Biochemical Engineering Journal 32 (2006) 13–18

Cultivation of Spirulina platensis in a combined

airlift-tubular reactor system
Attilio Converti ∗ , Alessandra Lodi, Adriana Del Borghi, Carlo Solisio
Department of Chemical and Process Engineering, University of Genoa, Via Opera Pia 15, 16145 Genoa, Italy
Received 22 February 2005; received in revised form 5 July 2006; accepted 24 August 2006

Abstract
This preliminary study aims at evaluating the efficiency of a bench-scale tubular photobioreactor by means of batch cultivations of Spirulina
platensis under light-limited conditions. The most interesting feature of this plant configuration is the use of an airlift system for biomass re-cycling
instead of traditional pumps to avoid the well-known problems of trichome damage owing to mechanical stress. A maximum cell concentration
of 10.6 g l−1 was attained after 15 days of cultivation using a photosynthetic active radiation of 120 ␮mol photons m−2 s−1 . Although the system
operated in laminar flow under all the conditions investigated in this study, excess thricome stress was prevented only at relatively low air flow
rates (<4.5 l min−1 ), corresponding to culture speeds lower than 0.21 m s−1 .
© 2006 Elsevier B.V. All rights reserved.

Keywords: Tubular bioreactor; Spirulina platensis; Light intensity; Biomass growth; Culture speed

1. Introduction grow in open ponds, except in the tropics, so as its production

Spirulina platensis is a marine microalga whose cultivation is
particularly attractive for several commercial purposes; it can be
used either as nutritional supplement for humans and animals [1]
or as source of active principles in pharmaceutical and cosmetic
industries [2]. Moreover, this microalga has been successfully
employing in integrated systems for wastewater treatment [3],
recovered and re-utilised [4] also as adsorbent material for heavy
metals [5].
For the above reasons, its large-scale production is of great
interest; the most widely used systems are the outdoor cultures
that allow obtaining large amounts of biomass at low costs.
Nowadays, the commercial production of this microalga is car-
ried out almost exclusively in open systems [6–8], which do
not require either particular care or control of the environmental
conditions (light and temperature). However, such systems did
not allow reaching very high biomass concentration because of
the difficulty of maintaining the optimal temperature, easiness of
contamination and limited exploitability of light due to low sur-
face/volume ratio [9]. In addition, during winter, this alga cannot
∗ Corresponding author. Tel.: +39 010 3532593; fax: +39 010 3532586.
E-mail address: converti@unige.it (A. Converti).
must be resumed once winter is over [10].
The use of a tubular bioreactor [11] can reduce these disad-
vantages owing to its particular structure. In fact, being closed,
it is able to provide a controlled environment preventing con-
tamination. Besides, thanks to its large outer surface exposed to
the light, it increases the surface/volume ratio with respect to
other configurations and reduces the shadow effect, which is the
main cause of growth inhibition in open ponds. Finally, such a
plant configuration makes the control of the operational param-
eters easier, hence resulting in an increased biomass production.
However, the peculiar fragility of the sheath of S. platensis and
its filamentous morphology [12,13] impose some constraints in
the design of a photobioreactor. The experience gathered over
many years on the culture of this microalga in tubular reactor
points out the diameter of the tubes, the length of the reactor
tube, the mixing of the culture and the circulation device as the
main factors influencing its performance [14].
The surface/volume ratio is mainly regulated by the diameter
of the tubes, therefore this factor has a strong impact upon the
irradiation intensity on the culture. On the other hand, the tube
length influences the circulation of the cultivation medium inside
the reactor, i.e. the residence time. During biomass circulation,
the photosynthetic activity of the cells causes the oxygen con-
centration to increase [15] and rate depends on light intensity,

