Use of concentric-tube airlift photobioreactors for microalgal outdoor mass cultures

F. Garc a Camacho, A. Contreras Go mez, F. G. Acie n Ferna ndez, J. Ferna ndez Sevilla, and E. Molina Grima
Department of Chemical Engineering, University of Almer a, Almer a, 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
Algal culture systems are generally classified according to their engineering and hydraulic characteristics as open systems (including ponds, deep channel, shallow circulating units, etc.) and closed or fully hydraulic systems commonly called photobioreactors. Both have been extensively reviewed.15 The industrial-scale production of algal biomass for highly valuable products (e.g., polyunsaturated fatty acids, sulfated polysaccharides, pigments, etc.) is feasible only in enclosed photobioreactors because contamination of culture must be prevented. Of enclosed bioreactors, the horizontal tubular photobioreactors in which the circulation of fluids is induced by bubbling air are now the best accepted.6 11 Although the horizontal tubular systems have notable advantages relative to conventional facilities (e.g., open ponds), they also have serious limitations such as difficult temperature control, the need for frequent recarbonation because of the tube length, growth inhibition by dissolved oxygen, foaming, fouling, etc. These limitations imply additional costs that may be justifiable only for high-value products.12 A possible alternative for overcoming the noted constrains may be the airlift reactor (ALP).

Address reprint requests to Dr. F. G. Camacho, University of Almeria, Department of Chemical Engineering, E-4071 Almeria, Spain Received 13 November 1997; revised 29 June 1998; accepted 16 July 1998

Airlift reactors allow better gas exchange, a more ordered liquid flow, and hence, a more efficient exposure of cells to light. The choice of a suitable photobioreactor is a complicated issue. Productivity comparison between culture systems may be a sufficient selection criterion. Availability of light is another important factor that affects productivity; however, illumination is difficult to control in outdoor cultures because of the variation in solar radiation during the day and nonhomogeneous distribution of radiation in a cylindrical geometry. Until now, the only model for light distribution and average solar irradiance inside a horizontal-loop tubular photobioreactor (HLTP) for outdoor microalgal culture was that developed by Acie n Ferna ndez et al.13 The HLTP was horizontally arranged (surface slope, , equal to 0) and placed on a solar receptor where the disperse radiation distribution on tubes surface had singular characteristics (reflectance around 2). In addition, one of the main constrains of this reactor and its emplacement (Almer a Bay, 3648N, 254W) was related to the photoinhibition effect which reduced the productivity of the system during the summer because of the high peak irradiance values. This effect was the main drawback of this type of photobioreactor which otherwise had excellent performance.14 In the present study, a concentric-tube airlift (ALP) was used to cultivate Phaeodactylum tricornutum UTEX 640 in outdoor continuous mode during the summer. Using a similar methodology to Acie n Ferna ndez et al.13 a mathe-

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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 profile and average irradiance inside the culture, and hence to compare the biomass production capability of ALP with that of the HLTP used by Acie n Ferna ndez et al.14

entrance of the draft tube. Air was used in all experiments. The oil-free air was filter sterilized (0.5 m sterile filter) prior to use.

Solar radiation measurement

A Meteocenter-386 (Geonica S. A., Madrid, Spain) weather station was used to check the daily global radiation, H , during the experimental run.

Materials and methods Organism and culture medium

The alga, P. tricornutum UTEX 640, and the culture medium were the same as those previously used by Molina Grima et al.7 Nutrient concentrations for the outdoor operation were successively increased to avoid growth limitation; eventually the concentration level was threefold that used by Molina Grima et al.7

Analytical measurements
The biomass concentration, C b , chlorophylls, carotenoids, and biomass absorption coefficient, Ka , were measured in accordance with Acie n Ferna ndez et al.13

