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A B S T R A C T
Article history:
Received 19 June 2014
Accepted 1 August 2014
A cost effective fertilizer based optimum culture medium was formulated for the mass production of
Spirulina platensis using NPK-10:26:26 complex fertilizer in air agitated sintered disk chromatographic
glass bubble column and the growth results were compared with the standard Zarrouks culture medium.
The optimum loadings of NPK-fertilizer and sodium bicarbonate was found to be 0.76 and 10.0 g L1
respectively and corresponding maximum dry biomass concentration with 1.82 g L1 was obtained at the
tenth day of biomass growth. Optimally formulated fertilizer medium was then used for the cultivation of
Spirulina using simulated ue gas which was similar to diesel generator exhaust. Flue gas was fed to the
bubble column reactor in a semi-batch fashion and Spirulina cultivation was carried out using
NPK-fertilizer culture medium involving sodium hydroxide. Biomass productivity and CO2 xation rate
was enhanced with the increased loading of sodium hydroxide in the culture medium. Maximum
biomass concentration with 1.85 g L1 was obtained at the sixth day of biomass growth when average CO2
solubility was maintained at 4.84 g L1. Finally, ue gas assisted biomass growth using optimum
NPK-10:26:26 complex fertilizer medium was compared with standard Zarrouks culture medium using
sintered disk chromatographic gas bubble column reactor and improved growth results (4.0%) with
enhanced lipid accumulation (5.0%) were obtained using NPK-10:26:26 fertilizer medium as compared
to the Zarrouks culture medium. An almost 50.0% cost saving was achieved due to the use of low cost
NPK-10:26:26 complex fertilizer as a nutrient for Spirulina growth in comparison to standard Zarrouks
culture medium.
2014 Published by Elsevier Ltd.
Keywords:
Spirulina platensis
NPK-10:
26:26 ?complex fertilizer
Simulated ue gas
CO2 xation
Bubble column
Mass transfer
Introduction
Greenhouse gases (GHG), particularly CO2, are being considered
as the most important contributing factor for global warming which
have substantial impacts on the environment, human health and the
economy [1]. The excess CO2 emission to the atmosphere is needed to
be reduced and the present day research has been focused to develop
numerous strategies to mitigate the CO2 emission by proposing
different sequestration techniques [26]. Alkali mediated CO2
capture and sequestration was reported by Budzianowski and Koziol
[46]. In this process, CO2 separation efciency was enhanced
signicantly by using reactive solvents (e.g., ammonia, potassium
hydroxide, and etc.). Moreover, these reactive solvents were also very
helpful to produce valuable fertilizer additives (for example,
* Corresponding author. Tel.: +91 326 2235411; fax: +91 326 2296632.
E-mail addresses: cguria.che@gmail.com, guria.c.pe@ismdhanbad.ac.in
(C. Guria).
http://dx.doi.org/10.1016/j.jece.2014.08.002
2213-3437/ 2014 Published by Elsevier Ltd.
1860
1861
11
8 9
Purge
5
1
4
14
15
Air Sucon
10
12
13
16
Fig. 1. Experimental set-up for S. platensis growth: 1 simulated ue gas cylinder; 2 two-stage stainless steel pressure regulator; 3 simulated ue gas lter 4 ue gas
rotameter; 5 air compressor; 6 pressure gauge; 7 surge tank; 8 air lter 9 air rotameter; 10 gas injection conical ask; 11 jacketed sintered disc chromatographybubble column; 12 water recirculation pump; 13 thermostatic bath; 14 moisture removing trap; 15 CO2 analyser; 16 at bottom ask with absorbing solution.
1862
Table 1
Experimental design of the culture medium studied for the growth of S. platensis using NPK-10:26:26 complex fertilizer in SDCG bubble column.
