Dujia Cheng1,2,3
Kinetic model for effects of simulated flue gas
onto growth profiles of Chlorella sp. AE10 and
Chlorella sp. Cv
1 ShanghaiAdvanced Research Institute, Chinese Academy of Sciences,
Shanghai, People’s Republic of China
2 University of Chinese Academy of Sciences, Beijing, People’s Republic of
China
3 ShanghaiTech University, Shanghai, People’s Republic of China
4 School of Life Science, Shanghai University, Shanghai, People’s Republic
of China
5 Schoolof Pharmaceutical Science, Nanjing Tech University, Nanjing,
People’s Republic of China
Abstract
Microalgae are potential candidate for biofuel production as
alternative one for fossil fuels. CO2 in flue gas is available
carbon source to support microalgae growth. In this study, the
effects of different concentrations of the simulated flue gas
onto algal growth and photosynthetic activity were evaluated
for both Chlorella sp. AE10 and Chlorella sp. Cv. The growth
profiles were correlated by a simple kinetic model. It was
indicated that the simulated flue gas led to low pH and the
photosynthetic activity was partially destroyed. Chlorella sp.
Cv can tolerate full simulated flue gas, 10% CO2 + 200 ppm
Keywords: simulated flue gas, CO2 capture, kinetic model, biofuels,
bioprocessing, cell cultivation
1. Introduction
Fossil fuels are widely used for more than one hundred years
all over the world to produce energy, fine chemicals, and so
on. The available resource of coal, petroleum, and natural gas
is limited because it is not renewable. Biofuels are converted
from biological feedstocks produced by photosynthesis in plants
and microalgae. It is considered that biofuels are alternative
Abbreviations: PBR, photobioreactor; RMSE, root mean square error..
∗ Addressfor correspondence: Prof. Quanyu Zhao, School of
Pharmaceutical Science, Nanjing Tech University, 30 Puzhu South Road,
Nanjing 211816, People’s Republic of China. Tel.: +86 25 58139942; Fax:
+86 25 58139942; e-mail: zhaoqy@njtech.edu.cn.
Received 10 June 2019; accepted 22 September 2019
DOI: 10.1002/bab.1829
Published online in Wiley Online Library
(wileyonlinelibrary.com)
Xuyang Li1,4
Yizhong Yuan1,2,3
Quanyu Zhao 1,3,5
∗
NOx + 100 ppm SOx . The pH in medium maintained at 6 and
the photosynthetic activity was more than 0.6 at the first 6
days. If the concentration of NOx was more 100 ppm and that
of SOx was more than 50 ppm, the pH was declined to 4 at day
2 or 3 for Chlorella sp. AE10. At the same time, the related
photosynthetic activities of Chlorella sp. AE10 were less than
0.4, which was not suitable for algal growth. It was shown that
Chlorella sp. Cv could be used for CO2 fixation from the
simulated flue gas.  C 2019 International Union of Biochemistry and
Molecular Biology, Inc. Volume 0, Number 0, Pages 1–7, 2019
and sustainable energy compared with fossil fuels. Microalgae
have high photosynthetic capability under photoautotrophic
conditions. The organic substances and other compounds
including nitrogen and phosphorus in wastewater are possible
substrates for microalgae. Some species of cyanobacteria can
fix nitrogen from air and produce polysaccharides to increase
organic matter contents in soil and improve soil structure.
Therefore, microalgae are potential candidates for CO2 fixation
[1–3], biofuels productions [4, 5], wastewater treatments [6–8],
and soil remediation [9].
Utilization of fossil fuels leads to greenhouse gas emissions
and other environmental issues. Microalgae could capture CO2
and accumulated lipids under nitrogen starvation and other
stress conditions. In the next step, the lipid could be converted
into biodiesels [10]. It is critical to obtain enough biomass of
microalgae for successful algal biodiesel development [11]. The
CO2 fixation by microalgae under photoautotrophic conditions
could be a negative carbon emission process. CO2 in flue gas
1

