation of
microalgae. In other words, both insufficient and excessive light
may lead to low biomass concentration, CO2 xation and
bioelectricities.18,19 In this context, optimum light intensity is
a great scientic and technological challenge to the develop-
ment of the ALMCC system. Therefore, one of the objectives of
the current study is to investigate and compare the effect of two
Chlorella strains on the performance (algal biomass accumu-
lation, CO2 xation, biodiesel production and power genera-
tion) of ALMCC. In addition, the effect of light intensity on the
performance of ALMCC is also studied. Finally, the best per-
forming strain was selected for ALMCC system and the
optimum light intensity was determined for the cathode
chamber of ALMCC based on the ALMCC system in this study.

2. Material and methods


2.1 Microalgae
Two algae strains were used in the present study, Chlorella
vulgaris (ESP-6) was obtained from National Cheng Kung
University and Chlorella sp. was purchased from Freshwater
Algae Culture Collection, Institute of Hydrobiology, Chinese Fig. 1 Schematic illustration of the functional principles of the ALMCC
Academy of Sciences (Wuhan, China). Prior to experiment, both (A) and (B) photo of the reactor.
the Chlorella strains were cultivated in autoclaved Erlenmeyer
ask with BG11 medium.16,20
39.04 mg L1; PO43–P, 3.62 mg L1; NaHCO3, 600 mg L1;
2.2 ALMCC construction and operation NaCl, 12.5 mg L1; MgSO4, 6.25 mg L1; CaCl2, 33.34 mg L1
and 1 mL L1 of trace elements. The synthetic municipal
Two-chamber ALMCC was constructed with Plexi-glass and it wastewater was fed continuously into the anode chamber at
was separated by a proton exchange membrane (126 cm2, a ow rate of 0.8 mL min1. To prevent the growth of algae in
Naon 117, Dupont, US). As shown in Fig. 1, the anode chamber the anode chamber, it was covered by tinfoil. The anode effluent
was a simple cube, whereas the cathode chamber of ALMCC was was autoclaved at 121  C, followed by cooling to room temper-
an air-li-type cubical photobioreactor with a centric tube. This ature, and used as medium of microalgae cultivation in the
design resulted in the liquid volume of anode chamber was cathode chamber of the ALMCC. The cathode chamber was
600 mL while the liquid volume of cathode chamber was inoculated with the microalgae and the initial inoculum
500 mL. 10% CO2 was aerated into the cathode chamber of biomass was 0.10 g L1. The light intensities studied were
ALMCC with 60 mL min1 during microalgae cultivation. A operated with 2.4, 5.0, 8.9 and 11.4 W m2, and controlled by
10 cm long carbon brush (5 cm in diameter) was used as the varying the number of uorescent lamps at a continuous
anode electrode. Prior to usage, the carbon brush was pre- illumination.
treated by heating at 450  C for 30 min.7 The cathode electrode
was carbon ber cloth (5 cm  15 cm ¼ 75 cm2). Then the anode
and cathode electrodes were connected by copper wires and the 2.3 Measurement and analysis
external resistance was 1000 U. Saturated calomel electrode The cell voltage was recorded every 30 min with a data acqui-
(SCEs; Spsic-Rex Instrument Factory, China) was inserted into sition system (PISO-813, ICP DAS Co., Ltd.). The power density
anode chamber as a reference electrode. was calculated by the effective volume of anode chamber.21 DO
Anodic effluent from a MFC operated more than half a year was measured by a DO meter (YSI 550A, America). The biomass
was used as inoculum of anodic biolm. The synthetic munic- concentrations of two strains were determined by measuring
ipal wastewater contained sodium acetate, 280 mg L1; NH4+–N, the optical density of the algal suspension6,22 with an UV-Vis

This journal is © The Royal Society of Chemistry 2016 RSC Adv., 2016, 6, 25094–25100 | 25095
View Article Online

RSC Advances Paper

Spectrophotometer (Jasco V-560) at a wavelength of 690 nm


(OD690). The OD690 values were converted to biomass concen-
trations using the standard curves shown in Appendices
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

