In-field experimental verification of cultivation of microalgae Chlorella sp. using the flue gas from a cogeneration unit as a source of carbon dioxide.

Abstract

A complex treatment of agricultural waste including the following major steps: anaerobic fermentation of suitable waste, cogeneration of the obtained biogas and growth of microalgae consuming the CO(2) from biogas and flue gas was verified under field conditions in a pilot-scale photobioreactor. The growth kinetics of microalgae Chlorella sp. consuming mixture of air and carbon dioxide (2% (v/v) of CO(2)), or flue gas (8-10% (v/v) of CO(2)) was investigated. The results obtained in the pilot photobioreactor were compared with results previously measured in laboratory photobioreactors. The field tests were performed in a pilot-scale outdoor solar-bubbled photobioreactor located at a biogas station. The pilot-scale photobioreactor was in the shape of a flat and narrow vertical prism with a volume of 300 L. The microalgae growth rates were correlated with empirical formulas. Laboratory analyses of the produced microalgae confirmed that it meets the strict EU criteria for relevant contaminants level in foodstuffs. Utilization of flue gases from cogeneration therefore was not found to be detrimental to the quality of microalgal biomass, and may be used in these types of bioreactors.

Full text

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Research Paper
In-field experimental verification of
cultivation of microalgae Chlorella sp.
using the flue gas from a cogeneration
unit as a source of carbon dioxide
Frantis ˇek Kas ˇta ´nek1, Stanislav Sˇabata1, Olga Sˇolcova ´1,
Ywette Male ´terova ´1, Petr Kas ˇta ´nek2, Irena Bra ´nyikova ´2,3,
Karel Kuthan4and Vile ´m Zachleder5
Abstract
A complex treatment of agricultural waste including the following major steps: anaerobic fermentation of suitable waste,
cogeneration of the obtained biogas and growth of microalgae consuming the CO2from biogas and flue gas was verified
under field conditions in a pilot-scale photobioreactor. The growth kinetics of microalgae Chlorella sp. consuming mixture of
air and carbon dioxide (2% (v/v) of CO2), or flue gas (8–10% (v/v) of CO2) was investigated. The results obtained in the pilot
photobioreactor were compared with results previously measured in laboratory photobioreactors. The field tests were per-
formed in a pilot-scale outdoor solar-bubbled photobioreactor located at a biogas station. The pilot-scale photobioreactor
was in the shape of a flat and narrow vertical prism with a volume of 300L. The microalgae growth rates were correlated with
empirical formulas. Laboratory analyses of the produced microalgae confirmed that it meets the strict EU criteria for relevant
contaminants level in foodstuffs. Utilization of flue gases from cogeneration therefore was not found to be detrimental to the
quality of microalgal biomass, and may be used in these types of bioreactors.
Keywords
Carbon dioxide recovery, flat-prism photobioreactor, flue gas, integrated waste treatment, microalgae cultivation
Date received: 15 December 2009; accepted: 18 May 2010
Introduction
The proposed technology of complex agricultural waste
treatment, which is described in detail in our previous
paper (Douskova et al., 2010), consists of the following pro-
cess steps: production of biogas from agricultural waste (and/
or distillery stillage), utilization of the biogas for electricity
and heat production (cogeneration), and the use of flue gases
as a source of carbon dioxide for microalgae cultivation. The
microalgal biomass can hereafter be processed to valuable
products such as food and feed supplements.
As the mode of algae cultivation influences the economy
of the whole process, the present study focused mostly on this
decisive step.
Technologies for algae cultivation have been studied over
the past decade in the context of greenhouse gas mitigation;
see for example, Borowitzka (1999), Pulz and Schibenbogen
(1998) and Benemann (2003). Algae can be grown in open
tanks or ponds or in closed photobioreactors. Categories of
1Institute of Chemical Process Fundamentals of the Academy of
Sciences of the Czech Republic, Prague, Czech Republic.
2EcoFuel Laboratories Ltd., Prague, Czech Republic.
3Instituteof ChemicalTechnology in
FermentationChemistryand
Republic.
4Suchohrdly u Miroslavi 48, CZ 67172, Czech Republic.
5Laboratory of Cell Cycle of Algae, Department of Autotrophic
Microorganisms, Institute of Microbiology of the Academy of
Sciences of the Czech Republic, Trebon-Opatovicky mlyn, Czech
Republic.
Prague, Department of
Bioengineering,Prague,Czech
Corresponding author:
Irena Bra ´nyikova ´, Institute of Chemical Technology in Prague,
Department of Fermentation
Technicka ´ 5, CZ 16628, Prague 6, Czech Republic
Email: irena@branyik.cz
ChemistryandBioengineering,
Waste Management & Research
28(11) 961–966
! The Author(s) 2010
Reprints and permissions:
sagepub.co.uk/journalsPermissions.nav
DOI: 10.1177/0734242X10375866
wmr.sagepub.com