Outdoor culture system

The culture system located in Almer a, Spain (3648N, 254W) was a plexiglas airlift photobioreactor 0.096 m in diameter and 2 m high (working volume of 12 103 m3). The vessel contained a 1.5 m high concentric tube (riser). The cross-sectional areas of the riser and downcomer were 2.83 103 m2 and 2.8 103 m2, respectively. The bottom clearance was 0.1 m. A diagram of the culture system is shown in Figure 1. The photobioreactor was operated during summer as continuous culture at different dilution rates; thus, fresh medium was added at a constant rate for a 12-h daylight period, stopping dilution during the night until biomass concentration at sunrise was the same for four consecutive days. The cultures were operated at constant pH 7.7 that was maintained by on-demand injection of CO2. The pH was measured with an Ingold pH glass probe. The dissolved oxygen was measured by an Ingold polarographic probe. Agitation and gassing were achieved by injecting air through a perforated pipe with 30 holes of 103 m diameter. The sparger (0.02 m in diameter, 0.03 m high) was located just inside the lower

Mathematical model
The mathematical model determines the distance travelled by an incident ray of light to any point inside the culture and estimates the local irradiance taking into account the light attenuation due to biomass. The incident total radiation is divided into direct and disperse radiation. The former is characterized by having a direction defined as a function of the position of the sun at any given moment while the latter, being reflected radiation, has no specific direction. The model developed here is based on that of Acie n Ferna ndez et al.13 but there are important differences to account for the geometry of the airlift reactor.

Angle of incidence of direct radiation

The angle of incidence of direct radiation on the photobioreactor 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 cos sin sin cos sin cos sin cos cos cos cos cos cos cos sin cos cos cos sin sin sin 23.45 sin [360 (28/4 N )/365] 15 (12 sh ) 24 360 N 2 s Isc 1 0.033 cos sin sin cos cos sins Ho 365 360 cos s tan tan Kh H / H o H d / H 1.390 4.027 Kh 5.530 Kh 2 3.108 Kh 3 HB H Hd cos coss x y cos) I H Ef 24 sin s s coss cos coss Id Hd Ef 24 sins s coss x 0.409 0.5016 sin(s 60) y 0.6609 04767 sin( s 60) IB I Id cos , Rb cos z RD 1 cos /2 cos z cos cos cos sin sina I Bt R b I B I dt R D I d 1 cos Ir IB Id 2 I Dt I dt I r l a sin ri cos R cos h a cos R sin ri sin R sin ri sin ri cos R cos ) ) a sin cos 2 2 Pdisperse h I (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11) (13) (14) (15) (16) (17) (19) (20) (21) (22) (23) (26) (27)

pdisperse
a

ri

sin R sin)2 (ri cos R cos)2

Eqs. (1)(19) were obtained from Duffie and Beckman16 and Eqs. (21)(27) from Acie n Ferna ndez et al.13,14 cos z should be replaced with cos [Eq. (1)] with for any surface tangent to the ALP surface and not oriented north-south

normal to the surface, , may be estimated at any given moment as a function of five variables: day of year ( N ); solar hour ( sh ); geographic latitude (); surface slope (), that is, the angle between the plane surface in question and the horizontal, and surface azimuth angle (), that is, the deviation of the projection on a horizontal plane of the normal to the surface from the local meridian, with zero due south, east negative, west positive.15,16 The angles and were not used by Acie n Ferna ndez et al.13 For a vertical airlift column, surface azimuth angle () will have infinite possible values between 180 and 180 because the surface is cylindrical. The equation relating the angle of incidence of direct radiation and the other variables is shown in Table 1 [Eq. (1)]. The declination, , and the angle corresponding to the solar hour, , needed for solving Eq. (1) are calculated according to Eqs. (2) and (3), respectively.

