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Use of concentric-tube airlift

photobioreactors for microalgal


outdoor mass cultures
F. Garcı́a Camacho, A. Contreras Gómez, F. G. Acién Fernández,
J. Fernández Sevilla, and E. Molina Grima

Department of Chemical Engineering, University of Almerı́a, Almerı́a, Spain

A vertical concentric-tube airlift photobioreactor (ALP) was used to cultivate Phaeodactylum tricornutum UTEX
640 in outdoor continuous mode during the summer. A mathematical model is developed to estimate the
irradiance profile and average irradiance inside the culture, and hence, to compare the biomass production
capability of the airlift device with a horizontal-loop tubular photobioreactor (HLTP) located at the same place
as the ALP. The maximum biomass productivities were similar in both photobioreactors in spite of the higher
light availability in HLTP; thus, the photosynthetic efficiency was higher in ALP. This behavior was attributed
to photoinhibition in HLTP and the negative effects of an inappropriate light-dark cycling. © 1998 Elsevier
Science Inc.

Keywords: Microalgal culture; photobioreactor; Phaeodactylum tricornutum

Introduction Airlift reactors allow better gas exchange, a more ordered


liquid flow, and hence, a more efficient exposure of cells to
Algal culture systems are generally classified according to
light.
their engineering and hydraulic characteristics as open
The choice of a suitable photobioreactor is a complicated
systems (including ponds, deep channel, shallow circulating
issue. Productivity comparison between culture systems
units, etc.) and closed or fully hydraulic systems commonly
may be a sufficient selection criterion. Availability of light
called photobioreactors. Both have been extensively re-
is another important factor that affects productivity; how-
viewed.1–5 The industrial-scale production of algal biomass
ever, illumination is difficult to control in outdoor cultures
for highly valuable products (e.g., polyunsaturated fatty
because of the variation in solar radiation during the day and
acids, sulfated polysaccharides, pigments, etc.) is feasible
nonhomogeneous distribution of radiation in a cylindrical
only in enclosed photobioreactors because contamination of geometry. Until now, the only model for light distribution
culture must be prevented. Of enclosed bioreactors, the and average solar irradiance inside a horizontal-loop tubular
horizontal tubular photobioreactors in which the circulation photobioreactor (HLTP) for outdoor microalgal culture was
of fluids is induced by bubbling air are now the best that developed by Acién Fernández et al.13 The HLTP was
accepted.6 –11 Although the horizontal tubular systems have horizontally arranged (surface slope, b, equal to 0°) and
notable advantages relative to conventional facilities (e.g., placed on a solar receptor where the disperse radiation
open ponds), they also have serious limitations such as distribution on tubes surface had singular characteristics
difficult temperature control, the need for frequent recar- (reflectance around 2). In addition, one of the main con-
bonation because of the tube length, growth inhibition by strains of this reactor and its emplacement (Almerı́a Bay,
dissolved oxygen, foaming, fouling, etc. These limitations 36°489N, 2°549W) was related to the photoinhibition effect
imply additional costs that may be justifiable only for which reduced the productivity of the system during the
high-value products.12 A possible alternative for overcom- summer because of the high peak irradiance values. This
ing the noted constrains may be the airlift reactor (ALP). effect was the main drawback of this type of photobioreac-
tor which otherwise had excellent performance.14
In the present study, a concentric-tube airlift (ALP) was
Address reprint requests to Dr. F. G. Camacho, University of Almeria, used to cultivate Phaeodactylum tricornutum UTEX 640 in
Department of Chemical Engineering, E-4071 Almeria, Spain outdoor continuous mode during the summer. Using a
Received 13 November 1997; revised 29 June 1998; accepted 16 July 1998 similar methodology to Acién Fernández et al.13 a mathe-

Enzyme and Microbial Technology 24:164 –172, 1999


© 1998 Elsevier Science Inc. All rights reserved. 0141-0229/99/$–see front matter
655 Avenue of the Americas, New York, NY 10010 PII S0141-0229(98)00103-3
Airlift photobioreactors for microalgal cultu: F. Garcı́a Camacho et al.