Page 2

closed photobioreactors include both horizontal and vertical
apparatus. Vertical photobioreactors (flat panels, bubble col-
umns, air lift reactors) are more convenient because in these
types of reactors it is easier to strip the inhibitive oxygen
from the algal suspension. As was illustrated for eicosa-
pentaenoic acid production from microalgae, a realistic
commercial process cannot rely on horizontal tubular photo-
bioreactor technology (Sa ´ nchez et al., 1999). Airlift and
bubble-column bioreactors are simple devices that have
gained wide acceptance in gas–liquid contacting application
in bioprocessing and in the chemical process industry and
can be useful for culturing phototropic organisms requiring
light as a source of energy (Kastanek et al., 1993). At
present, bubble columns and airlift reactors are not widely
used as photobioreactors, except for investigational pur-
poses. Nevertheless, because these systems have significant
advantages, there is a need to further develop bubble col-
umns and airlift devices as photobioreactors (Sa ´ nchez et al.,
2000; Rodolfi et al., 2008). However the obtained data indi-
cate that if the thickness of the bubbled algal suspension
layer exceeds 0.2m, the light availability will be severely
reduced. A flat photobioreactor for cultivation of photoau-
totrophic micro-organisms was described by Hu et al. (2000).
A flat panel laboratory airlift reactor with defined circulation
path was tested for microalgae culture by Degen et al.
(2001).
While many photobioreactors are easy to operate at lab-
oratory scale, only a few can be successfully scaled up to pilot
scale (Chaumont 1993; Ogbonna et al., 1997; Ugwu et al.,
2008). The scale-up strategies are very challenging, mainly
due to difficulties maintaining optimum light and tempera-
ture in photobioreactors. Important factors in process pro-
ductivity also include the availability of carbon oxide and
efficient oxygen removal.
The utilization of flue gas from incineration units for the
cultivation of algae was broadly discussed by Doucha et al.
(2005; 2006), Olaizola (2003), Wang et al. (2008) and
Douskova et al. (2009). The concept of a waste treatment
consisting of a combination of anaerobic fermentation and
subsequence algae cultivation has been introduced as a bior-
egenerative model farm system, where domestic and farm
wastes are recycled (Shelef et al., 1982; Douskova et al.,
2010). In general, despite the large number of papers devoted
to algae cultivation, information about the behaviour of algae
during their cultivation at field condition in bigger photobior-
eactors is very scarce. The aim of this study was the in-field
experimental verification of the cultivation of the microalgae
Chlorella sp. when using flue gas from the cogeneration unit
as a source of carbon dioxide. The data obtained from the
laboratory-scale bubblecolumn
volume of the batch in a reactor was 0.35L) were scaled-up
to the pilot bubble type photobioreactor (the volume of the
batch was up to 300L). Several field tests of the microalgae
cultivation in the pilot reactor were performed.
photobioreactors(the
Materials and method
Generation of biogas
Twoparallel anaerobicfermentors madeofstainless steelwith
a working volume of 2 ? 1500m3were used for anaerobic
production of biogas. The daily doses of substrates were: 16t
of swine manure, 2t of cereal husk, 18t of maize silage and 4t
ofsugarbeetpulp. Thesolidsubstratewas dosedwiththehelp
ofaspiralconveyerandthemanurewasdosedbyapump.The
biogas production was approximately 240m3h?1. The biogas
composition was as follows: 52% (v/v) of CH4, 300ppm of
H2S, 0.2% (v/v) of O2and 42% (v/v) of CO2.
Flue gas
The flue gas was generated in three co-generation units. Two
Tedom Cento 170 SP Bio (Tedom Ltd., Czech Republic)
units produced 2?170kW of electricity and 2?203kW of
heat. One unit Cento 180 SP Bio produced 180kW of elec-
tricity and 220kW of heat. The co-generation units were
located in the south Bohemia region near the town of
Znojmo, Czech Republic. Overall flue gas production was
approximately 500m3h?1. A small portion of the flue gas
was fed to the photobioreactor (1.33m3h?1). The flue gas
contained between 8% (v/v) and 10.2% (v/v) CO2, up to
46mgm?3NOx, 10mgm?3SO2, and 2mgm?3CO. The
flue gas was cooled in a heat exchanger to approximately
30?C. Due to the cooling, a liquid condensate amounting
to approximately 0.2Lday?1separated from the flue gas
before it was introduced into the photobioreactor.
Algal growth medium
The original growth medium based on an elemental biomass
composition had the following initial formula (mgL?1): 1100
(NH2)2CO;237KH2PO4;
40C10H12O8N2NaFe; 88CaCl2;
CuSO4?5H2O; 3.3 MnCl2?4H2O; 0.17 (NH4)6Mo7O24?4H2O;
2.7 ZnSO4?7H2O; 0.6 CoSO4?7H2O; and 0.014 NH4VO3in
tap water. The experiments were carried out in the batch
regime. The concentration of the suspended algal biomass
was determined both by the optical density measurement
(750nm) and by dry biomass weight determination.
204
0.83
MgSO4?7H2O;
H3BO3;0.95
Determination of gas concentrations
The concentrations of CO2and O2in the inlet gas mixtures
were measured continuously as well as the temperature of the
algal suspension and pH. CO2determination was performed
by infrared analyser Infralyt (Junkalor Dessau, Germany)
andO2
determinationby
Germany) measurement based on a zirconium oxide ion
selective sensor. The gas sampling (analysers suction) was
placed directly before the photobioreactor inlet.
Zirox(JunkalorDessau,
962Waste Management & Research 28(11)