Schematic diagram of photobioreactor system for
FIG. 1 simulated flue gas capture by microalgae. 1, Pure
CO2 cylinder; 2, air compressor; 3, air tank; 4, gas
container with high concentration of CO2 ; 5,
simulated flue gas cylinder with 1% NOx , 0.5 SOx ,
and 98.5% N2 (v v−1 ); 6, mixed gas container with
10% CO2 (v v−1 ), 800 ppm NOx , and 400 ppm SOx ;
7, mixed gas container for simulated flue gas
capture; 8, thermostatic water bath; 9, bubble
column photobioreactors; 10, LED lamps.
produced by chemical industry and other industrial processes
is possible inorganic carbon source to support the microalgae
growth. The typical CO2 concentration in flue gas was from
4.9% to 26.9% [12]. Not all of microalgae can tolerate high
concentration of CO2 . The concentration of CO2 in air is not
more than 0.04% (v v−1 ) and the suitable CO2 concentration
for microalgae growth may be less than 2% [13]. In addition,
the components in flue gas, NOx , SOx , heavy metals, and ash,
are also toxic for microalgae [12, 14]. It is important to find a
microalgae strain tolerating CO2 , NOx , and SOx . Isolation and
screening from environments are available approach to get the
microalgae strains while the efficiency is not very high. Genetic
modification by metabolic engineering tools is also difficult for
green microalgae because the genome information is few and
the related molecular biology method is scarce [15]. Adaptive
evolution is a powerful way to enhance metabolic tolerance
capability under specific environmental stresses [16]. It was
performed to improve CO2 fixation [1, 2], phenol degradation
[6], and high value-added compound production [17]. Chlorella
sp. AE10 was obtained after a long-term adaptive evolution
process under 10% CO2 in our previous study [1] and Chlorella
sp. Cv was another evolved strain based on Chlorella sp.
AE10 using the simulated flue gas as environmental stress
[18]. In this study, the effects of different concentrations of the
simulated flue gas onto algal growth and photosynthetic activity
of Chlorella sp. AE10 and Chlorella sp. Cv were investigated.
The experimental data were correlated by a simple kinetic
model.
2 Kinetic Model for Effects of Simulated Flue Gas
Biotechnology and
Applied Biochemistry
2. Methods
2.1. Algal organism and culture conditions
Both Chlorella sp. AE10 and Chlorella sp. Cv were cultivated in
330 mL bubble photobioreactors (PBRs) using BG11 medium.
The whole schematic diagram of PBR system is shown in
Fig. 1. The culture conditions, temperature, light intensity, and
input gas concentration, were accurately controlled. The light
intensity was 100 µmol photons m−2 Sec−1 at the surface of
PBRs and the culture temperature was carefully maintained at
28 ± 0.05 ◦ C in a thermostatic water bath. The input gas was
10% CO2 (v v−1 ) as control, which was mixed with air and pure
CO2 . The ranges of NOx and SOx in the simulated flue gas were
50–200 and 25–100 ppm, respectively. The concentration of
NOx in the input gas was twice as much as that of SOx and the
simulated flue gas with the maximal concentrations of NOx and
SOx included 10% CO2 , 200 ppm NOx , and 100 ppm SOx . The
mixed gases, 1% NOx , 0.5% SOx , and 98.5% N2 (v v−1 ), was from
Shanghai Pujiang Special Gas (Shanghai, China). The aeration
rate was 0.1 L Min−1 . The contents of the simulated flue gas
were measured by flue gas component analyzer (Lancom 4,
Pittsburgh, USA). The components of NOx were 95% NO and
5% NO2 .
2.2. Determination of growth rate, photosynthetic
activity, and pH in medium
Both Chlorella sp. AE10 and Chlorella sp. Cv were cultivated
under different simulated flue gases for 7 days. The biomass
concentration, the pH in medium, and the maximum quan-
tum yield of photosystem II of the microalgae (Fv/Fm) were
determined every day. The growth profiles of both Chlorella
sp. AE10 and Chlorella sp. Cv were characterized by the cell
dry weight method [18, 19]. It was the standard protocol and
used in the previous studies so that the procedure was not
mentioned again in detail. Ten milliliters samples in PBRs were
collected every day. The pH was measured by pH meter (PHSJ-
3F; Leici, China). The Fv/Fm of microalgae was determined
by fluorescence monitoring system (FMS2; Lufthansa Scientific
Instruments, Ltd., UK) [8].

2.3. Kinetic model

There were lots of kinetic models including parameters related
to light intensity, light quality, and temperature for microalgae
growth [20, 21]. The growth curves of microalgae under 10%
CO2 and different simulated flue gases were correlated by the
equation below [22, 23].
 
dC C
= μmax 1 − C (1)
dt C max

C 0 · C max · eμmax ·t
C (t) = (2)
C max − C 0 + C 0 · eμmax ·t

where C is the biomass concentration, g L−1 ; C0 , initial biomass

concentration, g L−1 ; Cmax , maximal biomass concentration,
g L−1 ; t, culture time, day; µmax , maximal specific growth rate,
d−1 . The correlation performance was evaluated by root mean
square error (RMSE) described by Eq. (3) [24].