Figure 1 Scheme of outdoor culture system. Vertical concentric-tube airlift photobioreactor (1); medium reservoir (2); biomass
reservoir (3); temperature control system (4); pH controller (5); O2 register (6); solenoid valve (7); gas flow meter (8); CO2 cylinder (9);
air (10)

matical model is developed here to estimate the irradiance entrance of the draft tube. Air was used in all experiments. The
profile and average irradiance inside the culture, and hence oil-free air was filter sterilized (0.5 mm sterile filter) prior to use.
to compare the biomass production capability of ALP with
that of the HLTP used by Acién Fernández et al.14 Solar radiation measurement
A Meteocenter-386 (Geonica S. A., Madrid, Spain) weather station
Materials and methods was used to check the daily global radiation, H, during the
experimental run.
Organism and culture medium
The alga, P. tricornutum UTEX 640, and the culture medium were Analytical measurements
the same as those previously used by Molina Grima et al.7 Nutrient The biomass concentration, C b , chlorophylls, carotenoids, and
concentrations for the outdoor operation were successively in- biomass absorption coefficient, Ka, were measured in accordance
creased to avoid growth limitation; eventually the concentration with Acién Fernández et al.13
level was threefold that used by Molina Grima et al.7

Outdoor culture system


Mathematical model
The culture system located in Almerı́a, Spain (36°489N, 2°549W)
was a plexiglas airlift photobioreactor 0.096 m in diameter and 2 m The mathematical model determines the distance travelled by an
high (working volume of 12 3 1023 m3). The vessel contained a incident ray of light to any point inside the culture and estimates
1.5 m high concentric tube (riser). The cross-sectional areas of the the local irradiance taking into account the light attenuation due to
riser and downcomer were 2.83 3 1023 m2 and 2.8 3 1023 m2, biomass.
respectively. The bottom clearance was 0.1 m. A diagram of the The incident total radiation is divided into direct and disperse
culture system is shown in Figure 1. The photobioreactor was radiation. The former is characterized by having a direction
operated during summer as continuous culture at different dilution defined as a function of the position of the sun at any given
rates; thus, fresh medium was added at a constant rate for a 12-h moment while the latter, being reflected radiation, has no specific
daylight period, stopping dilution during the night until biomass direction.
concentration at sunrise was the same for four consecutive days. The model developed here is based on that of Acién Fernández
The cultures were operated at constant pH 7.7 that was maintained et al.13 but there are important differences to account for the
by on-demand injection of CO2. The pH was measured with an geometry of the airlift reactor.
Ingold pH glass probe. The dissolved oxygen was measured by an
Ingold polarographic probe.
Agitation and gassing were achieved by injecting air through a
Angle of incidence of direct radiation
perforated pipe with 30 holes of 1023 m diameter. The sparger The angle of incidence of direct radiation on the photobioreactor
(0.02 m in diameter, 0.03 m high) was located just inside the lower surface, that is, the angle between the incident beam and the

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Table 1 Equations used to estimate the local and average irradiances inside culture

cosu 5 sind z sinf z cosb 2 sind z cosf z sinb z cosg 1 cosd z cosf z cosb z cosv 1 cosd z cosf z sinb (1)
z cosg z cosv 1 cosd z sinb z sing z sinv
d 5 23.45 z sin [360 z (28/4 1 N )/365] (2)
v 5 15 z (12 2 sh ) (3)

Ho 5 S 24
p D S
z Isc z 1 1 0.033 z cos S
360 z N
365 DD S
z cos f z cos d z sinvs 1
2 z p z vs
360
z sinf z sind D (4)

cosv s 5 2tand z tanf (5)


Kh 5 H / H o (6)
H d / H 5 1.390 2 4.027 z Kh 1 5.530 z Kh 2 2 3.108 z Kh 3 (7)
HB 5 H 2 Hd (8)
I 5 H z Ef z SD Sp
24
z x 1 y z cosv) z Scosv z cosvs
sin vs 2 vs z cosvs D (9)