NaNO3
(g L1)
K2HPO4
(g L1)
K2SO4
(g L1)
Saltsa
(g L1)
NPK-10:26:26
(g L1)
A5 micro
nutrients (mL)
1.33
1.0
P2
16.8/
1.33
P3
16.8/
1.33
P4
16.8/
1.33
P5
16.8/
1.33
P6
16.8/
1.33
0.36
(N = 0.036; P = 0.045; K = 0.077)
0.76
(N = 0.076; P = 0.089; K = 0.164)
1.06
(N = 0.106; P = 0.1224; K=0.23)
1.26
(N = 0.126; P = 0.146; K = 0.272)
1.36
(N = 0.136; P = 0.157; K = 0.293)
1.46
(N = 0.146; P = 0.169; K = 0.315)
1.33
1.33
1.33
1.33
1.33
1.33
1.33
1.33
0.76
0.76
0.76
0.76
1.06
1.06
1.06
1.06
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
Zarrouk (air)
Zarrouk
2.5
0.5
1.0
1.33
1.0
2.5
2.5
2.5
2.5
0.5
0.5
0.5
0.5
1.0
1.0
1.0
1.0
1.33
1.33
1.33
1.33
1.33
1.33
1.33
1.33
0.76
0.76
0.76
0.76
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
Culture medium
NaHCO3/NaOH
(g L1)
16.8
NaCl: 1.0, MgSO47H2O: 0.2, EDTA: 0.08, CaCl22H2O: 0.04 and FeSO47H2O: 0.01 (g L1).
1.0
1.0
1.0
1.0
1.0
2.1
2.1
1.5
P2C1(0.76,22)
P2C2(0.76,18)
P2C3(0.76,10)
P2C4(0.76,4.5)
P3C1(1.06,22)
P3C2(1.06,18)
P3C3(1.06,10)
P3C4(1.06,4.5)
1.8
Biomass concentration (g l-1 )
Biomass concentration (g l -1 )
1.8
1.2
0.9
0.6
1863
1.5
1.2
0.9
0.6
0.3
0.3
0
0
12
16
20
Time (d)
12
16
20
Time (d)
Fig. 2. (a) Time behavior of S. platensis growth with varying NPK-10:26:26 complex fertilizer loadings with xed sodium bicarbonate concentration using air agitated
SDCG-bubble column and comparison with Zarrouks culture medium. (b) Time behavior of S. platensis growth with varying sodium bicarbonate loading with xed NPK
fertilizer loading using air agitated SDCG-bubble column (Table 1: for details of variation of NPK-10:26:26 fertilizer and sodium bicarbonate).
the tenth day of biomass growth (Fig. 2b) which was comparable to
maximum biomass concentration obtained from Zarrouks culture
medium (i.e., 1.87 g L1). Details of kinetic parameters (i.e., Xm, PX,
mmax, YX/N and YX/P), chlorophyll, protein, lipid and the uptake of
the elemental N, P and K for the culture mediums with varying
bicarbonate concentration for P2C3 and Zarrouks culture medium
are also reported in Table 2. Comparable growth results were
obtained for P2C3 and Zarrouks culture medium. Therefore, the
composition of optimum NPK-10:26:26 complex fertilizer culture
medium for Spirulina growth using air agitated SDCG-bubble
column was found to be NPK-10:26:26 fertilizer0.76 g L1,
NaHCO310.0 g L1,
NaCl1.33 g L1
and
A5
micro
1
nutrients1.0 mL L . Above P2C3 culture medium with 0.76 g L1
NPK-10:26:26 complex fertilizer loading was considered for the CO2
sequestration from ue gas studies using SDCG-bubble column.
1864
0.20
3a. SFG Without NaOH
Zarrouk
P1(0.36 g/L)
P2(0.76 g/L)
P3(1.06 g/L)
P4(1.26 g/L)
P5(1.36 g/L)
7
3b. SFG With NaOH, g/L
P2: 0.76 g/L NPK
0.16
0.12
0.08
P2(0.84)
Z(0.84)
P3(0.84)
P2(1.68)
Z(1.68)
P3(1.68)
P2(3.32)
Z(3.32)
P3(3.32)
P2(5.04)
Z(5.04)
P3(5.04)
5
4
3
2
0.04
1
0.00
0
0
10
15
20
25
30
35
Time (min)
8
Time (min)
12
16
Fig. 3. (a) Time behavior of CO2 solubility with varying NPK-10:26:26 complex fertilizer loadings without NaOH using simulated ue gas agitated SDCG-bubble column and
comparison with Zarrouks culture medium (excluding NaHCO3). (b) Time behavior of CO2 solubility with varying NaOH (g L1: 0.84, 1.68, 3.32 and 5.04) using
NPK-10:26:26 complex fertilizer (P2: 0.76 g L1, P3: 1.06 g L1) and simulated ue gas using SDCG-bubble column and comparison with Zarrouks culture medium (excluding
NaHCO3).