Solar irradiance estimation

The total daily radiation, H , daily diffuse radiation, H d , and daily direct radiation, H B , on a horizontal surface were calculated according to Eqs. (4)(8) (Table 1). The theoretical values of H and the measured data agreed within 9% error. The photosynthetically active hourly direct, I B , and diffuse, I d , irradiance on a horizontal surface were estimated by substituting H and H d in Eqs. (9)(10) (Table 1), respectively, for firstly obtaining I and I d , and after in Eq. (13) to estimate I B . The hourly direct and diffuse radiation values estimated in this way are valid

for horizontal surfaces. On a tilted surface, the geometric factors, R b (the ratio of the beam radiation on the tilted surface, I Bt , to that on a horizontal surface), and R D (the ratio of diffuse radiation on the tilted surface, I dt , to that on a horizontal surface) must be taken into account [see Eqs. (14)(18)]. Also, the solar radiation diffusely reflected from the ground, I r , was estimated by Eq. (19) (Table 1). A value of 0.5 was used for the ground reflectivity, , because reflecting surfaces existed in the surroundings of ALP (solar receptor of HLTP, white walls, etc.). The selected value of was in between 0.7 and 0.2 that were recommended by Liu and Jordan15 for diffuse ground reflectance of 0.2 with and without snow cover, respectively. Henceforth, hourly disperse irradiance on the ALP surface, I Dt , will refer to the sum of the diffuse radiation and the solar radiation diffusely reflected from the ground [Eq. (20)]. Eqs. (14)(19) were not used by Acie n Ferna ndez et al.14 because of the singular distribution of disperse radiation on surfaces of horizontal tubes.

Length of path travelled by a ray of light

The distance, p Direct, travelled by a direct ray from the tube surface to a point within the culture may be determined from the position of the sun and the location of the point ( ri , ) ( Figure 2). Figure 3 shows the various angles in the cross-section of the tube. In spite of the vertical orientation of the airlift, the trigonometric relationships identical to those of Acie n Ferna ndez et al.13 could be used to determine the transverse light path length, a (the projection of

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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 , )

the true light path, p Direct, on the cross-section). The Eqs. (21) (23) of Table 1 were used, but the value was /2 ; thus, the true light path, p Direct , was related to a ( Figure 2) by the equation: p Direct a cos R sin ri sin cos / 2 cos / 2 z z (24)

where z is the zenith angle modified by the light refraction in the culture. The angles z and z are related to the indexes of refraction in accordance with Snells law: n 1 sin z n 2 sin z (25)

where n 1 1 and n 2 1.33 are the refractive indexes of air and water, respectively. The path, p disperse, travelled by any disperse ray was determined 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 by biomass gives rise to a heterogeneous illumination profile inside the culture bulk for which mathematical evaluation is
Figure 3 Projection of the characteristic angles and the solar ray on the normal section of the tube containing the considered point ( r i , )

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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 growth of the microalgae depends.17 Lambert-Beers law usually represents this attenuation; therefore, the local direct, I Bt ( r i , ), and local disperse I Dt ( r i , ), irradiances may be estimated with the following equations: I Bt r i , I Bt , exp[Ka Xp C b P Direct ] I Dt r i , I Dt exp[Ka Xp C b P dirperse ] (28) (29)

with growth severely limited by self-shading. This effect is better observed in the variation of the average irradiance [calculated by Eq. (30)] with the dilution rate (Figure 4). As in previous works,17,19,21 the specific growth, , and average irradiance, I av , in light-limited cultures followed a hyperbolic relationship.

Summing Eqs. (28) and (29) provides the total hourly irradiance at any point inside the culture. If this summation is extended to the full culture volume, the hourly average irradiance, I av , may be estimated by: I av 1 R2