Id 5 Hd z Ef z SD S p
24
z
cosv z cosvs
sinvs 2 vs z cosvs D (10)

x 5 0.409 1 0.5016 z sin(vs 2 60) (11)


y 5 0.6609 2 04767 z sin(v s 2 60)
IB 5 I 2 Id (13)
cos u~g, v! (14)
Rb 5
cos uz ~v!
RD 5 ~1 1 cos b!/2 (15)
cos u z 5 cosd z cosf z cos v 1 sind z sinfa (16)
I Bt 5 R b z I B (17)
I dt 5 R D z I d
~1 2 cos b! (19)
Ir 5 ~IB 1 Id! z r z
2
I Dt 5 I dt 1 I r (20)
l 5 a z sinv 5 ri z cosw 2 R z cos « (21)
h 5 a z cosv 5 R z sin« 2 ri z sinw (22)
a 5
~ri z cos w 2 R z cos ε!
sinv
) 5 S
R z sine 2 ri z sin w
cos v
)
(23)

Pdisperse 5 Î ~h 1 I !
2 2 (26)
pdisperse 5 Î ~ri z sinw 2 R z sinε)2 1 (ri cosw 2 R z cosε)2 (27)

Eqs. (1)–(19) were obtained from Duffie and Beckman16 and Eqs. (21)–(27) from Acién Fernández et al.13,14
a
cos uz should be replaced with cosu [Eq. (1)] with g 5 v for any surface tangent to the ALP surface and not oriented north-south

normal to the surface, u, may be estimated at any given moment as for horizontal surfaces. On a tilted surface, the geometric factors,
a function of five variables: day of year (N); solar hour (sh); R b (the ratio of the beam radiation on the tilted surface, I Bt , to that
geographic latitude (f); surface slope (b), that is, the angle on a horizontal surface), and R D (the ratio of diffuse radiation on
between the plane surface in question and the horizontal, and the tilted surface, I dt , to that on a horizontal surface) must be taken
surface azimuth angle (g), that is, the deviation of the projection on into account [see Eqs. (14)–(18)].
a horizontal plane of the normal to the surface from the local Also, the solar radiation diffusely reflected from the ground, I r ,
meridian, with zero due south, east negative, west positive.15,16 was estimated by Eq. (19) (Table 1). A value of 0.5 was used for
The angles u and g were not used by Acién Fernández et al.13 For the ground reflectivity, r, because reflecting surfaces existed in the
a vertical airlift column, surface azimuth angle (g) will have surroundings of ALP (solar receptor of HLTP, white walls, etc.).
infinite possible values between 2180° and 180° because the The selected value of r was in between 0.7 and 0.2 that were
surface is cylindrical. recommended by Liu and Jordan15 for diffuse ground reflectance
The equation relating the angle of incidence of direct radiation of 0.2 with and without snow cover, respectively. Henceforth,
and the other variables is shown in Table 1 [Eq. (1)]. The hourly disperse irradiance on the ALP surface, I Dt , will refer to the
declination, d, and the angle corresponding to the solar hour, v, sum of the diffuse radiation and the solar radiation diffusely
needed for solving Eq. (1) are calculated according to Eqs. (2) and reflected from the ground [Eq. (20)].
(3), respectively. Eqs. (14)–(19) were not used by Acién Fernández et al.14
because of the singular distribution of disperse radiation on
Solar irradiance estimation surfaces of horizontal tubes.
The total daily radiation, H, daily diffuse radiation, H d , and daily
direct radiation, H B , on a horizontal surface were calculated
Length of path travelled by a ray of light
according to Eqs. (4)–(8) (Table 1). The theoretical values of H The distance, p Direct, travelled by a direct ray from the tube surface
and the measured data agreed within 9% error. to a point within the culture may be determined from the position
The photosynthetically active hourly direct, I B , and diffuse, I d , of the sun and the location of the point (ri, w) (Figure 2). Figure
irradiance on a horizontal surface were estimated by substituting H 3 shows the various angles in the cross-section of the tube. In spite
and H d in Eqs. (9)–(10) (Table 1), respectively, for firstly of the vertical orientation of the airlift, the trigonometric relation-
obtaining I and I d , and after in Eq. (13) to estimate I B . The hourly ships identical to those of Acién Fernández et al.13 could be used
direct and diffuse radiation values estimated in this way are valid to determine the transverse light path length, a (the projection of

166 Enzyme Microb. Technol., 1999, vol. 24, February 15/March


Airlift photobioreactors for microalgal cultu: F. Garcı́a Camacho et al.