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Microalgae
The strain P12 of the single-celled fresh water algae Chlorella
vulgaris BEIJ 1890 was used. The strain has a high specific
growth rate (about 0.22h?1under optimal conditions) and
has the ability to grow at high concentrations of CO2. The
strain is deposited in the Culture Collection of the Algal
Laboratory (CCALA),the
Academy of Sciences of the Czech Republic, the Centre of
Phycology.
Institute of Botany,the
Pilot-plant photobioreactor
A chart of the whole pilot experiment layout as well as the
schema of the PBR is shown in Figure 1. The pilot-plant
photobioreactor was a flat vertical prism-shaped closed
bubble reactor. Two flat transparent polycarbonate plates
(thickness 8mm, height 1500mm and length 2000mm)
formed the two large sides of the prism. The transparent
plates were secured in an iron frame. Potential bulges in
the transparent plates caused by the hydrostatic pressure
weresuppressed byafew
entrenched in the frame. The distance between the transpar-
ent plates was 130mm. There was the possibility to insert a
third transparent plate inside the prism and to form a nar-
rower reactor with the distance of the plates being 60mm.
The top of the prism was closed, with several openings left
for the operating and controlling instruments. The gas was
introduced into the photobioreactor through a perforated
pipe of diameter 25mm located at the bottom of the reactor.
The volumetric rate of the flue gas was 1.33m3h?1. This flow
rate corresponds to the linear velocities in the suspension in
horizontal ironstringers
the range of 0.14–0.3cms?1, identical to the range of the
linear velocities in the laboratory bubble columns. The
linear velocity of the inlet gas in the orifice of the perforated
pipe was maintained at a level greater than 10ms?1to ensure
a uniform distribution of the bubbles in the algal suspension.
During the experiments, the lengthwise axis of the prism was
situated in the east–west direction. During periods of suffi-
cient intensity of the natural light (>1000Lux), the suspen-
sion in the photobioreactor was bubbled with flue gas. After
nightfall, only air was supplied. The pH, temperature and the
concentrations of the gases were automatically registered and
saved in a computer. The set-up value of the pH in the sus-
pension was between 6.5 and 7.5 and was maintained auto-
matically by the addition of 1molL?1solution of NaOH
and by altering the feed of the flue gas and the feed of the
airaccordingtothepH
measurements.
andilluminationintensity
Results and discussion
The photobioreactor was tested and operated first on a mix-
ture of pure carbon dioxide with air (2% (v/v) of CO2and
under natural sunlight. Afterwards, the reactor was tested
with the flue gas obtained by co-generation of biogas in the
field conditions. The results of both tests are described below.
Microalgae cultivation in the pilot-plant
photobioreactor
The growth of the algae in the pilot photobioreactor oper-
ated on the mixture of food-grade CO2and air (2% (v/v) of
CO2) is shown in Figure 2 All other conditions were kept as
Solar photobioreactor
1 M NaOH
Air
(night)
Flue
gas
(day)
Flue
gas
Biogas
Swine Manure
Digestate
Condensate
Cooling
Cogeneration
unit
Heat
Electricity
Maize stilage
Anaerobic
fermentation
pH, T, CO2
O2, light
Figure 1. Scheme of the whole process and the pilot photobioreactor.
Kas ˇta ´nek et al.963

