Microalgal Reactors: A Review of Enclosed System Designs and Performances
Ana P. Carvalho, Luı ´s A. Meireles, and F. Xavier Malcata*
Escola Superior de Biotecnologia, Universidade Cato ´lica Portuguesa, Rua Dr. Anto ´nio Bernardino de Almeida, P-4200-072
One major challenge to industrial microalgal culturing is to devise and develop technical apparata,
cultivation procedures and algal strains susceptible of undergoing substantial increases in
efficiency of use of solar energy and carbon dioxide. Despite several research efforts developed
to date, there is no such thing as “the best reactor system”- defined, in an absolute fashion, as
the one able to achieve maximum productivity with minimum operation costs, irrespective of
the biological and chemical system at stake. In fact, choice of the most suitable system is situation-
dependent, as both the species of alga available and the final purpose intended will play a role.
The need of accurate control impairs use of open-system configurations, so current investigation
has focused mostly on closed systems. In this review, several types of closed bioreactors described
in the technical literature as able to support production of microalgae are comprehensively
presented and duly discussed, using transport phenomenon and process engineering methodologi-
cal approaches. The text is subdivided into subsections on: reactor design, which includes tubular
reactors, flat plate reactors and fermenter-type reactors; and processing parameters, which include
gaseous transfer, medium mixing and light requirements.
2. Reactor design
2.1. Tubular reactors
2.1.1.Vertical tubular reactors
2.1.2.Horizontal tubular reactors
2.1.3.Helical tubular reactors
2.2. Flat plate reactors
2.3. Fermenter-type reactors
3. Processing parameters
3.1. Gaseous transfer
3.3. Light requirement
From an economic point of view, microalgae may be
described as microorganisms with the ability to “harvest the
sun” and hence transform its radiant energy into valuable
products, at the expense of (theoretically) inexpensive natural
resources (viz., CO2and H2O). The idea of producing microal-
gae at the technical scale first occurred to German scientists, in
concerted attempts to devise inexpensive sources of protein able
to replace those from animal sources, which were difficult to
obtain during World War II (1). In the U.S., research on mass
culture of microalgae began as a collateral development of
fundamental studies on photosynthesis; in attempts to translate
the biological requirements of microalgal culture into engineer-
ing specifications, a large-scale culture plant was made at
Stanford Research Institute, back in 1948. During 1951, Arthur
D. Little, Inc. (Cambridge, MA) made further advances through
construction and operation of a Chlorella pilot plant for the
Carnegie Institution (2). Other studies followed in Japan, under
the guidance of Tamiya (2). Although experimental results
showed that continuous culture was possible, many subjects still
needed improvement, as microalgal proteins could not compete
with such inexpensive plant sources as soybean meal.
Other developments were achieved by Oswald, who started
studying the role of microalgal photosynthesis in ponds and
accordingly developed a high-rate algal pond for photosyn-
thetic wastewater treatment. In the 1960s, Nichoporovich and
Semenenko intensively studied closed culture systems, for
extraterrestrial life support during prolonged missions in outer
space; this subject also received considerable attention by NASA
(1). The advent of the oil crisis in the 1970s led researchers to
investigate microalgae as potential sources of biomass, aiming
at methane production (3); more recently, advances have focused
on the production of fine chemicals and secondary metabolites,
which may reach high prices in the world market.
The evolution in goals throughout time has therefore been
driven by two major streamlines: (i) requirement for alternative
sources of several products, which were scarce as a result of
political or economic reasons; and (ii) perception that microal-
gal-mediated processes (as happens with most biotechnological
ones) are usually characterized by noncompetitive production
costs, the economic feasibility of which relies heavily on the
market value of the resulting compounds. As expected, the
* To whom correspondence should be addressed. Tel: 351 225 580 004.
Fax: 351 225 090 351. Email: firstname.lastname@example.org.
Biotechnol. Prog. 2006, 22, 1490−1506
10.1021/bp060065r CCC: $33.50 © 2006 American Chemical Society and American Institute of Chemical Engineers
Published on Web 11/15/2006
nature of these compounds has evolved with time, in response
to changing market demands.