Figure 2 Relation of characteristic angles with light path length associated with the penetration of direct radiation to an internal point
in the culture ( r i , w)

the true light path, p Direct, on the cross-section). The Eqs. (21)–
(23) of Table 1 were used, but the e value was p/2 2 g; thus, the
true light path, p Direct , was related to a (Figure 2) by the equation:
a z cos v R z sin e 2 ri z sin w
p Direct 5 5 (24)
cos~p/ 2 2 u9z ! cos~p/ 2 2 u9z !
where u9z is the zenith angle modified by the light refraction in the
culture. The angles u9z and u z are related to the indexes of
refraction in accordance with Snell’s law:
n 1 sinu9z
5 (25)
n 2 sinu z
where n 1 5 1 and n 2 5 1.33 are the refractive indexes of air and
water, respectively.
The path, p disperse, travelled by any disperse ray was deter-
mined as for HLTP [Eqs. (26) and (27), Table 1).

Local and average irradiance inside the culture


In a well-mixed microalgal mass culture system, light attenuation Figure 3 Projection of the characteristic angles and the solar
by biomass gives rise to a heterogeneous illumination profile ray on the normal section of the tube containing the considered
inside the culture bulk for which mathematical evaluation is point ( r i , w)

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Figure 4 Effect of dilution rate, D , on steady-state biomass concentration, biomass productivity, and average irradiance inside the
culture

essential in order to estimate the average irradiance on which the with growth severely limited by self-shading. This effect is
growth of the microalgae depends.17 Lambert-Beer’s law usually better observed in the variation of the average irradiance
represents this attenuation; therefore, the local direct, I Bt (r i , w), [calculated by Eq. (30)] with the dilution rate (Figure 4). As
and local disperse I Dt (r i , w), irradiances may be estimated with in previous works,17,19,21 the specific growth, m, and aver-
the following equations:
age irradiance, I av , in light-limited cultures followed a
I Bt ~r i , w! 5 I Bt ~g, v! z exp[2Ka~Xp! z C b z P Direct ] (28) hyperbolic relationship.
I Dt ~r i , w! 5 I Dt ~v! z exp[2Ka~Xp! z C b z P dirperse ] (29)
Summing Eqs. (28) and (29) provides the total hourly irradiance at Discussion
any point inside the culture. If this summation is extended to the
full culture volume, the hourly average irradiance, I av , may be Normally, the optimization of photobioreactor orientation is
estimated by: based on the same criteria as those for any solar process;

HS E E D
thus, for maximum annual energy availability, a surface
1 slope equal to latitude seems to be the best; a horizontal
I av 5 I Bt ~r i , w!rd rd w
p z R2 surface has the highest peak value of irradiance; however, at
R w

S EEE DJ
high irradiances, negative photoinhibition effects can ap-
1 pear.21–23 The slope is therefore, an important design factor
1 I Dt ~r i , w!rd rd wde (30) with regard to future yield of culture systems.9 In outdoor
2zp
R w e horizontal or inclined tubular photobioreactors, this design
variable cannot be varied significantly because of fluid-
dynamic problems and cells settling; however, the vertically
Results positioned bubble columns and airlift photobioreactors have
In Figure 4, the steady-state biomass concentration and not been used extensively in outdoor or indoor conditions.
biomass productivity are shown as a function of dilution The vertical arrangement will avoid the high irradiances in
rate, D. The pattern obtained was typical of a light-limited summer and spring, and during noonday for each day of the
continuous culture as previously reported;7,18 –20 that is, the year when the temperature is high and the photooxidative
higher the dilution rate or specific growth rate, the lower the processes in the cell are most marked. This effect can be
steady-state biomass concentration since availability of light seen in Figure 5 where average radiation on a monthly basis
is greater. The steady-state biomass concentration attained, on both vertical (b 5 90°) and horizontal (b 5 0°) surfaces
C b , is determined by the imposed dilution rate since the oriented N-S has been estimated from Eqs. (7) and (8). The
limiting growth factor is light availability which is limited maximum value of total radiation on the horizontal surface
by shelf-shading of the cells in dense cultures; thus, high is reached when it is minimum on the vertical surface and
dilution rates can be supported by fast-growing cells whose vice versa; however, the averaged total radiation received
illumination requirements can only be met at low biomass by both surfaces would be equal only if the latitude of
concentrations, and low dilution rates give rise to cultures facility was 45°. In contrast, it would be higher in horizontal