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described in the ‘Materials and methods’ section. The low
points on the zigzag growth curve correspond to the night-
time declines of the biomass content due to the aerobic res-
piration when aeration with air was applied. The average
productivity was 0.23g(DW)L?1day?1. It may be assumed
that during one calendar day in August the algae were effec-
tively exposed to sunshine for approximately 12h. Therefore,
it is estimated that the above-mentioned productivity was
obtained during12h.The
M¼0.019gL?1h?1.
During previous laboratory experiments, microalgae
were cultivated under constant artificial illumination in bub-
bled cylinders of different diameters (36, 65 and 140mm).
The microalgal growth was linear, which is the typical
growth pattern when cultivating microalgae under constant
illumination and temperature. The specific productivity of
the algae was correlated as a function of the cylinder diam-
eter with the formula
specificproductivity was
M ¼ 2:2D?0:8
ð1Þ
where M is the growth rate of the algae (gL?1h?1), and D
is the diameter of the cylinder (mm). The deviation between
the experimental data and the model values was <15%.
The data show that under the same illumination, a thicker
layer of the suspension produces a lower biomass concentra-
tion (Douskova et al., 2010). In comparison with the labora-
tory results, the productivity under the field conditions was
2.5 times lower than the productivity calculated with the help
of Equation (1) which was based on the laboratory data
obtained at constant illumination. The difference could
have been caused by significant temperature, illumination
and pH changes during the field cultivation that were mea-
sured in the following experiments.
During the following experiment the photobioreactor was
supplied with flue gas obtained from the cogeneration unit
located at the biogas station. Figure 3 shows the results of the
first experiment, in the beginning of which the inoculums of
algae were not yet adapted to the flue-gas. During the first 3
days, a lag phase (slow growth) was observed, due to the
adaptation of the algae. The algae recovery and growth
were significantly more efficient during the fourth day.
Lack of sunshine during the fifth and sixth days caused
another drop in temperature, a decrease in productivity
and a disturbance in the pH value which had to be moder-
ated by the control system. As the weather improved during
the last (seventh) day of the experiment, the growth rate
increased.
DW (g L–1)
2.5
Dry weight
Time (days)
0
1234567
2.0
1.5
1.0
0.5
0.0
Figure 2. Chlorella sp. growth in the pilot photobioreactor operating on the mixture of pure CO2and air (2% (v/v) of CO2).
Temperature (°C)
Temperature
Dry weight
pH
pH
DW (g L–1)
45
14
12
10
8
6
4
2
0
40
35
30
25
20
15
10
5
0
1.5
1.0
0.5
0.0
01234567
0123
Time (days)
456
7
Figure 3. Growth curve of Chlorella in field conditions. The
pilot photobioreactor was fed with the flue gases from a
co-generation unit (concentration of CO2between 8% (v/v) and
10.2% (v/v)). Adaptation of the microalgal culture algae on the
flue gas.
964 Waste Management & Research 28(11)