Fig. A.1.† CO2 xation rate was calculated according to


a previous study23 and the equation is shown in the
Appendices.† The oil-droplet formation of the two algae stained
with Bodipy 505/515 was observed by confocal laser scanning
microscopy (CLSM, OlympusFV1000).24 The lipid content was
determined using the method of FTIR spectroscopy (Bruker
VERTEX 70, Germany) and its accuracy has been validated by
traditional methods.25,26 The measurements of lipid content
and productivity are described in the Appendices.†

3. Results and discussion


3.1 Effect of algal species on the performance of ALMCC
3.1.1 Effect of algal species on power generation. To
investigate the effect of algal species on the power generation
performance of ALMCC, two different microalgae strains,
Chlorella vulgaris and Chlorella sp. were incubated in two
cathode chambers of ALMCCs and the experiment was operated
under the light intensity of 2.4 W m2. As shown in Fig. 2A, the
maximum voltage output (external resistance of 1000 U) of
0.429 V was generated in ALMCC with Chlorella vulgaris, which
was signicantly higher than that of the Chlorella sp. (0.379 V).
The polarization and power density curves were shown in
Fig. 2B, it is obvious that Chlorella vulgaris exhibited a peak
power density of 10.95% higher compared to Chlorella sp. Along
with power generation, the dissolved oxygen (DO) in the ALMCC
system with Chlorella vulgaris (5.65 mg L1) was also higher
than that with Chlorella sp. (5.20 mg L1) (Fig. 2C). These results
indicate that the power output of ALMCC system is closely
related to DO produced by microalgae in the cathode chamber,
due to a signicant inuence of the DO concentration in the
cathode compartment on the MFC power generation.6,8 In the
current study, DO concentrations of both ALMCCs with two
strains were increased linearly with the increasing algal
biomass concentrations, but the biomass concentration of
Chlorella vulgaris was obviously higher than that of Chlorella
sp., indicating that the power generation indirectly relied on the
microalgae concentration in the cathode compartment. It was
also reported that the power outputs are related to oxygenic
photosynthetic activities of microalgae.27 In addition, the
difference of electricity production between two ALMCC Fig. 2 Performance for electricity generation of the ALMCCs with two
systems (one with Chlorella vulgaris and another with Chlorella Chlorella strains: (A) voltage outputs with time; (B) polarization and
power density curves; (C) changes of dissolved oxygen with time.
sp.), was also due to the fact that the internal resistance
(138.00 U) of the ALMCC with Chlorella vulgaris is lower than
that with Chlorella sp. (158.45 U). The internal resistance was
proven to be a key factor on the electricity production of chambers of ALMCC systems showed different growth variation
MFCs.21,28 In this study, the concentration of DO of ALMCC with with time (Fig. 3A). It was noticed that the biomass concentra-
Chlorella vulgaris was higher than that with Chlorella sp., which tion achieved 0.80 g L1 for Chlorella vulgaris, and consequently
could lead to lower internal resistance. It has been well evi- its biomass productivity attained 121.57 mg L1 d1, while the
denced that a higher concentration of DO can decrease the biomass productivity of Chlorella sp. was only 70.16 mg L1 d1
internal resistance.29 with 0.54 g L1 as biomass concentration. It is commonly
3.1.2 Effect of algal species on CO2 xation and lipid believed that higher biomass productivity could be benecial
accumulation. The comparison of growth characteristics for CO2 xation.23 Therefore, CO2 xation rate of Chlorella vul-
between Chlorella vulgaris and Chlorella sp. in the cathode garis attained 223.68 mg L1 d1, which was 44.17% higher than

25096 | RSC Adv., 2016, 6, 25094–25100 This journal is © The Royal Society of Chemistry 2016
View Article Online