6sr
dB
(1)
The values of kL/dB in Eq. (1) was calculated according to Chisti [46]
using Eq. (2) for simulated ue gaswater dispersions and waterlike suspending uid:
!0:5
kL
gDL sr2
5:63 105
exp0:131 C 2S
(2)
dB
m3L
where g = acceleration due to gravity (m s2), DL = diffusivity of the
transferring CO2 into liquid (m2 s1), s = interfacial tension(J m2),
mL = viscosity of the culture broth (kg m1 s1), r = density of the
suspension (kg m3) and CS = concentration of suspended algae
(g L1). To evaluate volumetric mass transfer coefcient at given
ue gas ow rate (i.e., 1.3 L min1), the parameters in Eqs. (1) and
(2) (i.e., dB, er, s , mL, r and CS) were measured using standard
measuring instruments during maximum biomass growth period
and the details of these parameters are given in Table 3 for P2 and
Zarrouks culture medium with varying NaOH concentration. To
evaluate the values of mass transfer coefcients of CO2, it is
essential to know the exact diffusivity values of CO2. The diffusivity
values are calculated from the duration of ue gas cycle, which was
related to the characteristic diffusion time. It was noted that ue
gas cycle time for given NaOH loading in the culture medium was
18
18
4a. P2:SFG+NPK
16
Frequency of bubbles (Number)
NPK2: NaOh-2.22 g
NPK3: NaOH-3.32 g
14
Zarrouk: NaOH-1.22 g
4b. SFG+Zarrouk
NPK1: NaOH-1.22 g
16
NPK4: NaOH-5.04 g
1865
12
10
8
6
4
2
Zarrouk: NaOH-2.22 g
Zarrouk: NaOH-3.32 g
14
Zarrouk: NaOH-5.04 g
12
10
8
6
4
2
0
0
0.002
0.004
0.006
0.008
0.01
Fig. 4. (a) Bubble size distribution at sixth day of biomass growth for P2 culture medium with S. platensis under varying NaOH loading using simulated ue gas agitated
SDCG-bubble column. (b) Bubble size distribution at sixth day of biomass growth for Zarrouks culture medium with S. platensis under varying NaOH loading using simulated
ue gas agitated SDCG-bubble column.
much shorter than that of air cycle time which indicates that the
2
characteristic diffusion time dB =36DL was much less than the
biomass growth time, where DL = diffusivity of the transferring CO2
in liquid and Characteristic length = 1/3 dB/2. The details of
diffusion time for P2 and Zarrouks culture medium with varying
NaOH loading are given in Table 3 and it was increased with the
increased in NaOH loading. The shorter diffusion time was mainly
due to high gasliquid interfacial area and demonstrates the
Table 2
Responses of S. platensis in SDGC bubble column using NPK-10:26:26 complex fertilizer and Zarrouk medium.