  Nexp  2

 i=1 C corr, i − C exp, i
RMSE = (3)
Nexp

where Ccorr, i was the correlated biomass concentration at i-th

day; Cexp, i was the experimental biomass concentration at
i-th day; Nexp was the total number of the experimental days
(Nexp = 8). The correlated biomass concentrations were solved
by function, nlinfit, in Matlab (R2012, USA).

2.4. Statistical analysis

All of the experiments were performed with three biological
replicates. The statistical significance was evaluated using
Student’s t-test. If P value was less than 0.05, it was considered
as significant one.
3. Results and Discussion
3.1. Effects onto growth profiles
Under control conditions, 10% CO2 , there was no significantly
difference between Chlorella sp. AE10 and Chlorella sp. Cv
(P = 0.1923). The final biomass concentration of Chlorella sp.
AE10 was a little higher than that of Chlorella sp. Cv (Fig. 2).
When Chlorella sp. AE10 was cultivated under the simulated
flue gas conditions, the growth was inhibited. The final biomass
concentration of Chlorella sp. AE10 was 0.575 g L−1 so that it
could not tolerate the full simulated flue gas. Under different
concentrations of the simulated flue gas, the biomass concen-
trations of Chlorella sp. Cv were more than 2 g L−1 (Fig. 2B).
The final biomass concentration of Chlorella sp. Cv under
the full simulated flue gas was 2.499 g L−1 . Just as shown in
Table 1, the maximal biomass productivity is 0.53 g L−1 d−1
for the current study, which was a little lower than that of our
previous study [18]. The possible reason was the difference of
the initial cell density. The initial cell density was 0.33 g L−1
Growth profiles of Chlorella sp. AE10 (A) and
FIG. 2 Chlorella sp. Cv (B) under different simulated flue
gas conditions. AE-0 and Cv-0, control, 10% CO2 ;
AE-50 and Cv-50, 10% CO2 , 50 ppm NOx , and
25 ppm SOx ; AE-100 and Cv-100, 10% CO2 ,
100 ppm NOx , and 50 ppm SOx ; AE-200 and
Cv-200, 10% CO2 , 200 ppm NOx , and 100 ppm
SOx . The point data are experimental results
shown as mean ± SD (n = 3). The lines were
correlated results by Eq. (2).
in this study and it was about 0.45 g L−1 in the previous work
[18]. In general, high initial cell density is helpful to improve
the tolerance capability of microalgae [6].
It was proved that the satisfied correlations were per-
formed by Eqs. (1) and (2) for microalgae growth profiles
(Fig. 2). The maximal RMSE of Chlorella sp. AE10 was
0.1695 g L−1 . All of RMSEs of Chlorella sp. Cv were lower
than those of Chlorella sp. AE10. The correlated parameters of
Chlorella sp. AE10 and Chlorella sp. Cv are shown in Table 2.
The maximal specific growth rates of Chlorella sp. AE10 under

Biotechnology and Applied Biochemistry 3

 Biotechnology and
Applied Biochemistry

Comparison of biomass productivity of microalgae cultivated by simulated flue gas

TABLE 1

Maximum
biomass
Aeration productivity
Algal species rate (vvm) Aeration time Gas component (g L−1 d−1 ) Ref.

Nannochloris – – 15% CO2 , 50 ppm SO2 0.215 [25]

sp. NANNO2

Nannochloris – – 15% CO2 , 300 ppm NO 0.08 [25]

sp. NANNO2

Chlorella KR-1 0.5 Continuous 15% CO2 , 100 ppm NO 1.35 [26]
Chlorella KR-1 0.5 Continuous 15% CO2 , 100 ppm SO2 0.78 [26]

Scenedesmus 0.05–0.5 Continuous 18% CO2 , 200 ppm SO2 , 150 ppm NO 0.1 [27]
obliquus
WUST4

Chlorella 0.3 Continuous 12% CO2 , 60 ppm SO2 , 100 ppm NO 0.09 [28]
vulgaris
LEB-106
Scenedesmus 0.25 Continuous 15% CO2 , 400 ppm SO2 , 300 ppm NO 0.037 [29]
dimorphus

Chlorella sp. 0.2 12 H d−1 25% CO2 , 80–90 ppm SO2 , 70–80 ppm NO 0.515 [30]
MTF-15

Scenedesmus 0.2 Continuous 15% CO2 , 200 ppm SO2 , 100 ppm NO 0.90 [31]
dimorphus
WZKM

Chlorella fusca 0.05 1 Min every 40 Min 15% CO2 , 200 ppm SO2 , 100 ppm NO 0.11 [32]
(light period)

Synechococcus 0.05 1 Min every 40 Min 10% CO2 , 200 ppm SO2 , 100 ppm NO 0.06 [33]
nidulans (light period)
Chlorella sp Cv 0.3 Continuous 10% CO2 , 100 ppm SO2 , 200 ppm NO 0.64 [18]

Chlorella sp Cv 0.3 Continuous 10% CO2 , 100 ppm SO2 , 200 ppm NO 0.53 This
study

–, not available.