168 Enzyme Microb. Technol., 1999, vol. 24, February 15/March


Airlift photobioreactors for microalgal cultu: F. Garcı́a Camacho et al.

Figure 5 Annual variation of direct, diffuse,


and reflected monthly radiation on horizon-
tal (b 5 0°) and vertical (b 5 90°) surfaces in
Almerı́a (Spain), 36°489N latitude. There is no
reflected radiation for b 5 0° in accordance
with Eq. (19) of Table 1

surfaces as photobioreactor nears the equator and lower as it on a solar receiver with albedo values (reflectance) around
moves away from it. Because in this work, the location of 2.14 These special culture conditions increased the available
the ALP was at latitude 36°.489N, close to 45°, the averaged light to the cells. Consider a hypothetical case where a
total radiation received by both surfaces were similar steady-state biomass concentration of 1.9 g l21 and a
(19,942 kJm22 day21 for the vertical surface and 21,660 pigment content of 2.221% on dry weight (obtained in this
kJm22 day21 for the horizontal surface). work for D 5 0.033 h21) is maintained through the year in
In spite of these theoretical considerations in favor of a HLTP like the one used by Acién Fernández et al.13 but
photobioreactors arranged vertically, the maximum biomass with the same internal diameter as the concentric tube airlift
volumetric productivity obtained in the ALP was approxi- (ALP). As shown in Figure 6, the average irradiance inside
mately 1 g l21 day21 (Figure 4) which was about half that the HLTP culture would be always higher.
obtained by Acién Fernández et al.14 in a HLTP of 5 cm Acién Fernández et al.14 proposed a kinetic model for
internal diameter using the same algal species and time of estimating the year-long biomass productivity of microalgal
year; however, the comparison may be misleading if the cultures. That model reproduced the experimental results
experimental conditions are not considered. In the HLTP with less than a 10% error. The specific growth rate m was
culture system, the bioreactor diameter was smaller (5 cm related only to I av and to mean daily photosynthetic irradi-
versus 9.5 cm in ALP). Also, the external loop was located ance measured inside the thermostatic water pond of a

Figure 6 Comparison of annual variation of


average irradiance, I av , for ALP and HLTP (with
solar receiver) for C b 5 1.9 g l21

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Figure 7 Polar plot of irradiance profiles in the cross-section of ALP (dashed lines) and HLTP (solid lines) for the 0.0414 m and 0.023
m internal radiuses at the 8 and 12 solar h