Culture medium X (mg L1) PX (mg L1 d1 mmax (d1) Nutrient uptake
(mg L1)
N
YX/N
YX/P
PCO2 (mg L1 d1) Chlorophyll (mg L1) Protein (%) Lipid (%)
(g g1) (g g1)
K
7.7
18.0
19.0
18.0
18.0
12.50
14.34
15.94
6.83
4.41
10.82
12.25
13.74
5.89
3.82
5.13
8.87
12.37
7.52
6.01
44.07
44.83
45.40
45.78
45.97
7.69
8.44
9.01
9.39
9.57
Varying NaHCO3
P2C1
P2C2
P2C3
P2C4
P3C1
P3C2
P3C3
P3C4
14.0
9.0
17.0
18.0
15.0
16.0
13.0
16.0
11.58
14.87
23.29
9.74
6.60
15.19
6.32
6.13
9.89
12.70
19.89
8.31
5.69
13.15
5.45
5.28
7.64
9.10
12.84
6.82
6.59
11.35
6.41
6.30
44.49
44.73
45.81
48.80
44.92
45.26
46.77
50.94
8.10
8.34
9.41
12.38
8.54
8.87
10.36
14.51
47.1
4.43
20.45
13.13
51.20
14.76
7.0
8.0
13.0
19.0
7.0
9.0
14.0
17.0
174.72
205.38
328.92
499.26
195.10
246.50
365.50
452.33
6.0
6.6
9.0
12.4
6.4
7.4
9.7
11.5
45.8
47.0
48.8
53.3
46.0
51.0
53.1
54.5
9.4
10.6
12.4
16.8
9.2
10.5
12.1
16.0
0.14
243.0
14.0
P2 and Zarrouk: varying NaOH loading, six days biomass growth (simulated
NPK1
642
98.71
0.10
36.0
6.0
NPK2
746
116.0
0.12
40.0
9.0
NPK3
1365
185.8
0.15
40.7
12.0
NPK4
1845
282.1
0.21
54.0
14.8
Z1
711
110.2
0.11
129.0
4.0
Z2
886
139.3
0.12
157.5
5.0
Z3
1289
206.5
0.16
186.0
7.0
Z4
1783
255.6
0.17
226.0
9.5
ue gas)
10.0
7.79
12.0
9.16
14.0
14.67
14.0
22.27
38.0
1.61
40.0
3.38
42.0
3.01
45.0
3.73
Where Xm: maximum biomass concentration (mg L1), PX: biomass productivity(mg L1 day1), mmax: maximum specic biomass growth rate (d1), PCO2 : CO2 xation rate
(mg L1 day1) and calculated based on CH1.650O0.531N0.170S0.007P0.006 molecular mass of S. platensis (Cornet et al., [27]): 1.77 Px,YX/N: conversion yield of
nitrogen to biomass (g g1), YX/P: conversion yield of phosphorous to biomass (g g1).
1866
Table 3
Details of the average measured parameters at the maximum biomass growth using simulated ue gas in SDCG-bubble column.
Parameters
Culture medium
NPK1
1
NaOH loading (g L )
Temperature (1 K)
Air ow rate/cycle,
(L min1 cycle)
Flue gas ow rate/cycle,
(L min1 cycle)
No. of ue gas cycle/day
Diffusion time, tD (s)
Initial CO2 solubility (g L1)
Average CO2 solubility (g L1)
Mean bubble diameter, dB 103 (m)
Gas holdup, er (%)
Density of the suspension, r (kg m3)
Interfacial tension, s 102 (J m2)
Viscosity of the culture broth, mL 103 (kg m1 s1)
Concentration of suspended solids, CS (g L1)
2
Diffusivity of the transferring CO2 in liquid, DL 1010 (m2 s1) dB =36tD
where characteristic length of sphere = radius of sphere/3.
Overall gasliquid volumetric mass transfer coefcient, kLaL 103 (s1) [46]
Average pH
Dissolved oxygen (mg L1)
NPK2
NPK3
NPK4
Z1
Z2
Z3
Z4
1.22
303
1.3
2.22
303
1.3
3.32
303
1.3
5.04
303
1.3
1.22
303
1.3
2.22
303
1.3
3.32
303
1.3
5.04
303
1.3
1.3
1.3
1.3
1.3
1.3
1.3
1.3
1.3
4.0
4.2
4.5
4.6
4.0
4.2
4.5
4.6
674
951
1288
1804
607
902
1205
1503
1.28
2.34
3.48
5.24
1.28
2.34
3.48
5.24
1.20
2.34
3.26
4.84
1.18
2.34
3.35
4.98
2.10
1.78
1.46
0.74
1.31
1.20
1.09
0.61
0.054
0.053
0.053
0.053
0.057
0.057
0.056
0.056
1484.2
1694.6
1956.5
2358.2
1815.1
2032.5
2292.9
2666.3
6.31
6.25
6.13
6.08
5.42
5.32
5.23
5.15
1.14
1.15
1.15
1.16
1.17
1.17
1.18
1.18
0.65
0.75
1.17
1.75
0.72
0.89
1.29
1.59
0.93
0.46
0.08
0.79
0.44
0.27
0.07
1.82
7.46
9.36
4.0
5.75
9.35
3.8
4.17
9.33
3.6
1.69
9.34
3.2
5.59
9.37
3.7
4.50
9.31
3.5
3.42
9.37
3.4
1.76
9.47
2.9
are given in Table 1. It was also noted that biomass growth increased
withtheincreasedloadingofNaOH(Fig.5aandc).Detailsofmaximum
biomass concentration with varying NaOH concentration in ue gas
agitatedbubblecolumnaregiveninTable2.ForNPK4culturemedium
(NaOH: 5.04 g L1, Table 1), maximum biomass concentration (Xm)
with 1.85 g L1 was obtained at the sixth day of biomass growth using
NaOH-ue gas assisted SDCG-bubble column, whereas Xm with
1.82 g L1 was obtained at tenth day of biomass growth using
NaHCO3-air assisted SDCG-bubble column for P2C3 culture medium
(NaHCO3:10 g L1,Table1).Theenhancementofbiomassgrowthrate
was mainly due to the maintenance of higher average carbon
concentration in the culture medium throughout biomass growth.