Paper RSC Advances

that of Chlorella sp. (Fig. 3B). This might be originating from the
difference of algal species, cell size and growth rate. In other
words, the biomass accumulation and CO2 xation efficiency
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

could be affected by the cell size, growth rate and environmental


requirement of species.30,31 In the present study, the cell size
and growth rate of Chlorella vulgaris (about 5 mm and 0.406 d1,
respectively) were larger and higher than those of Chlorella sp.
(about 3 mm and 0.359 d1, respectively), indicating that the
CO2 xation rate of Chlorella vulgaris was higher than those of
Chlorella sp. It was also reported that much more CO2 are
required to satisfy carbon demand in larger or rapidly growing
cells.31 These results indicated that Chlorella vulgaris was
a better candidate to be cultivated in the ALMCC for CO2
xation.
The lipid contents in microalgae are signicantly different
among various species. To clearly visualize the oil-droplet
formation of the two Chlorella stains, the algal cells were
stained with Bodipy 505/515 and observed by CLSM. As shown
in Fig. 3C, the green uorescence (oil-droplet) intensities of
Chlorella vulgaris were higher than those of Chlorella sp. To
further accurately determine the lipid content of algal cells,
FTIR spectroscopic method was chosen for the quantitative
analysis of the lipid content. The peaks in the range of 2800–
3000 cm1 could be assigned to microalgae and was shown in
Fig. 3D. The lipid contents and productivities were calculated by
using the equation in the Appendices.† As shown in Fig. 3E, the
lipid content of Chlorella vulgaris and Chlorella sp. were 17.90%
and 17.27%, respectively. No signicant difference of lipid
content was observed between the two strains (p > 0.05), but the
lipid productivity of Chlorella vulgaris (21.75 mg L1 d1) was
44.32% higher than those of Chlorella sp. This was due to higher
biomass productivity of Chlorella vulgaris.

3.2 Effect of irradiance on the performance of ALMCC


3.2.1 Effect of light intensity on the power generation. To
better understand the inuence of illumination on the ALMCC
system, a total of four different light intensities (2.4, 5.0, 8.9 and
11.4 W m2) were applied to the system and the impact on the
performance of electricity generation was investigated. As
shown in Fig. 4A, an increase in voltage output was observed as
the light intensity increased from 2.4 to 8.9 W m2 (from 0.429
to 0.490 V), while the result turned down when light intensity
was further increased to 11.4 W m2 (0.478 V). The polarization
and power density curves of ALMCC system under four different
light intensities are shown in Fig. 4B. The maximum power
density of the system was 972.5 mW m3 under the intensity of
8.9 W m2, which was higher 42.60%, 26.79% and 19.22% than
that at 2.4 W m2, 5.0 W m2 and 11.4 W m2, respectively. It is
apparent that the electricity generation was obviously improved
with increasing light intensity but too much light resulted in the
Fig. 3 The performance of cell growth, CO2 fixation efficiency and
decrease of peak power and voltage output. However, it was
lipid accumulation of the ALMCCs with two Chlorella strains: (A)
biomass concentration with time; (B) CO2 fixation rate. (C) CLSM previously reported that the increase of the illumination
images of algae labeled in vivo with Bodipy 505/515; (D) expanded part intensity could signicantly increase the electricity production
of infrared spectra showing the band around 3000–2800 cm1 of by promoting the production of DO.29,32 This unconformity may
algae. (E) Lipid content and productivity of algae. be from the difference of microbial species and operating
conditions. In this study, Chlorella vulgaris (ESP-6) was found to

This journal is © The Royal Society of Chemistry 2016 RSC Adv., 2016, 6, 25094–25100 | 25097
View Article Online

RSC Advances Paper

with light intensity, demonstrating again that the cathode


reaction benets from oxygen produced by Chlorella vulgaris
photosynthesis. The above results demonstrated that 8.9 W m2
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