HLTP solar receiver. This model applied irrespective of the apparatus. Repair and damage proceed simultaneously and
tube diameters employed; thus, using the highest value of the observed growth is the sum of the two processes. If a
I av (220 mEm22 s21 during the summer) calculated for dark period is introduced under this situation, the duration
HLTP (Figure 6) in the model proposed by Acién Fernán- of the photosynthetic period declines, but the damaging
dez et al.14, the expected biomass productivity in the HLTP period is also reduced while the photon trap repair continues
would be 0.95 g l21 day21. This value is similar to that during the dark time. Consequently, during the next light
obtained experimentally in the ALP for D 5 0.033 h21 and period, a substantially rejuvenated photon trap compensates
C b 5 1.9 g l21 (productivity 5 0.75 g l21 day21) and for the loss in photosynthetic time. Under these circum-
during the same time of the year. stances, alternating light/dark periods do not reduce growth
This behavior of HLTP, in spite of a higher illumination, which may in fact be slightly enhanced; nevertheless, the
must be related to the negative effects of an inappropriate length of the dark period is important. Lengthening the light
modulation of the light-dark cycle due to the interaction period beyond an optimal value will produce loss of growth.
between light distribution inside the culture and hydrody- The optimal or critical dark period is not a fixed quantity;
namics. Light is not always beneficial. Excessively high instead it depends on the photon flux density of the previous
photon flux density may reduce productivity via photoinhi- light period and the fluid residence time in zones of
bition.24 Photoinhibition is caused by oversaturation of different irradiance. Clearly, therefore, the principal prob-
photosystem II which damages the D1 protein that carries lem of designing or choosing a photobioreactor is assuring,
the binding site of the electron carrier.22,25 This photoinhi- for any species with preestablished photosynthetic charac-
bition effect is quite distinct from that of temperature teristics, that the largest possible fraction of cells experi-
increase that occurs in uncontrolled systems as a function of ences optimal exposure to light in the largest possible
the photon flux density. Whereas a single cell of microalgae reactor volume.
cannot be simultaneously photolimited and photoinhibited, In this sense in Figure 7, the local irradiance profiles in
in bioreactors photolimited and photoinhibited cell popula- both photobioreactors at 8 and 12 solar h are shown. As
tions may coexist because of variations in photointensity in expected, as the solar hour changes, curves of local irradi-
different zones. ance at the same internal ratio adjust to the position of the
At low light intensities, the few damaged D1 protein sun for both ALP and HLTP photobioreactors. In the
molecules are replaced rapidly and the net damage to the morning (sh 5 8), the ALP surface facing the sun had
photosynthetic apparatus is negligible. Under this situation, much higher direct irradiance values than the opposite side;
a dark period reduces growth rate (photosynthesis) because this difference is lower in HLTP; however, at noon, the
fewer photons are captured but no gain is obtained from the irradiance distribution in ALP, unlike HLTP, was practi-
dark time. In contrast, under conditions of intense illumi- cally homogeneous. That is, the local irradiance value at the
nation, part of the light energy impairs the photosynthetic same internal radius did not depend on the angle w. This