1369-703X/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.bej.2006.08.013
14 A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18

biomass concentration and temperature. Since a high concen-

tration of dissolved oxygen affects both growth and protein
synthesis [16], the cultivation conditions should be selected so as
to prevent oxygen accumulation. Mixing is necessary to assure
a good exposure of biomass to light and an adequate distribu-
tion of nutrients. Finally, the selection of the re-cycling device
is crucial for the successful design of a bioreactor, since it can
exert a negative effect of mechanical stress on the cells [17]. The
airlift system is increasingly used for this purpose in the pres-
ence of very dense cultures of filamentous cyanobacteria such
as S. platensis, because it allows avoiding damages to the sheath
[18].
S. platensis cultivations were carried out in this work in two
bench-scale open ponds and one bench-scale tubular reactor, in
order to evaluate and compare the performance of these differ-
ent reactor configurations. The efficiency of the tubular reactor,
which was composed of a set of glass tubes disposed to form
a “loop” and an airlift system for biomass re-cycling, was then
checked by varying the main parameters typically influencing
the algal growth, i.e. the light intensity and the re-cycling flow
rate.
2. Materials and methods
2.1. Microorganism
S. platensis (UTEX 1926) was obtained from the Culture
Collection of the University of Texas. Cells were maintained
in the medium of Schlösser [19], whose composition was as
follows (per liter): 13.6 g NaHCO3 , 4.03 g Na2 CO3 , 0.50 g
K2 HPO4 , 2.50 g NaNO3 , 1.00 g K2 SO4 , 1.00 g NaCl, 0.20 g
MgSO4 ·7H2 O, 0.04 g CaCl2 ·2H2 O, pH 9.6. All the nutrients
were dissolved in distilled water containing (per liter): 6.0 ml
of metal solution (97.0 mg FeCl3 ·6H2 O, 41.0 mg MnCl2 ·4H2 O,
5.0 mg ZnCl2 , 2.0 mg CoCl2 ·6H2 O, 4.0 mg Na2 MoO4 ·2H2 O),
1.0 ml of micronutrient solution (50.0 mg Na2 EDTA, 618 mg
H3 BO3 , 19.6 mg CuSO4 ·5H2 O, 44.0 mg ZnSO4 ·7H2 O, 20.0 mg
CoCl2 ·6H2 O, 12.6 mg MnCl2 ·4H2 O, 12.6 mg Na2 MoO4 ·2H2 O)
and 1.0 ml of a 1.5 ␮g l−1 B12 vitamin solution.
A suspension collected at the latest exponential growth phase
was harvested, filtered, washed with 0.9% NaCl solution and
used to inoculate either the ponds or the tubular photobioreactor.
Fig. 1. Experimental set-up of open ponds.
2.3. Cultivations in tubular reactor
The tubular reactor (Fig. 2) was composed of a set of 21 glass
tubes, each having a length of 1 m, inner and outer diameters of
12 and 14 mm, respectively. The tubes were arranged horizon-
tally with a slight inclination and placed on two parallel planes
so that they were not superimposed each other and could feel
the same light intensity. The culture was continuously mixed by
injecting compressed air at the bottom of the tubes by means of
a pump blowing air into a vertical pipe used as a riser. A 3.0-l
Erlenmeyer flask closed with cotton cap was used at the top of
photobioreactor as a reservoir and degasser. The air bubbles pro-
vided efficient de-oxygenation by scouring the inner surface of
the tubes. The total volume of the culture (tubes plus reservoir)
was 5.5 l, the illuminated surface area and the surface/volume
ratio were 0.40 m2 and 135 m−1 , respectively. Culture tempera-
ture was monitored at 30 ± 1 ◦ C by incubation of the equipment
within a thermostatted chamber. The pH was daily adjusted at
9.5 whenever it exceeded 10.0 by bubbling gaseous CO2 .
Cultivations were carried out in the tubular reactor with the
aim of comparing the efficiency of this system with that of
the ponds. For this purpose, preliminary experiments were per-
formed at Xo = 0.15 g l−1 under the same conditions of light
intensity and temperature as those employed in the ponds. Suc-
cessively, according to the literature [20,21], light intensity was