DetailsofaverageCO2 solubilitywithvaryingNaOHloadingforP2and
Zarrouks culture medium are given in Table 3. Moreover, dissolved
oxygen in the culture medium for all experiments remained almost
steady at 3.5 mg L1 (Table 3) and the constant values of dissolved
oxygen indicates that the accumulatedreactive oxygen in the culture
medium is minimum which was mainly due to high liquidgas
interfacial area with improved back mixing in the culture medium
and helped to reduce the inhibitoryeffect of oxygen accumulation on
growth.
Biomass productivity (Px) and maximum specic growth rate
(mmax) of S. Platensis using SDCG-bubble column for all the culture
mediums using air and ue gas are given in Table 2. Px and mmax for
ue gas agitated culture medium was found to be 282.1 mg L1 d1
and 0.21 d1 respectively (i.e., NPK4: Table 2), whereas low values
of Px (=177.0 mg L1 d1) and mmax (=0.141 d1) were obtained for air
agitated culture medium (i.e., P2C3: Table 2). Details of these
kinetic parameters (Xm, Px and mmax) using P2 culture medium
with varying NaOH in ue gas agitated SDCG-bubble column were
reported in Table 2 and compared with Zarrouks culture medium.
Better biomass growth results were obtained for ue gas agitated
NPK culture medium (e.g., NPK4 in Table 2: Xm = 1.85 g L1,
Px = 282.0 mg L1 d1 and mmax = 0.21 d1) as compared to ue gas
agitated Zarrouk culture medium (e.g., Z4 in Table 2: Xm = 1.78 g L1,
Px = 255.6 mg L1 d1and mmax = 0.17 d1). The improved kinetic
parameters show the efciency of NPK-10:26:26 based biomass
cultivation using ue gas assisted biomass growth in SDCG-bubble
column over air purging. Comparing the biomass growth using
NPK and zarrouks culture medium, an enhancement in S. platensis
growth was also obtained for NPK fertilizer medium as compared
to standard Zarrouks culture medium (Table 2). It was also
2000
10.5
1867
1600
10.0
1200
pH
Biomass (mg.L-1)
9.5
800
9.0
400
8.5
0
10
0.0
0.5
2000
2.0
Z1 (NaOH:1.22 g/L)
10.0
1200
pH
Biomass (mg.L-1)
1.5
10.5
5c:SFG+Zarrouk
1600
1.0
Time (d)
Time(d)
9.5
800
9.0
400
8.5
0
0
10
Time (d)
0.0
0.5
1.0
Time (d)
1.5
2.0
Fig. 5. (a) Time behavior of S. platensis growth using P2 (NPK: 0.76 g L1) culture medium with varying NaOH loadings (g L1: 1.22, 2.22, 3.32, 5.04) using simulated ue gas
agitated SDCG-bubble column. (b) Variation of pH during two days of biomass growth period using P2 (NPK: 0.76 g L1) and NaOH (1.22 and 5.04 g L1) in simulated ue gas
agitated SDCG-bubble column. (c) Time behavior of S. platensis growth using Zarrouks culture medium with varying NaOH loadings (g L1: 1.22, 2.22, 3.32, 5.04) using
simulated ue gas agitated SDCG-bubble column. (d) Variation of pH during two days of biomass growth period using Zarrouks medium and NaOH (1.22 and 5.04 g L1) in
simulated ue gas agitated SDCG-bubble column.