170 Enzyme Microb. Technol., 1999, vol. 24, February 15/March


Airlift photobioreactors for microalgal cultu: F. Garcı́a Camacho et al.
profile is because during midday, the contribution of dis- Acknowledgments
perse irradiance to total irradiance in relation to the direct
Assistance of Dr. Yusuf Chisti with the preparation of this
irradiance is very great in the ALP; thus, although the level
manuscript is greatly acknowledged. This research was
of irradiance for each internal radius and for any hour of the
supported by the Comision Interministerial de Ciencia y
day was higher in HLTP than in ALP, irradiance distribu-
Tecnologı́a (CICYT) (BIO-95-0652), Spain; Plan Andaluz
tion inside the culture as well as the pattern of cell de Investigación II, Junta de Andalucı́a, Spain; and the EEC
movement inside the photobioreactors were different. project BRPR CT97-0537.
The improved productivity in the ALP was apparently
due to a better combination of mixing and light distribution
in the riser and the downcomer. The mixing was higher List of symbols
inside the ALP than HLTP. A value of 0.04 m2 s21 was
calculated previously for the axial dispersion coefficient for a Projection of direct path length over cross-
the ALP26 and a value of 0.015 m2 s21 for the 5 3 1022 m section (m)
internal diameter HLTP was calculated following the ALP Vertical airlift photobioreactor
method described by Levenspiel27; moreover, with respect Cb Biomass concentration (g l21 or g m23)
to illumination, a certain grade of order exists in the flow of E13
f Photosynthetic efficiency of solar radiation,
the ALP because the culture is forced to circulate regularly 1.74 6 0.07 mE z J21
from an well-illuminated zone (downcomer) to a dark zone H Daily radiation on a horizontal surface (kJ
(riser). This would be in agreement with other works m22 d21)
showing that ordered flow and the increasing mixing im- HB Daily direct radiation on a horizontal surface
prove photosynthetic productivity.28,29 The calculated pho- (kJ m22d21)
tosynthetic efficiency30 also inferred this behavior; thus, Hd Daily diffuse radiation impinging on a hori-
during summer, the efficiency was approximately 20% for zontal surface (kJ m22 d21)
the ALP (C b 5 1.9 g l21) but only 9% for the hypothetical HLTP Horizontal-loop tubular photobioreactor
situation in the HLTP. Ho Daily global solar radiation on the atmosphere
surface, extraterrestrial radiation (kJ m22 d21)
In conclusion, vertically oriented concentric-tube airlift
I Hourly incident photosynthetic radiation
photobioreactors may be as productive a culture system as
(mE m22 s21)
HLTP; moreover, the productivity of the ALR may be
Iav Photosynthetically active hourly average irra-
higher when a comparison is made under identical illumi-
diance inside culture (mE m22 s21)
nation conditions. This conclusion is also supported by
IB Photosynthetically active hourly direct irradi-
other experimental work in a tubular-loop photobioreactor.9
ance on a horizontal surface (mE m22 s21)
Lee and Low9 also reported that despite the large differ- IBt(g, v) Direct hourly irradiance on ALP surface
ences in the amount of photosynthetic radiance absorbed by (mE m22 s21)
the algal cultures positioned at the various angles of IBt(ri, w) Local direct hourly irradiance inside ALP
inclination (0 – 80°), the overall biomass production rate (mE m22 s21)
over an 8-h period was comparable. Another advantage of a Id Photosynthetically active hourly diffuse irra-
vertical orientation is the smaller land area demand and the diance on a horizontal surface (mE m22 s21)
ease of scale-up. Idt Photosynthetically active hourly diffuse irra-
As seen in Figures 5 and 6, moreover, the highest values diance on a sloped surface (mE m22 s21)
of average irradiance inside the culture are attained during IDt(v) Disperse hourly irradiance on ALP surface
summer and spring in the HLTP whereas for the ALP, this (mE m22 s21)
occurs during autumn and winter (Figure 6); thus, the costs IDt(ri, w) Local disperse hourly irradiance inside ALP
of cooling should be lower with the ALP. (mE m22 s21)
Ir Photosynthetically active hourly reflected ir-
radiance on a surface (mE m22 s21)
Conclusions Isc Universal solar constant 1,353 W z m22
Ka Absorption coefficient (m2 g21)
The closed horizontal tubular systems have notable advan- Kh13 Daily clearness index, 0.74 6 9% (r2 5
tages relative to other more conventional photobioreactors; 0.918)
however, the horizontal tubular devices present significant N Day of the year
photoinhibition problems during the summer because of pDirect Path travelled by a direct radiation ray from
high peak irradiances. As shown in this work, the vertically the tube surface through the culture to an
oriented concentric-tube airlift systems offer a credible internal point (m)
alternative to horizontal tubular photobioreactors for cul- pdisperse Path travelled by any disperse ray (m)
tures at latitudes close to 45°. The vertical arrangement R ALP radius (m)
avoids the high irradiances in the summer and spring, and at Rb Geometric factor for direct radiation
noonday all through the year; thus, the airlift system seems RD Geometric factor for diffused radiation
to provide a more appropriate combination of local irradi- sh Solar hour
ance distribution, mixing, and ordered flow to assure a x Constant
suitable modulation of the light-dark periods. y Constant

Enzyme Microb. Technol., 1999, vol. 24, February 15/March 171


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b Surface slope (rad) 13. Acién Fernández, F. G., Garcı́a Camacho, F., Sánchez Pérez, J. A.,
g Surface azimuth angle (rad) Fernández Sevilla, J. M., and Molina Grima, E. A model for light
distribution and average solar irradiance inside outdoor tubular
d Declination (rad) photobioreactors for the microalgal mass culture. Biotechnol. Bio-
u Angle between the beam radiation on a sur- eng. 1997, 55, 701–714
face and the normal to that surface (rad) 14. Acién Fernández, F. G., Garcı́a Camacho, F., Sánchez Pérez, J. A.,
u9 Angle u modified by the light refraction in the Fernández Sevilla, J. M., and Molina Grima, E. Modelling of
culture (rad) biomass productivity in tubular photobioreactors for microalgal
cultures. Effects of dilution rate, tube diameter, and solar irradiance.
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