2.2. Cultivations in open ponds

Three batch cultivations were performed in quadruplicate in

two open ponds at different starting biomass concentrations,
namely 0.15, 0.30 and 0.50 g l−1 . Each pond (Fig. 1), having
a surface area of 0.13 m2 and a water depth of 5 cm, was contin-
uously illuminated by eight fluorescent lamps (40 W), located
at about 40 cm over its surface, furnishing a light intensity
of 55 ␮mol photons m−2 s−1 . Culture mixing was assured by
paddled wheels at 25 rpm. Temperature was kept at the opti-
mum value suggested by the literature for S. platensis growth
(30 ± 1 ◦ C) [8,20] by means of electrical heaters. The pH, which
was daily monitored by a pH meter, never exceeded 9.5, hence
assuring bicarbonate availability for microalga growth. Fig. 2. Experimental set-up of the combined airlift-tubular reactor system.
 A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18
increased up to 120 ␮mol photons m−2 s−1 and re-cycling flow
rate was progressively raised from 0.34 to 4.5 l min−1 to evaluate
the influence of these parameters on the reactor performance.
2.4. Analytical procedures
Cell concentration was determined by dry weight after fil-
tration through Millipore filters (0.45-␮m pore diameter) and
washing with 3.0N acetic acid solution to eliminate precipitates.
The light intensity was measured by an irradiometer (Delta
OHM, mod. HD 9021, Padua, Italy) as photon flux density
(PPFD). This parameter is usually converted in photosynthet-
ically active radiation (PAR) (␮mol photons m−2 s−1 ), express-
ing the effective radiation quantity that the alga is able to
utilise. The measurements were performed at different points
of the plant surface to ensure an average illumination intensity.
The input of PAR (IPAR), expressing the quantity of radiation
impacting on the reactor, was calculated as suggested by Watan-
abe and Hall [22] as the product of PAR (kJ m−2 d−1 ) and the
illuminated surface (m2 ). For the conversion of PAR expressed
as ␮mol photons m−2 s−1 to kJ m−2 d−1 , the conversion factor
18.78 kJ s d−1 ␮mol−1 for cool white fluorescent lamps has been
used [23].
According to Watanabe and Saiki [24], the photosynthetic
efficiency (%) (PE) was calculated as:
rG HG × 100
PE =
IPAR
where rG is the maximum daily growth (gDB d−1 ) and HG the
enthalpy of dry biomass (21.01 kJ gDB −1 ) [25].
3. Results and discussions
Fig. 3 shows the behavior of S. platensis growth in ponds
at two different inoculum concentrations, namely Xo = 0.15 and
0.50 mg l−1 . At given light intensity and temperature, a higher
inoculum level (Xo = 0.50 g l−1 ) allowed the system to reach the
maximum growth (1.5 g l−1 ) in shorter time (about 10–15 d) than
at Xo = 0.15 g l−1 (about 20 d). The dramatic increase in biomass
concentration observed in the tubular reactor at Xo = 0.15 g l−1
in the same figure demonstrates the better performance of such
a configuration with respect to the ponds. The successive tests