Comparison of correlated maximal specific growth rate in kinetic model

TABLE 2

Chlorella sp. AE10 Chlorella sp. Cv

Input gas conditions µmax (d−1 ) RMSE (g L−1 ) µmax (d−1 ) RMSE (g L−1 )

10% CO2 0.8133 0.1695 0.7685 0.0962

10% CO2 , 50 ppm NOx and 25 ppm SOx 0.9081 0.1075 0.7664 0.0921
10% CO2 , 100 ppm NOx and 50 ppm SOx 1.144 0.0989 0.7537 0.0873

10% CO2 , 200 ppm NOx and 100 ppm SOx 0.2948 0.1180 0.9824 0.0836

4 Kinetic Model for Effects of Simulated Flue Gas

10% CO2 , 10% CO2 + 50 ppm NOx + 25 ppm SOx , and 10%
CO2 + 100 ppm NOx , + 50 ppm SOx were higher than those of
Chlorella sp. Cv. It was indicated that Chlorella sp. AE10 had
faster growth than Chlorella sp. Cv at the beginning two days. If
the concentrations of the accumulated salts from NOx and SOx
were not more than a threshold value, Chlorella sp. AE10 can
grow normally. Under full simulated flue gas conditions (10%
CO2 + 200 ppm NOx + 100 ppm SOx ), the maximal specific
growth rate was 0.2948 d−1 for Chlorella sp. AE10, whereas it
was 0.9824 d−1 for Chlorella sp. Cv because 200 ppm NOx and
100 ppm SOx in the simulated flue gas strongly inhibited the
growth of Chlorella sp. AE10 at the beginning of the cultivation
(Table 2).

3.2. Effects onto photosynthetic activity and pH

Fv/Fm of Chlorella sp. AE10 was about 0.7 under 10% CO2
[1]. If 10% CO2 + 50 ppm NOx + 25 ppm SOx were added into
PBRs, Fv/Fm was in normal range from day 0 to day 6 (Fig. 3A)
for both Chlorella sp. AE10 and Chlorella sp. Cv. If the input
gas was 10% CO2 + 100 ppm NOx + 50 ppm SOx , Fv/Fm of
Chlorella sp. AE10 was reduced to 0.05 at day 3. Fv/Fm of
Chlorella sp. AE10 was declined to about 0.4 at day 1 under
10% CO2 + 200 ppm NOx + 100 ppm SOx conditions, which
can explain why its specific growth rate was very low (Fig. 2A).
The photosynthetic activities of Chlorella sp. Cv were more
than 0.65 before day 6 under different concentrations of the
simulated flue gas conditions (Fig. 3B).
If the microalgae strains could not utilize the accumulated
salts from the simulated flue gas, continuously inputting
simulated flue gas led to low pH of the culture medium.
Then, the photosystem of microalgae will be destroyed and
the photosynthetic activities will be decreased. Finally, the
microalgae strains did not tolerate the stress of the simulated
flue gas. The pH of Chlorella sp. Cv under all conditions were Maximum quantum efficiency of photosystem II
FIG. 3 (Fv/Fm) of Chlorella sp. AE10 (A) and Chlorella sp.
more than 6 (Fig. 4B), whereas the pH of Chlorella sp. AE10
Cv (B) under different simulated flue gas
under high concentrations of NOx and SOx were 2 (Fig. 4A). It conditions. AE-0 and Cv-0, control, 10% CO2 ;
was obvious that Chlorella sp. AE10 could not maintain normal AE-50 and Cv-50, 10% CO2 , 50 ppm NOx , and
photosynthetic activity and grow under the full simulated flue 25 ppm SOx ; AE-100 and Cv-100, 10% CO2 ,
gas conditions. 100 ppm NOx , and 50 ppm SOx ; AE-200 and
Cv-200, 10% CO2 , 200 ppm NOx , and 100 ppm
SOx . The data are shown as mean ± SD (n = 3).
3.3. Discussion
SOx and NOx can be dissolved in culture medium while the
solubility of SOx was much higher than that of NO. The toxicities
of flue gas components were investigated for both Dunaliella 150 ppm SOx and pH control conditions was similar to that
abundans RSM and Scenedesmus sp.UTEX1589 [34]. Compared under SO2 free conditions [36]. In this study, the pH of medium
with 1,067 ppm (w v−1 ) NO2 − and 254 ppm SO3 2− (w v−1 ), was not controlled. The process without pH control was easier
39 ppm (w v−1 ) bisulfite had significant effect to their growth. to operate compared with that with pH control. When the
In the typical flue gas, most of the component of NOx was culture time was less than 7 days, the carbon capture from the
NO and the solubility of NO is very low in water (0.032 g L−1 simulated flue gas was feasible by Chlorella sp. Cv. Much more
at 101.325 kPa and 25 ◦ C) [12]. SOx is more dangerous than SOx was dissolved in medium when the culture time was more
NOx for microalgae. Besides of toxicity of the dissolved salts than 7 days. Low pH may lead to lethal effect to microalgae.
of SOx , low pH is also critical reason for the growth inhibition The evolved strain, Chlorella sp. Cv was candidate one for flue
of microalgae. It was confirmed that the pH was the primary gas capture.
cause of growth inhibition under high concentration of CO2 The lipid contents of C. fusca were changed slightly under
[35]. It was also shown that the growth of Chlorella KR-1 under different flue gas conditions [32]. In general, the nitrogen,