was the optimal light intensity for power generation in the


ALMCC. In addition, it was found that the power density of
ALMCC at optimal light intensity was highest compared with
other MCCs (Table A.1†). It might be due to that the decreased
electrode spacing and a stable pH of the catholyte (nearly 7) lead
to the enhanced power generation.11
3.2.2 Effect of light intensity on the CO2 xation and lipid
accumulation. For photoautotrophic algae, the cell growth and
CO2 xation are signicantly inuenced by the irradiance.
Furthermore, the light intensity may also change the
biochemical compositions in microalgae cell such as the lipid
content. In the current study, the effect of varying light intensity
on the growth of Chlorella vulgaris was investigated and the
biomass concentration was reported in Fig. 5A. A signicant
increase in the biomass concentration was observed with
increasing light intensity, and the highest biomass concentra-
tion was obtained at 8.9 W m2 (3.04 g L1). Similarly, as shown
in Fig. 5B, the CO2 xation also increased dramatically along
with the rising light intensity, with the highest value of 887.8
mg L1 d1 at the light intensity of 8.9 W m2, which was 3.97
and 2.47 fold higher than those at the light intensity of 2.4
W m2 and 5.0 W m2, respectively. However, further increase
in light intensity to 11.4 W m2 resulted in the decrease of both
biomass concentration and CO2 xation rate (2.60 g L1 and
780.54 mg L1 d1, respectively), indicating that the cell growth
of Chlorella vulgaris was inhibited when light intensity was
further increased to 11.4 W m2. Similar photo-inhibition
phenomenon was also found in other previous studies.34,35 It
was also demonstrated that microalgae might be susceptible to
photo-inhibition under too high light intensity.33 Therefore,
a further increase of light intensity would lead to the decline of
photo-synthetic activity of algae and so lower the biomass
concentration and CO2 xation rate. In this study, the excellent
biomass concentration and CO2 xation rate prove that the light
intensity of 8.9 W m2 was an optimal light intensity for cell
growth of Chlorella vulgaris and CO2 capture.
The light intensity can not only inuence the cell growth and
CO2 xation in the photosynthetic system, but also affect the
lipids accumulation. To clearly visualize the oil-droplet change
Fig. 4 Performance of the electricity generation under different light of Chlorella vulgaris under different light intensity, the algal
intensity: (A) voltage outputs with time; (B) polarization and power cells were stained with Bodipy 505/515 and were observed by
density curves; (C) changes of dissolved oxygen with time. CLSM. As shown in Fig. 5C, the green uorescence (oil-droplet)
intensities of Chlorella vulgaris were increased gradually with
the increasing of light intensity. It was indicated that the lipid
be susceptible to photo-inhibition at light intensity further content of algal cells was increased as the light intensity
increased to 11.4 W m2, which falls in the agreement with increased. To further determine accurately the lipid content of
previous reports.33,34 Thus, further increased light intensity algal cells, FTIR spectroscopic method was chosen for the
resulted in the decrease of biomass concentration, which led to quantitative analysis of the lipid content and the microalgae
the lowering of DO (8.49 mg L1). As clearly shown, DO was assignment peaks in the range of 2800–3000 cm1 were shown
lowered up to 12.83% compared with the intensity of 8.9 W m2 in Fig. 5D. The lipid contents and productivities were calculated
(Fig. 4C). It was also reported that a further increased light by using the equation in the Appendices.† It was found that the
intensity could lead to the decrease of photosynthetic activity, lipid content of the dry weight was increased signicantly from
hence it lowers the electron transfer potential.33 DO concen- 17.90 to 30.02% with the light intensity increasing from 2.4 to
tration and power density of ALMCC exhibited a similar trend 11.4 W m2 (Fig. 5E). Other studies have also shown that the

25098 | RSC Adv., 2016, 6, 25094–25100 This journal is © The Royal Society of Chemistry 2016
View Article Online

Paper RSC Advances

lipid content of microalgae could be signicantly increased


under high light intensity.23 Also, a great amount of light energy
(ATP and NADH) in the form of high light intensity is required
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

for the production of triacylglycerides to avoid any photo-


chemical damage in the microalgae cells.36 Furthermore, the
lipid contents increased gradually with the increase of light
intensity, and the lipid productivity increased with the light
intensity ranging from 2.4 to 11.4 W m2 (21.75, 39.79, 109.44
and 128.11 mg L1 d1, respectively). However, there is no
difference of lipid productivities between light intensity of 8.9
and 11.4 W m2 (p > 0.05). According to the results above, it is
indicated that 8.9 W m2 was the optimal light intensity for CO2
xation and lipid accumulation in the ALMCC. Moreover, the
lipid productivity of microalgae in ALMCC at optimal light
intensity was relatively high compared with ALPs due to its high
biomass productivity (Table A.1†). The main reason was prob-
ably that constant supplement of cation species into cathode
chamber of ALMCC through the Naon membrane.37,38 These
cation species are essential nutrients and micronutrients for the
algae growth and metabolism.16