Fig. 3. Comparison of S. platensis growth performed in tubular reactor (()
Xo = 0.15 g l−1 ); ponds ((䊉) Xo = 0.15 g l−1 ; () Xo = 0.50 g l−1 ).
15
Fig. 4. Biomass growth in tubular reactor at different light intensities. PAR
(␮mol photons m−2 s−1 ): (䊉) 55; () 80; () 120.
were then performed in tubular reactor, and the influence of light
intensity and air flow rate on S. platensis growth were explored.
Fig. 4 illustrates the growth behavior versus time at dif-
ferent PAR values (55, 80 and 120 ␮mol photons m−2 s−1 ).
The light intensity did not seem to influence biomass
growth up to a cell concentration of about 1 g l−1 , while
a positive effect is evident beyond this threshold. Besides,
PAR = 55 ␮mol photons m−2 s−1 allowed producing a maxi-
mum cell concentration (Xm ) of only 6.5 g l−1 , hence evidencing
a clear photolimitation effect; increasing the light intensity up
to 80 and 120 ␮mol photons m−2 s−1 , biomass level increased,
reaching Xm = 10.6 g l−1 within 19 and 15 days, respectively.
(1)
The different kinetics of these cultivations suggests that no
photoinhibition took place under the conditions investigated
in this study. These results can be considered to be a signifi-
cant advance if compared with those obtained in raceway ponds
(Xm = 0.8 g l−1 ) [26], tubular airlift reactor (Xm = 4.2 g l−1 ) [17]
and elevated panels (Xm = 5.0 g l−1 ) [27].
Since Xm did not increase further when raising the light inten-
sity from 80 to 120 ␮mol photons m−2 s−1 , it is likely that a
shading effect limited the biomass growth [29] when its level
exceeded a critical threshold. In fact, the amount of light that
impinges on the cells does depend not only on the surface
exposed to radiation but also on the depth of the culture, if ponds
are used, or the degree of turbulence and the population density,
if the tubular reactor is employed [4,28], as the superficial film
of biomass hinders the light through the inner biomass, thus
preventing the optimal enlightenment.
Table 1 summarizes the main results of these tests, high-
lighting the performance of the tubular reactor in comparison
with that of the ponds (Table 2) in terms either of biomass pro-
ductivity or photosynthetic efficiency. A PAR increase from
55 to 120 ␮mol photons m−2 s−1 resulted in a correspond-
ing increase in productivity from 0.29 to 0.62 gDB l−1 d−1 ,
whereas PE resulted to be practically independent of the
light intensity (PE = 8.0–8.1%), which is consistent with the
above suggested light-limited conditions in the tubular reac-
tor. These results also confirm that, at the same light intensity
(55 ␮mol photons m−2 s−1 ), the tubular reactor allowed for bet-
ter exposition and higher photosynthetic efficiency with respect
to the ponds, where the cells likely experienced full light radia-
tion at the surface and darkness at the bottom.
16 A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18