A broad list of applications of microalga cultures has been
described and discussed in the literature. Those that have attained
commercial expression encompass the areas of healthy foods,
food additives, pigments, diets for aquaculture, growth-regulat-
ing agents, secondary metabolites and wastewater treatments
(4, 5) (see Table 1). The production of several bioactive
compounds such as hydrocarbons, isotopes, polysaccharides, and
antifungal, antitumor, antibacterial and antiviral substances is
currently under study; uses of microalgae for CO2 fixation,
removal of nitric oxide from flue gas, fuel production, recovery
of heavy metals from effluents and in outer space technologies
are also in order (3, 5-11). Nevertheless, despite such enormous
potential, the number of applications that has reached the
industrial scale is comparatively rather limited.
From the pioneer commercial large-scale cultures of microal-
gae in the 1960s in Japan using Chlorella (12), only a few more
species have been employed industrially ever since, which
include Spirulina sp. and Scenedesmus sp. for healthy food and
phycocyanin synthesis (a blue colorant in food and cosmetics),
Haematococcus pluVialis for production of astaxanthin (a food
colorant), and Dunaliella salina for the manufacture of ?-car-
otene (a vitamin A substitute and food colorant). In addition,
Crypthecodinium cohnii and Schizochytrium sp. are also com-
mercially used for production of polyunsaturated fatty acids
(e.g., docosahexaenoic acid), although following a fermentative
Open ponds were the ancient configurations proposed for
microalga production and are still the most widely applied in
industrial processes. They usually consist of either circular ponds
with a rotating arm to mix the culture, or long channels in a
single or multiple loop configuration stirred by paddle wheels
(3), although simpler configurations also exist. The main
constraints related to operation of these open systems are the
impossibility to control contamination, the difficulty to keep
the culture environment constant and the cost of the harvesting
stage. In order to avoid microbial contamination, highly selective
conditions are necessary, so as to guarantee dominance by the
selected strain (e.g., D. salina dominance requires highly salted
media, whereas Spirulina platensis demands high pH values);
unfortunately, both of these conditions are not suitable for most
microalgal species. The direct effect of weather conditions on
the characteristics of the open-pond cultivation media also makes
it very difficult to keep preset values for the environmental
parameters. Regarding the harvesting phase, the huge volume
of culture to be harvested (because of the low cell densities
attained) magnifies the cost of processing, thus substantially
increasing the final cost of the product. Because of the
aforementioned serious constraints, open systems have appar-
ently reached their upper limit, with little room for further
In view of these difficulties, another approach was envisaged,
which is based on the alternative use of closed systems. These
are more appropriate for sensitive strains (which grow in non-
extreme environments) or when the final product is highly
susceptible to microbial degradation (e.g., bacterial metaboliza-
tion of amino acids and polysaccharides). The closed config-
uration makes the control of contaminants easier, hence allowing
growth in photo-autotrophic, heterotrophic or mixotrophic
modes; because of the higher cell mass productivities attained
(up to 3-fold those obtained in open systems) (3), harvesting
costs per unit mass can also be significantly reduced. Neverthe-
less, the costs of closed systems are higher than their open-
system counterparts, in addition to several other disadvantages
(see Table 2). In fact, despite their higher volumetric productiv-
ity, closed systems were not a consensual industrial choice until
only recently; intensive capital investments and high production
costs account for this realization. In order to minimize produc-
tion costs, the major factors that play a role in the process ought
to be identified and their specific contributions comprehensively
studied, in order to maximize advantages and minimize disad-
vantages. The choice of which configuration is preferable
depends obviously on the objective function considered; e.g.,
wastewater treatment would preclude closed systems, owing to
the unacceptably high costs that arise from the large volumes
to be processed and the low added value of the feedstock
When improvement in efficacy of a closed photo-bioreactor
is the goal, light and CO2supply are key processing parameters,
especially owing to the difficulties associated with their control
(viz., assurance of stability throughout time and uniformity
throughout space); most of the so-called novel bioreactors do
in fact attempt to overcome the constraints related to control of
said parameters (14). However, the technology that supports
supply of adequate amounts of CO2to microalgal cells is still
poorly developed, which contrasts with the substantial research
efforts currently underway on the genetic improvement of native
freshwater and marine species for specific applications. On the
other hand, although the problem of light supply has sometimes
been circumvented by growing the microalgae heterotrophically,
not all microalgae (or microalgal products, for that matter) can
be produced in this way.