4. Conclusion
In this study, the effect of algal species (Chlorella vulgaris and
Chlorella sp.) and light intensity on the performance of ALMCC
were investigated. The ALMCC incubating Chlorella vulgaris
performed better than that one with Chlorella sp., resulting
from the high biomass productivity and CO2 xation rate of
Chlorella vulgaris. Moreover, the light intensity showed
a profound impact on the performance of ALMCC and the
intensity of 8.9 W m2 was found to be an optimal light inten-
sity for power generation and CO2 capture. Lipid productivity
was the highest at the light intensity of 11.4 W m2. However,
there is no difference of lipid productivities between light
intensity of 8.9 to 11.4 W m2 (p > 0.05), indicating that 8.9
W m2 was the optimal light intensity for performance of the
ALMCC with Chlorella vulgaris.

Acknowledgements
We wish to thank Professor Jo-Shu Chang in Department of
Chemical Engineering, National Cheng Kung University, and
Professor Xin-Qing Zhao in the school of life science and
biotechnology, Dalian University of Technology for the supply of
Chlorella vulgaris, ESP-6 for this study. We wish to extend
appreciation to Dr Pancras Ndokoye in the school of Environ-
mental Science and Technology, Dalian University of Tech-
nology for polishing of the manuscript.

References
Fig. 5 The performance of cell growth, CO2 fixation efficiency and
1 R. J. Brecha, Energy Policy, 2008, 36, 3492–3504.
lipid accumulation under different light intensity: (A) biomass
concentration with time; (B) CO2 fixation rate. (C) CLSM images of 2 S. B. Velasquez-Orta, T. P. Curtis and B. E. Logan, Biotechnol.
algae labeled in vivo with Bodipy 505/515; (D) expanded part of Bioeng., 2009, 103, 1068–1076.
infrared spectra showing the band around 3000–2800 cm1 of algae; 3 X. Zeng, M. K. Danquah, X. D. Chen and Y. Lu, Renewable
(E) lipid content and productivity of algae. Sustainable Energy Rev., 2011, 15, 3252–3260.
4 Y. Chisti, Biotechnol. Adv., 2007, 25, 294–306.

This journal is © The Royal Society of Chemistry 2016 RSC Adv., 2016, 6, 25094–25100 | 25099
View Article Online

RSC Advances Paper

5 Y. Zhang, J. S. Noori and I. Angelidaki, Energy Environ. Sci., 22 B. Kokabian and V. G. Gude, Environ. Sci.: Processes Impacts,
2011, 4, 4340–4346. 2013, 15, 2178–2185.
6 L. Xiao, E. B. Young, J. A. Berges and Z. He, Environ. Sci. 23 S. H. Ho, C. Y. Chen and J. S. Chang, Bioresour. Technol.,
Published on 01 March 2016. Downloaded by Middle East Technical University (Orta Dogu Teknik U) on 05/05/2016 02:06:03.

Technol., 2012, 46, 11459–11466. 2012, 113, 244–252.