Table 1
Cell productivities obtained for Spirulina platensis cultivations carried out in tubular photobioreactor under different condition

PARa (␮mol m−2 s−1 ) IPARb (kJ d−1 ) Qx c (gDB l−1 d−1 ) vd (m s−1 ) μe (d−1 ) PEf (%)

55 413 0.29 0.05 0.17 8.1

80 601 0.42 0.05 1.7 8.1
120 901 0.62 0.05 0.19 8.0
55 413 0.18 0.21 0.13 4.9

Starting biomass concentration = 0.50 gDB l−1 .

a PAR, photosynthetic active radiation.
b IPAR, input of photosynthetic active radiation.
c Q , average cell productivity.
x
d v, culture speed.
e μ, average specific growth rate.
f PE, photosynthetic efficiency.

Alternation of light and dark periods were considered to be as
a crucial factor for a stable, high density culture of S. platensis
[1]. During the dark period, some of biomass is in fact con-
sumed by respiration [30], the consumed fraction consisting of
reserve materials such as carbohydrates and lipids. Since the
heterotrophic metabolism in the absence of light is notoriously
quicker than the autotrophic one and energetically more prof-
itable, it is possible that its occurrence would be fundamental to
guarantee a long-term survival of photosynthetic organisms. In
this sense, turbulence in outdoor systems may represent the most
practical way to create an intermittent pattern to illuminate cells
[31]. Such a necessary light–dark alternation was ensured in
our system by lateral illumination in addition to the secondary
motion caused by the centrifugal effect in correspondence of
tube curvature [32].
During the growth in the tubular reactor, the microalga
showed a tendency to settle in the tubes, probably due to the
high biomass level; in order to reduce this disadvantage, a fur-
ther test was performed under the same conditions (Xo = 0.5 g l−1
and PAR = 55 ␮mol photons m−2 s−1 ) but increasing the culture
specific upward velocity from 0.05 up to 0.21 m s−1 so as to
assure better mixing in the tubes. Biomass concentration reached
a maximum (Xm = 2.75 g l−1 ) after 13 days (data not shown) and
decreased slowly. The unsatisfactory productivity and photo-
synthetic efficiency (Qx = 0.18 g l−1 d−1 and PE = 4.9%, respec-
tively) obtained under these conditions (Table 1) suggest a state
of mechanical stress ascribable to excess flow rate, which was
confirmed by the microscopial observation of necridia (sacrifi-
Mixing of the culture and then its rheological properties
are very important for the operation of the bioreactor, because
they influence nutrient supply, exposition to the light and mass
transfer conditions [11]. So, culture circulation inside the airlift-
tubular reactor system becomes one of the main factors to be
taken into account to improve its performance, especially in
terms of productivity.
In order to evaluate the effect of culture speed on the behavior
of S. platensis culture, this parameter was gradually increased
from 0.05 to 0.21 m s−1 by increasing the air flow rate from 0.33
to 4.5 l min−1 . According to Torzillo [11], these values were
tested at two extreme biomass concentrations, namely at very
low (about 0.05 g l−1 ) and high (10 g l−1 ) biomass levels. These
authors did in fact demonstrate that S. platensis cultures behave
as Newtonian fluids at biomass concentrations of about 2 g l−1 or
lower, while over 4 g l−1 they showed a pseudoplastic behavior.
Moreover, the experiments performed in the bioreactor revealed
that an increase in biomass concentration up to 10 g l−1 led to an
extensive entanglement of the culture; therefore, a progressive
rise in the air flow was needed to favor its disentanglement.
For high biomass concentration (X = 10 g l−1 ), the relation
valid for the non-Newtonian fluids was then assumed according
to Metzner and Reed [33]:
 
 Dn v(2−n ) ρ
NRe =  (2)
K 8(n −1)
where NRe is the Reynolds number for non-Newtonian fluids,

cial cells) in the trichome that lost its cellular content becoming D the inner diameter of pipes, v the culture speed, ρ the culture
colorless [12]. density, n the flow behavior index and K is the consistency

Table 2
Cell productivities obtained for Spirulina platensis cultivations carried out in open ponds under different conditions

Xo a (gDB l−1 ) PARb (␮mol m−2 s−1 ) IPARc (kJ d−1 ) Qx d (gDB l−1 d−1 ) μe (d−1 ) PEf (%)

0.15 55 134 0.050 0.12 5.9

0.30 55 134 0.054 0.098 6.4
0.50 55 134 0.060 0.081 7.1
a Xo , starting biomass concentration.
b PAR, photosynthetic active radiation.
c IPAR, input of photosynthetic active radiation.
d Qx , average cell productivity.
e μ, average specific growth rate.
f PE, photosynthetic efficiency.
 A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18
index. In this equation, n and K can be considered as the degree
of non-Newtonian fluid behavior of the culture and the culture
consistency, respectively.
For Newtonian fluids, n = 1 and K reduces to viscosity of the
fluid, therefore for low biomass concentration (X = 0.05 g l−1 )
the relation valid for the Newtonian fluids may be applied:
Dvρ
NRe =
μv
where μv is the culture viscosity (kg m−1 s−1 ).
The parameter K is defined as:
 