Therefore, issues such as contamination control, gaseous
exchanges, mixing patterns, suitability of light supply (which
comprises light quality and quantity), geometrical configuration
and building material are considered relevant, and will accord-
ingly be discussed to some extent in this review. The aspects
of nutrient supply, as well as pH and temperature control, will
not be considered here, because no major improvements are
Table 1. Generic Description of Commercial Microalgal Culture Systems Currently in Use
microorganismmetabolite commercial useculturing systemlocation
Chlorella spp.astaxanthinpigmenting agent circular ponds with
extensive open ponds
ferredoxin laboratory use
?-carotenepigmenting agent Australia, China, India,
Chile, U.S., Israel
functional food additive
functional food additive
Biotechnol. Prog., 2006, Vol. 22, No. 6
expected therefrom, as their control is rather simple. There has
been indeed substantial research on those topics, and the
solutions available to date already address conveniently the
intended purposes (15). Despite its relative importance, the
harvesting phase is also out of the scope of this review.
2. Reactor Design
The main parameter that affects reactor design is provision
for light penetration, which implies a high surface-to-volume
ratio; such penetration is crucial if one wants to improve the
photosynthetic efficiency, which is in turn a sine qua non
condition to reach high product and biomass productivities. In
order to achieve said high surface-to-volume ratio, several
shapes have been developed that met with success. These shapes
can be grouped in three basic types, viz., tubular, flat plate and
fermenter-type; the former two are specifically designed for
efficient harvest of sunlight, whereas the latter requires artificial
Tubular and flat plate reactors are undoubtedly the most
popular choices (12), considering that the light source required
is free and readily available. Those reactor types are based on
the same principle, viz., to guarantee the highest possible area-
to-volume ratio while ensuring reasonable working volume,
mixing pattern and carbon dioxide level. Both reactor configura-
tions may work with a separate unit for gas transfer, and several
layouts have been already tested with success (16-20). Such
systems comprise: a light-harvesting unit, which employs small
diameter tubing so as to provide a high area-to-volume ratio
that favors high photosynthetic activity, and a gas exchange unit,
in which CO2is supplied and biomass harvesting is processed.
The culture is circulated between those two units by a pump,
which needs to be carefully designed and operated in order to
prevent shear forces from disrupting cell integrity (17, 21-27).
Several reactor designs and corresponding productivities are
tabulated in Table 3.
2.1. Tubular Reactors. Most configurations of tubular
reactors (TR) are one of the following three types: (i) simple
airlift and bubble column, which is composed of vertical tubing
(in the form of a vertical tubular reactor) that is transparent so
as to allow for light penetration and where CO2is supplied via
bubbling; (ii) horizontal tubular reactor, which is composed of
horizontal transparent tubing, usually bearing gas transfer
systems attached to the connections; and (iii) helical tubular
reactor, which is composed of a flexible plastic tube coiled in
a circular framework. Another such reactor that deserves
particular attention is the R-shape tubular reactor, initially
conceived by Lee (28), because of its unique engineering design
that is characterized by a unidirectional, high liquid flow rate,
concomitant with a low air flow and an excellent angle relative
2.1.1. Vertical Tubular Reactors. The airlift and bubble
column reactors are examples of vertical tubular reactors (VTR),
regularly composed of polyethylene or glass tubes (Figure 1),
which are sufficiently transparent to allow good light penetration
but are manufactured with sufficiently common materials so as
to be nonexpensive. Air is bubbled at the bottom-a strategy
that provides good overall mixing, sufficient supply of CO2,
and efficient removal of O2. Polyethylene bags have frequently
been used, with advantage taken from their particularly low cost,
high transparency and good sterility at startup-due to the high
temperatures used during film extrusion (29, 30); 32 cm × 250
cm (ca. 25 L) bag reactors were employed by Cohen (31) for
cultivation of Porphyridium sp., which were able to reach cell
concentrations 3-fold those typically attained in open ponds.