Discussion
Normally, the optimization of photobioreactor orientation is based on the same criteria as those for any solar process; thus, for maximum annual energy availability, a surface slope equal to latitude seems to be the best; a horizontal surface has the highest peak value of irradiance; however, at high irradiances, negative photoinhibition effects can appear.2123 The slope is therefore, an important design factor with regard to future yield of culture systems.9 In outdoor horizontal or inclined tubular photobioreactors, this design variable cannot be varied significantly because of fluiddynamic problems and cells settling; however, the vertically positioned bubble columns and airlift photobioreactors have not been used extensively in outdoor or indoor conditions. The vertical arrangement will avoid the high irradiances in summer and spring, and during noonday for each day of the year when the temperature is high and the photooxidative processes in the cell are most marked. This effect can be seen in Figure 5 where average radiation on a monthly basis on both vertical ( 90) and horizontal ( 0) surfaces oriented N-S has been estimated from Eqs. (7) and (8). The maximum value of total radiation on the horizontal surface is reached when it is minimum on the vertical surface and vice versa; however, the averaged total radiation received by both surfaces would be equal only if the latitude of facility was 45. In contrast, it would be higher in horizontal

1 2
R

I Bt r i , r d r d

I Dt r i , r d r d d

(30)

Results
In Figure 4, the steady-state biomass concentration and biomass productivity are shown as a function of dilution rate, D . The pattern obtained was typical of a light-limited continuous culture as previously reported;7,18 20 that is, the higher the dilution rate or specific growth rate, the lower the steady-state biomass concentration since availability of light is greater. The steady-state biomass concentration attained, C b , is determined by the imposed dilution rate since the limiting growth factor is light availability which is limited by shelf-shading of the cells in dense cultures; thus, high dilution rates can be supported by fast-growing cells whose illumination requirements can only be met at low biomass concentrations, and low dilution rates give rise to cultures 168

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Figure 5 Annual variation of direct, diffuse, and reflected monthly radiation on horizontal ( 0) and vertical ( 90) surfaces in Almer a (Spain), 3648N latitude. There is no reflected radiation for 0 in accordance with Eq. (19) of Table 1

surfaces as photobioreactor nears the equator and lower as it moves away from it. Because in this work, the location of the ALP was at latitude 36.48N, close to 45, the averaged total radiation received by both surfaces were similar (19,942 kJm2 day1 for the vertical surface and 21,660 kJm2 day1 for the horizontal surface). In spite of these theoretical considerations in favor of photobioreactors arranged vertically, the maximum biomass volumetric productivity obtained in the ALP was approximately 1 g l1 day1 (Figure 4) which was about half that obtained by Acie n Ferna ndez et al.14 in a HLTP of 5 cm internal diameter using the same algal species and time of year; however, the comparison may be misleading if the experimental conditions are not considered. In the HLTP culture system, the bioreactor diameter was smaller (5 cm versus 9.5 cm in ALP). Also, the external loop was located

on a solar receiver with albedo values (reflectance) around 2.14 These special culture conditions increased the available light to the cells. Consider a hypothetical case where a steady-state biomass concentration of 1.9 g l1 and a pigment content of 2.221% on dry weight (obtained in this work for D 0.033 h1) is maintained through the year in a HLTP like the one used by Acie n Ferna ndez et al.13 but with the same internal diameter as the concentric tube airlift (ALP). As shown in Figure 6, the average irradiance inside the HLTP culture would be always higher. Acie n Ferna ndez et al.14 proposed a kinetic model for estimating the year-long biomass productivity of microalgal cultures. That model reproduced the experimental results with less than a 10% error. The specific growth rate was related only to I av and to mean daily photosynthetic irradiance 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 1.9 g l1