Biotechnology and Applied Biochemistry 5


Dynamic curves of pH in medium of Chlorella sp.
FIG. 4
AE10 (A) and Chlorella sp. Cv (B) under different
simulated flue gas conditions. AE-0 and Cv-0,
control, 10% CO2 ; AE-50 and Cv-50, 10% CO2 ,
50 ppm NOx , and 25 ppm SOx ; AE-100 and Cv-100,
10% CO2 , 100 ppm NOx , and 50 ppm SOx ; AE-200
and Cv-200, 10% CO2 , 200 ppm NOx , and 100 ppm
SOx . The data are shown as mean ± SD (n = 3).
sulfur, and phosphorus were consumed in the PBRs. At the end
of cultivations, it is possible to achieve a nutrient starvation
condition and it is beneficial for lipid and carbohydrate accu-
mulations [31]. Just as mentioned above, the solubility of SOx
was significantly higher than that of NO so that the sulfur was
not limited element during the cultivation of microalgae using
the simulated flue gas. Compared with nitrogen and sulfur,
it is easy to reach phosphorus starvation conditions. Further
studies will be performed to characterize and optimize the
bioprocess for CO2 capture and biofuels production using flue
gas.
Chlorella sp. AE10 was high concentration of CO2 -tolerance
strain [1] and it can grow under <20 g L−1 salt conditions [2].
6 Kinetic Model for Effects of Simulated Flue Gas
Biotechnology and
Applied Biochemistry
It was indicated that the evolved strain can tolerate other
environmental stress besides the original one. Chlorella sp. Cv
had rapid growth rate under the simulated flue gas conditions
while its tolerance capabilities to heavy metals, ash, and other
components in industrial flue gas have not been evaluated. Low
concentration of heavy metals in flue gas promoted biomass
formation and lipid yield [37]. In the practical application of CO2
fixation by microalgae from real or industrial flue gas, buffer
solution [38] or dilution was utilized [33]. New strategy should
be proposed to improve the CO2 fixation capability and removal
efficiencies of NOx , SOx , heavy metal, and other components in
flue gas. It will be carried out in the further study.
4. Conclusions
In this study, the growth profiles and photosynthetic activities
of Chlorella sp. AE10 and Chlorella sp. Cv were evaluated.
The biomass concentrations of them were also correlated by
a simple kinetic model. It was proved that the evolved strain,
Chlorella sp. Cv tolerated up to 10% CO2 , 200 ppm NOx , and
100 ppm SOx . The Fv/Fm was maintained to more than 0.6 for
6 days and the pH of culture medium was also more than 6.
If concentrations of NOx and SOx in flue gas were more than
100 and 50 ppm, respectively, the growth of Chlorella sp. AE10
was significantly inhibited. The Fv/Fm was decreased to less
than 0.1 from day 2 and the pH of culture medium was lower
than 4. Compared with the previous study, initial cell density
is an important parameter for the CO2 capture from flue gas.
Chlorella sp. Cv was a potential candidate algal strain for flue
gas capture without pH control.
5. Acknowledgement
This study is supported by National Natural Science Foundation
of China (21576278).
The authors declare no conflict of interests. The funding
sponsors have no role in the design of the study.
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