3n − 1 n
K = K
4n
where K (dynes sn cm−2 ) is the power law constant of the expo-
nential equation of Ostwald-de Waele:
τw = K(γw )n
being τw (dynes cm−2 ) is the shear stress and γw (s−1 ) is the
shear rate.
It should be noticed that the n parameter appearing in Eqs.
(4) and (5), denominated power law index, corresponds to the
non-Newtonian behavior index (n ) of Eq. (2).
Assuming for n and K the values calculated by Torzillo
for a biomass concentration of 10.2 g l−1 , namely 0.540 and
0.577 dynes sn cm−2 [11], it was possible to evaluate the fluid
dynamic behavior of the system under the above two limit con-
ditions (Fig. 5). The values of the Reynolds number were low in
both cases, even when the maximum air flow rate was applied
at the lower biomass concentration, hence indicating that the
system always worked in laminar flow. It was suggested that the
Reynolds number should be higher than 2100 to assure turbu-
lence flow [17]; therefore, these conditions could be only get
at very high concentration of biomass, but a high air flow led
to cells damage probably produced in the bubbled section, and
during bubble disengagement. Because significant increases in
the culture speed (from 0.05 to 0.21 m s−1 ) did not imply any
proportional increase in the culture re-cycling flow, it can be
deduced that low culture speeds (0.16 m s−1 or lower) should
Fig. 5. Dependence of the Reynolds number on the culture re-cycling flow rate
at different biomass concentrations: () 10 g l−1 ; (䊉) 0.05 g l−1 .
17
Table 3
Different fluid dynamic conditions tested for Spirulina platensis cultivations
performed in the airlift-tubular photobioreactor
Air flow rate Culture re-cycling Culture speed
(l min−1 ) flow rate (l min−1 ) (m s−1 )
0.33 0.34 0.05
1.0 0.78 0.11
2.0 1.07 0.16
(3)
3.5 1.34 0.20
4.5 1.40 0.21
be sufficient to assure good mixing of the culture, avoiding cell
(4) damage.
The plant configuration proposed in this study did not allow
even at the highest tested flow rate reaching turbulent regime
conditions, which were considered by some authors to be crucial
to ensure significant productivity increases [34,35]. Neverthe-
(5) less, it was demonstrated that the optimal conditions of turbu-
lence regime were very narrow (2680 < NRe < 4000) in the spe-
cific photobioreactor they utilised and that a turbulence excess
was deleterious for the culture [35].
As described in Table 3, an increased air flow rate (from 3.5
to 4.5 l min−1 ) did not result in any significant increase either
in the culture re-cycling flow rate or in the culture speed. This
suggests that the best operating conditions for the tubular photo-
bioreactor would be those of a laminar regime preventing culture
damage. The next effort will deal with improvement of the bub-
bled section so as to minimize cell damage at high culture speed.
4. Conclusions
The main novelty of this work was the simultaneous use of a
tubular photobioreactor with slightly inclined tubes, so that the
fluid circulation was guaranteed by the simple gravity force, and
an airlift system to prevent shear stress to a culture of S. platensis.
The experimental biomass concentrations obtained under differ-
ent conditions were higher than those reported in the literature
for analogous systems and much higher than those obtained in
open ponds.
The results presented in this study confirm that, under light-
limited and laminar flow conditions, the air flow rate in the
airlift system for S. platensis re-cycling appreciably influences
biomass productivity and photosynthetic efficiency of a tubu-
lar photobioreactor. In fact, if from the one hand, turbulent
conditions should favor the cultivation because of enhanced
mass transfer, from the other hand, they can induce cell dam-
age when filamentous microorganisms like S. platensis are used,
hence requiring an optimum compromise between these oppo-
site requirements.
The proposed plant configuration proved to be very promising
under the suboptimal conditions investigated in this preliminary
study; therefore, in order to get a clearer picture of its potential, a
set of additional fed-batch tests will be performed in next work,
varying the light intensity, the regime conditions and comparing
the results with those of tests to be performed alternating dark
and light periods.
18 A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18
Acknowledgement
The authors thank the financial support of MIUR (Italy),
FIRB 2002, Prot. RBAU01E83L, to carry out this work.
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