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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 tube diameters employed; thus, using the highest value of I av (220 Em2 s1 during the summer) calculated for HLTP (Figure 6) in the model proposed by Acie n Ferna ndez et al.14, the expected biomass productivity in the HLTP would be 0.95 g l1 day1. This value is similar to that obtained experimentally in the ALP for D 0.033 h1 and C b 1.9 g l1 (productivity 0.75 g l1 day1) and during the same time of the year. This behavior of HLTP, in spite of a higher illumination, must be related to the negative effects of an inappropriate modulation of the light-dark cycle due to the interaction between light distribution inside the culture and hydrodynamics. Light is not always beneficial. Excessively high photon flux density may reduce productivity via photoinhibition.24 Photoinhibition is caused by oversaturation of photosystem II which damages the D1 protein that carries the binding site of the electron carrier.22,25 This photoinhibition effect is quite distinct from that of temperature increase that occurs in uncontrolled systems as a function of the photon flux density. Whereas a single cell of microalgae cannot be simultaneously photolimited and photoinhibited, in bioreactors photolimited and photoinhibited cell populations may coexist because of variations in photointensity in different zones. At low light intensities, the few damaged D1 protein molecules are replaced rapidly and the net damage to the photosynthetic apparatus is negligible. Under this situation, a dark period reduces growth rate (photosynthesis) because fewer photons are captured but no gain is obtained from the dark time. In contrast, under conditions of intense illumination, part of the light energy impairs the photosynthetic 170

apparatus. Repair and damage proceed simultaneously and the observed growth is the sum of the two processes. If a dark period is introduced under this situation, the duration of the photosynthetic period declines, but the damaging period is also reduced while the photon trap repair continues during the dark time. Consequently, during the next light period, a substantially rejuvenated photon trap compensates for the loss in photosynthetic time. Under these circumstances, alternating light/dark periods do not reduce growth which may in fact be slightly enhanced; nevertheless, the length of the dark period is important. Lengthening the light period beyond an optimal value will produce loss of growth. The optimal or critical dark period is not a fixed quantity; instead it depends on the photon flux density of the previous light period and the fluid residence time in zones of different irradiance. Clearly, therefore, the principal problem of designing or choosing a photobioreactor is assuring, for any species with preestablished photosynthetic characteristics, that the largest possible fraction of cells experiences optimal exposure to light in the largest possible reactor volume. In this sense in Figure 7, the local irradiance profiles in both photobioreactors at 8 and 12 solar h are shown. As expected, as the solar hour changes, curves of local irradiance at the same internal ratio adjust to the position of the sun for both ALP and HLTP photobioreactors. In the morning ( sh 8), the ALP surface facing the sun had much higher direct irradiance values than the opposite side; this difference is lower in HLTP; however, at noon, the irradiance distribution in ALP, unlike HLTP, was practically homogeneous. That is, the local irradiance value at the same internal radius did not depend on the angle . This

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profile is because during midday, the contribution of disperse irradiance to total irradiance in relation to the direct irradiance is very great in the ALP; thus, although the level of irradiance for each internal radius and for any hour of the day was higher in HLTP than in ALP, irradiance distribution inside the culture as well as the pattern of cell movement inside the photobioreactors were different. 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 inside the ALP than HLTP. A value of 0.04 m2 s1 was calculated previously for the axial dispersion coefficient for the ALP26 and a value of 0.015 m2 s1 for the 5 102 m internal diameter HLTP was calculated following the method described by Levenspiel27; moreover, with respect to illumination, a certain grade of order exists in the flow of the ALP because the culture is forced to circulate regularly from an well-illuminated zone (downcomer) to a dark zone (riser). This would be in agreement with other works showing that ordered flow and the increasing mixing improve photosynthetic productivity.28,29 The calculated photosynthetic efficiency30 also inferred this behavior; thus, during summer, the efficiency was approximately 20% for the ALP ( C b 1.9 g l1) but only 9% for the hypothetical situation in the HLTP. In conclusion, vertically oriented concentric-tube airlift photobioreactors may be as productive a culture system as HLTP; moreover, the productivity of the ALR may be higher when a comparison is made under identical illumination conditions. This conclusion is also supported by other experimental work in a tubular-loop photobioreactor.9 Lee and Low9 also reported that despite the large differences in the amount of photosynthetic radiance absorbed by the algal cultures positioned at the various angles of inclination (0 80), the overall biomass production rate over an 8-h period was comparable. Another advantage of a vertical orientation is the smaller land area demand and the ease of scale-up. As seen in Figures 5 and 6, moreover, the highest values of average irradiance inside the culture are attained during summer and spring in the HLTP whereas for the ALP, this occurs during autumn and winter (Figure 6); thus, the costs of cooling should be lower with the ALP.