Page 5

Figure 4 shows the growth curve during the steady sun-
shine conditions. It can be seen that the day-and-night oscil-
lations in the temperature of the suspension and the pH
during the sunny days follow a pattern. At night, when the
suspension was bubbled with air only, the pH increased as a
consequence of dissolved CO2desorption. Furthermore, the
pattern of the oscillations in the concentration of the carbon
dioxide in the flue gas (supplied during the day period) and
the concentration of the oxygen (during the nights, when the
suspension was aerated) was almost regular. The algae pro-
ductivity obtained under such ideal weather conditions (sim-
ilar to the Mediterranean countries) was approximately
0.26gL?1day?1(or 0.021gL?1h?1on a 12h basis). The
daily temperature during the sunny days reached 28–30?C
(16?18?C at night). The productivity obtained with the mix-
ture of air and CO2(2% (v/v)) did not differ significantly
from the productivity obtained with the flue gas.
By contrast, Figure 5 shows the drop in temperature in
the photobioreactor during the following rainy days. The
outside temperature during the rainy days was 18–22?C
only (11–14?C at night). With the declining temperature
and, primarily, with the decrease of the sunshine, the pH
also decreased as the CO2 was not consumed. The huge
decrease of the pH bellow pH 5 was almost fatal for the
algae in the reactor. The control system based on the alter-
nation of the flue gas with the air and NaOH addition was
unable to maintain the pH in the desired range between 6.5
and 7.5. The swing in the acidity was large enough to cause a
decrease in the concentration of the algal biomass.
A single experiment (on a sunny day, with an average
daily outside temperature of 22?C) was performed with the
third transparent plate placed inside the prism. This arrange-
ment limited the thickness of the suspension to 60mm. The
obtained data show a substantial increase in the volumetric
Temperature (°C)
Temperature
Oxygen (%) (v/v)
Oxygen (%) (v/v)
Corbon dioxide (%) (v/v)
Corbon dioxide (%) (v/v)
pH
pH
DW (g L–1)
45
14
12
10
8
6
4
2
0
30
25
20
15
10
5
0
40
35
30
25
20
15
10
5
0
30
20
25
10
15
5
0
0
1234
Time (days)
Dry weight
0123
4
01
2
34
1.00
0.75
0.25
0.50
0.00
Figure 4. Growth curve of Chlorella sp. during ‘sunny days’.
The pilot photobioreactor was fed with the flue gases from a
co-generation unit (concentration of CO2between 8% (v/v) and
10.2 % (v/v)).
Temperature (°C)
Temperature
Oxygen (%) (v/v)
Oxygen (%) (v/v)
Corbon dioxide (%) (v/v)
Corbon dioxide (%) (v/v)
pH
pH
DW (g L–1)
45
14
12
10
8
6
4
2
0
30
25
20
15
10
5
0
40
35
30
25
20
15
10
5
0
30
20
25
10
15
5
0
0123
Time (days)
Dry weight
01
2
3
0
123
0.4
0.3
0.1
0.2
0.0
Figure 5. Growth curve of Chlorella sp. during ‘rainy days’.
The pilot photobioreactor was fed with the flue gases from a
co-generation unit (concentration of CO2between 8% (v/v) and
10.2 % (v/v)).
Kas ˇta ´nek et al.965

Page 6

productivity of the photobioreactor to 0.4gL?1day?1. More
experiments with the thin layers of the suspension under
favourable weather conditions are needed. Nevertheless,
including the obtained data with the thin layer of the suspen-
sion, the productivity of the growth of the algae was corre-
lated by the empirical Equation (2), which has a similar form
obtained in laboratory experiments (Equation (1)).
M0¼ 11D?0:8
ð2Þ
Accumulation of cogeneration incineration
products in the microalgal biomass
The toxicological analysis of the biomass grown using the
cogeneration flue gas was carried out (Table 1). It can be
assumed that no significant accumulation of heavy metals
or organic incineration products was observed. The biomass
even complied with the EU legal requirements on maximum
contaminants levels in foodstuff.
Conclusion
The major findings of the present study are summarized here.
The algae growth was not limited or inhibited by the com-
position of real flue gases and also no accumulation of harm-
ful incineration products was detected in the microalgal
biomass cultivated in the flue gas. In a mid-European climate
the growth rate of the Chlorella in the flat bubble reactor was
less than or equal to 0.4gL?1day?1(11–12h of sunlight,
60mm thickness of the layer of the algae suspension.) After
approximately 20 days of cultivation, the maximum values
reached for the so-called harvesting biomass concentration
were approximately 8gL?1. Because of the limited capacity
of the closed vertical bubble type photobioreactors, these
reactors were suitable and economically viable only for the
cultivation of the algae in cases where biomass products are
highly valued, or used as reactors for the production of low
volumes of pure cultures of innocula for larger systems.
Acknowledgements
This study was supported by CEZ Group, Czech Republic [grant
No. 2009.S079.02]; Czech Science Foundation [grant No. P503/
10/1270]; and the Ministry of Education Youth and Sports of
the Czech Republic [grant No. OE09025].
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Table 1. Concentrations of toxicologically relevant
compounds in the biomass of Chlorella vulgaris cultivated
on the cogeneration flue gas compared with the legal limits
ContaminantUpper legal limit Algal biomass cultivated
on flue gas
Cda
Pba
Hga
Benzo[a]pyrena
PAHsb
0.05 to 1mgkg?1
0.1 to 1.5mgkg?1
0.5 to 1mgkg?1
1 to 10mgkg?1
0.002mgkg?1
<0.02mgkg?1
<0.2mgkg?1
0.012mgkg?1
<0.5mgkg?1
<0.0005mgkg?1
aRequirements of the Commission Regulation (EC) No 1881/2006 of
19 December 2006 setting maximum levels for certain contaminants
in feedstuffs.
bAdditional requirements of the Decree of the Government of the
Czech Republic No. 305/2004 Col.
966Waste Management & Research 28(11)