observed that the CO2 xation rate using NPK4 and Z4 culture
medium was found to be 499.26 and 452.33 mg L1 d1 respectively (Table 2) and corresponding CO2 xation rate was increased
by 10.0% using NPK4 culture medium. The increased CO2 xation
rate was mainly due to the increased loading of NaOH. In CO2-toalgae route, CO2 xation was enhanced by the addition of NaOH in
liquid phase with following reactions:
CO2 g CO2 l
(3)
CO2 l H2 O H2 CO3 l
(4)
(5)
2
HCO
3 NaOH CO3 Na H2 O
(6)
1868
was more than 8.3. Biomass yield based on nitrogen (YX/N) and
phosphorous (YX/P) calculated on basis of nutrient uptake and the
details of nutrient uptake and corresponding yields are reported in
Table 2 with varying NaOH concentration in P2 and Zarrouks
culture medium. The values of YX/N and YX/P for P2 and Zarrouks
culture medium were increased with the increased in NaOH
loading.
Details of chlorophyll, lipid and protein content in biomass
using SDGC-bubble column for all the experiments with/without
using ue gas are given in Table 2. An enhancement of chlorophyll
and lipid accumulation was observed using NPK culture medium as
compared to Zarrouks culture medium. Chlorophyll and lipid
accumulation using NPK4 culture medium was found to be
12.4 mg L1 and 16.8% respectively, which were higher than Z4
culture medium (Table 2) and corresponding increases in
chlorophyll and lipid accumulation were found to be 7.8% and
5.0% respectively. The enhancement of lipid accumulation was
mainly due to deciency of initial nitrogen in the culture medium.
The decreased cellular nitrogen content of thylakoid membrane
activates diacylglycerol acytransferage and converts acyl-CoA to
tri-glycerides [26]. Comparable results for protein were obtained
for with varying NaOH concentration in P2 and Zarrouks culture
medium. It was also found that the accumulation of chlorophyll,
lipid and protein content were increased with the increase in
biomass growth.
The cost of nutrients at the maximum biomass growth using
NPK4 and Z4 was calculated. The cost of nutrients per kilogram of dry
biomass using NPK fertilizer medium was found to be US $46.2 which
was much lower than Zarrouks culture medium with US $92.5. The
corresponding cost saving was found to be almost 50.0% using NPK
fertilizer medium as compared to standard Zarrouks culture
medium. The reduction in unit cost of biomass using NPK fertilizer
was mainly due to the reduced quantity of the low-priced NPK
fertilizer and higher biomass growth rate as compared to standard
Zarrouks culture medium. Therefore, the merits of the NPK
fertilizer based culture medium are clearly emphasized, not only
as a low-cost alternative but also as a highly productive for CO2
sequestration, which may be used protably in rural population for
large-scale biomass cultivation of protein-rich S. platensis.
Conclusions
The present investigation was carried out to formulate a simple
and inexpensive culture medium for the growth of S. platensis
using NPK-10:26:26 complex fertilizer using air agitated sintered
disk chromatographic glass bubble column. The composition of
optimal NPK fertilizer was found to be NPK-10:26:26
fertilizer0.76 g L1, NaHCO310.0 g L1, NaCl1.33 g L1 and A5
micro nutrients1.0 mL L1 and comparable growth results were
obtained as compared to the standard Zarrouks culture medium.
Using above optimally formulated NPK fertilizer culture medium,
diesel generator simulated ue gas was used for the mass
cultivation of biomass in presence of sodium hydroxide using
sintered disk chromatographic glass bubble column. A semi-batch
feeding strategy of ue gas purging was adopted in presence of
NaOH for CO2-to-Spirulina route, and the following technological
improvements were obtained over the conventional method of
biomass cultivation: (i) use of soluble carbonates (e.g., NaHCO3 and
Na2CO3) for Spirulina cultivation (ii) reduction of biomass growth
period using NPK-NaOH culture medium by four days in ue gas
agitated SDCG-bubble column as compared to air agitated
NPK-NaHCO3 culture medium where maximum biomass concentration was obtained on tenth day of biomass growth (iii) an
improvement in maximum biomass concentration (4.0%),
chlorophyll production (7.8%) and lipid accumulation
(5.0%) by using NPK-NaOH culture medium as compared to
1869
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