Acknowledgments
Assistance of Dr. Yusuf Chisti with the preparation of this manuscript is greatly acknowledged. This research was supported by the Comision Interministerial de Ciencia y Tecnolog a (CICYT) (BIO-95-0652), Spain; Plan Andaluz de Investigacio n II, Junta de Andaluc a, Spain; and the EEC project BRPR CT97-0537.

List of symbols
a ALP Cb E13 f H HB Hd HLTP Ho I Iav IB IBt(, ) IBt(ri, ) Id Idt IDt() IDt(ri, ) Ir Projection of direct path length over crosssection (m) Vertical airlift photobioreactor Biomass concentration (g l1 or g m3) Photosynthetic efficiency of solar radiation, 1.74 0.07 E J1 Daily radiation on a horizontal surface (kJ m2 d1) Daily direct radiation on a horizontal surface (kJ m2d1) Daily diffuse radiation impinging on a horizontal surface (kJ m2 d1) Horizontal-loop tubular photobioreactor Daily global solar radiation on the atmosphere surface, extraterrestrial radiation (kJ m2 d1) Hourly incident photosynthetic radiation (E m2 s1) Photosynthetically active hourly average irradiance inside culture (E m2 s1) Photosynthetically active hourly direct irradiance on a horizontal surface (E m2 s1) Direct hourly irradiance on ALP surface (E m2 s1) Local direct hourly irradiance inside ALP (E m2 s1) Photosynthetically active hourly diffuse irradiance on a horizontal surface (E m2 s1) Photosynthetically active hourly diffuse irradiance on a sloped surface (E m2 s1) Disperse hourly irradiance on ALP surface (E m2 s1) Local disperse hourly irradiance inside ALP (E m2 s1) Photosynthetically active hourly reflected irradiance on a surface (E m2 s1) Universal solar constant 1,353 W m2 Absorption coefficient (m2 g1) Daily clearness index, 0.74 9% (r2 0.918) Day of the year Path travelled by a direct radiation ray from the tube surface through the culture to an internal point (m) Path travelled by any disperse ray (m) ALP radius (m) Geometric factor for direct radiation Geometric factor for diffused radiation Solar hour Constant Constant 171

Conclusions
The closed horizontal tubular systems have notable advantages relative to other more conventional photobioreactors; however, the horizontal tubular devices present significant photoinhibition problems during the summer because of high peak irradiances. As shown in this work, the vertically oriented concentric-tube airlift systems offer a credible alternative to horizontal tubular photobioreactors for cultures at latitudes close to 45. The vertical arrangement avoids the high irradiances in the summer and spring, and at noonday all through the year; thus, the airlift system seems to provide a more appropriate combination of local irradiance distribution, mixing, and ordered flow to assure a suitable modulation of the light-dark periods.