7 X. Wang, Y. Feng, J. Liu, H. Lee, C. Li, N. Li and N. Ren, 24 Y. M. Zhang, H. Chen, C. L. He and Q. Wang, PLoS One, 2013,
Biosens. Bioelectron., 2010, 25, 2639–2643. 8, e69225.
8 A. González del Campo, P. Cañizares, M. A. Rodrigo, 25 A. M. Pistorius, W. J. DeGrip and T. A. Egorova-Zachernyuk,
F. J. Fernández and J. Lobato, J. Power Sources, 2013, 242, Biotechnol. Bioeng., 2009, 103, 123–129.
638–645. 26 Y. Meng, C. Yao, S. Xue and H. Yang, Bioresour. Technol.,
9 Y. Cui, N. Rashid, N. Hu, M. S. U. Rehman and J.-I. Han, 2014, 151, 347–354.
Energy Convers. Manage., 2014, 79, 674–680. 27 A. J. McCormick, P. Bombelli, A. M. Scott, A. J. Philips,
10 G. Dragone, B. D. Fernandes, A. P. Abreu, A. A. Vicente and A. G. Smith, A. C. Fisher and C. J. Howe, Energy Environ.
J. A. Teixeira, Appl. Energy, 2011, 88, 3331–3335. Sci., 2011, 4, 4699–4709.
11 X. Hu, B. J. Liu, J. T. Zhou, R. F. Jin, S. Qiao and G. F. Liu, 28 Z. He, N. Wagner, S. D. Minteer and L. T. Angenent, Environ.
Environ. Sci. Technol., 2015, 49, 10710–10717. Sci. Technol., 2006, 40, 5212–5217.
12 S. Y. Chiu, M. T. Tsai, C. Y. Kao, S. C. Ong and C. S. Lin, Eng. 29 Y. C. Wu, Z. J. Wang, Y. Zheng, Y. Xiao, Z. H. Yang and
Life Sci., 2009, 9, 254–260. F. Zhao, Appl. Energy, 2014, 116, 86–90.
13 R. Ranjbar, R. Inoue, T. Katsuda, H. Yamaji and S. Katoh, J. 30 L. Cheng, L. Zhang, H. Chen and C. Gao, Sep. Purif. Technol.,
Biosci. Bioeng., 2008, 106, 204–207. 2006, 50, 324–329.
14 A. F. Clarens, E. P. Resurreccion, M. A. White and 31 S. Burkhardt, I. Zondervan and U. Riebesell, Geochim.
L. M. Colosi, Environ. Sci. Technol., 2010, 44, 1813–1819. Cosmochim. Acta, 1999, 63, 3729–3741.
15 G. Petkov and G. Garcia, Biochem. Syst. Ecol., 2007, 35, 281– 32 H. He, M. Zhou, J. Yang, Y. Hu and Y. Zhao, Bioprocess
285. Biosyst. Eng., 2014, 37, 873–880.
16 Y. Li, W. Zhou, B. Hu, M. Min, P. Chen and R. R. Ruan, 33 A. E. Inglesby, K. Yunus and A. C. Fisher, Phys. Chem. Chem.
Bioresour. Technol., 2011, 102, 10861–10867. Phys., 2013, 15, 6903–6911.
17 S. P. Singh and P. Singh, Renewable Sustainable Energy Rev., 34 C. Jimenez, B. R. Cossı́o and F. Xavier Niell, Aquaculture,
2014, 38, 172–179. 2003, 221, 331–345.
18 M. Cuaresma, M. Janssen, C. Vilchez and R. H. Wijffels, 35 J. C. Ogbonna and H. Tanaka, J. Appl. Phycol., 2000, 12, 207–
Biotechnol. Bioeng., 2009, 104, 352–359. 218.
19 L. Xiao and Z. He, Renewable Sustainable Energy Rev., 2014, 36 M. Atta, A. Idris, A. Bukhari and S. Wahidin, Bioresour.
37, 550–559. Technol., 2013, 148, 373–378.
20 R. Y. Stanier, R. Kunisawa, M. Mandel and G. Cohen-Bazire, 37 R. A. Rozendal, H. V. M. Hamelers and C. J. N. Buisman,
Bacteriol. Rev., 1971, 35, 171–205. Environ. Sci. Technol., 2006, 40, 5206–5211.
21 S. Cheng, H. Liu and B. E. Logan, Environ. Sci. Technol., 2006, 38 A. Rinaldi, B. Mecheri, V. Garavaglia, S. Licoccia, P. Di Nardo
40, 2426–2432. and E. Traversa, Energy Environ. Sci., 2008, 1, 417–429.

25100 | RSC Adv., 2016, 6, 25094–25100 This journal is © The Royal Society of Chemistry 2016

You might also like