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