Isc Ka Kh13 N pDirect pdisperse R Rb RD sh x y

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Z Z s Surface slope (rad) Surface azimuth angle (rad) Declination (rad) Angle between the beam radiation on a surface and the normal to that surface (rad) Angle modified by the light refraction in the culture (rad) Zenith angle of the sun (rad) Zenith angle of the sun modified by the light refraction in the culture (rad) Reflectance of surroundings (value used was 0.5) Latitude (in our case 3648N) (rad) Angle corresponding to the solar hour (rad) Hour angle at sunrise (rad)
13. Acie n Ferna ndez, F. G., Garc a Camacho, F., Sa nchez Pe rez, J. A., Ferna ndez Sevilla, J. M., and Molina Grima, E. A model for light distribution and average solar irradiance inside outdoor tubular photobioreactors for the microalgal mass culture. Biotechnol. Bioeng. 1997, 55, 701714 Acie n Ferna ndez, F. G., Garc a Camacho, F., Sa nchez Pe rez, J. A., Ferna ndez Sevilla, J. M., and Molina Grima, E. Modelling of biomass productivity in tubular photobioreactors for microalgal cultures. Effects of dilution rate, tube diameter, and solar irradiance. Biotechnol. Bioeng. 1997, 58, 605 616 Liu, B. Y. H. and Jordan, R. C. The interrelationship and characteristic distribution of direct, diffuse and total solar radiation. Solar Energ. 1960, 7, 53 65 Duffie, J. A. and Beckman, W. A. Solar Engineering of Thermal Processes. John Wiley & Sons, New York, 1980, Molina Grima, E., Garc a Camacho, F., Sa nchez Pe rez, J. A., Ferna ndez Sevilla, J. M., Acie n Ferna ndez, F. G., and Contreras Go mez, A. A mathematical model of microalgal growth in lightlimited chemostat culture. J. Chem. Tech. Biotechnol. 1994, 61, 167173 Goldman, J. C. Outdoor algal mass cultures. II. Photosynthetic field limitations. Water Res. 1979, 13, 119 160 Molina Grima, E., Sa nchez Pe rez, J. A., Garc a Camacho, F., Garc a Sa nchez, J. L., and Lo pez Alonso, D. n3 PUFA productivity in chemostat cultures of microalgae. Appl. Microbiol. Biotechnol. 1993, 38, 599 605 Molina Grima, E., Sa nchez Pe rez, J. A., Garc a Camacho, F., Ferna ndez Sevilla, J. M., and Acie n Ferna ndez, F. G. Productivity analysis of outdoor chemostat culture in tubular air-lift photobioreactors. J. Appl. Phycol. 1996, 8, 369 380 Molina Grima, E., Ferna ndez Sevilla, J. M., Sa nchez Pe rez, J. A., and Garc a Camacho, F. A study on simultaneous photolimitation and photoinhibition in dense microalgal cultures taking into account incident and averaged irradiances. J. Biotechnol. 1996, 45, 59 69 Jensen, S. and Knutsen, G. Influence of light and temperature on photoinhibition of photosynthesis in Spirulina platensis. J. Appl. Phycol. 1993, 5, 495504 Vonshak, A. and Guy, R. Photoinhibition as a limiting factor in outdoor cultivation of Spirulina platensis. In: Algal Biotechnology (Stadler, T., Mollion, J., Verdus, M. C., Karamanos, Y., Morvan, H., and Christiaen, D., Eds.). Elsevier Science Publ., New York, 1988, 365370 Powells, S. B. Photoinhibition of photosynthesis induced by visible light. Ann. Rev. Plant Physiol. 1984, 35, 15 44 Barber, J. A. A. Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem. Sci. 1992, 17, 61 66 Merchuk, J. C., Contreras, A., Garc a, F., and Molina, E. Studies of mixing in a concentric-tube airlift bioreactor with different spargers. Chem. Eng. Sci. 1997. 53, 709 719 Levenspiel, O. The Chemical Reactor Omnibook. OSU Book Stores, Corvallis, OR, 1979 Laws, E. A., Terry, K. L., Wickman, J., and Chalup, M. S. A simple algal production system designed to utilize the flashing light effect. Biotechnol. Bioeng. 1983, 25, 2319 2335 Ma rkl, H., Modelling of algal production systems. In: Algal Biomass (Shelef, C. J., Ed.). Elsevier/North Holland, Amsterdam, 1980, 361383 Molina Grima, E., Garc a Camacho, F., Sa nchez Pe rez, J. A., Acie n Ferna ndez, F. G., and Ferna ndez Sevilla, J. M. Evaluation of photosynthetic efficiency in microalgal cultures using averaged irradiance. Enzyme Microb. Technol. 1997, 21, 375381

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