Trotta (30) described a reactor composed of several 30 cm ×
180 cm (ca. 50 L) polyethylene bag reactors, with various
closing devices, and complemented with air and medium
supplies. Martine ´z-Jero ´nimo (32) also reported cultivation in
16.8 cm × 224 cm (ca. 40 L) bags to be practical, and to exhibit
an improved area-to-volume ratio. Tredici and Rodolfi (33)
improved this idea by using a culture chamber made of flexible
transparent plastic film contained in a rigid metal framework,
so as to form a vertical panel of reduced width. More recently,
Chae (34) reported a pilot-scale photo-bioreactor that uses
sunlight and flue gas, and consists of a vertical tubular part (kept
in the dark) and a horizontal tubular part (subject to sunlight).
Although cultivation of microalgae in the above systems is
simple and hence widely employed (including in hatcheries),
the corresponding technology is somehow primitive, with
obvious constraints derived from the high fragility and the low
versatility of the material in stake (21). Furthermore, scale-up
of these systems was initially thought to be easy, but ac-
cumulated experience (32) has indicated that increases in culture
volume decrease bag productivity.
Rigid VTR have also been frequently used. A 33.7 cm ×
250 cm (ca. 40 L) polyethylene reactor was discussed by Laing
(29), in which temperature was controlled by a refrigeration
fluid flown through its double wall and in which artificial light
was provided from the inside. Myamoto (35), James (36) and
Fukami (37) presented similar reactor configurations, but using
direct sunlight; their main advantages were low cost and ease
of operation. Unfortunately, scale-up is not straightforward;
furthermore, in order to provide enough culture volume, as well
as efficient gas transfer rate, the reactor diameter should be
relatively high when compared to flat plate or tubular loop
reactors, a requirement that in turn decreases the area-to-volume
ratio and consequently constrains photosynthetic efficiency.
Another major drawback is the large angle relative to the
direction of sunlight, which causes a high fraction of incident
Table 2. Main Design Features of Open and Closed Photobioreactors
featureopen systems closed systems
main criteria for species selection
water loss through evaporation
light utilization efficiency
most costly parameters
large (4-10 times higher than closed counterpart)
oxygen control, temperature control
aDependent on transparency of construction material.
Biotechnol. Prog., 2006, Vol. 22, No. 6
(34) Chae, S. R.; Hwang, E. J.; Shin, H. S. Single cell protein
production of Euglena gracilis and carbon dioxide fixation in an
innovative photo-bioreactor. Bioresour. Technol. 2006, 97, 322-
(35) Miyamoto, K.; Wable, O.; Benemann, J. R. Vertical tubular reactor
for microalgae cultivation. Biotechnol. Lett. 1988, 10, 703-708.
(36) James, C. M.; al-Khars, A. M. An intensive continuous culture
system using tubular photobioreactors for producing microalgae.
Aquaculture 1990, 87, 381-393.
(37) Fukami, K.; Nishimura, S.; Ogusa, M.; Asada, M.; Nishijima, T.
Continuous culture with deep seawater of a benthic food diatom
Nitzchia sp. Hydrobiology 1997, 358, 245-249.
(38) Lee, Y. K. Enclosed bioreactors for the mass cultivation of
photosynthetic microorganisms: the future trend. TIBTECH 1986,
(39) Richmond, A. The challenge confronting industrial microagricul-
ture: high photosynthetic efficiency in large-scale reactors. Hydro-
biology 1987, 151/152, 117-121.
(40) Torzillo, G.; Puspararaj, B.; Bocci, F.; Balloni, W.; Materassi,
R.; Florenzano, G. Production of Spirulina biomass in closed
photobioreactors. Biomass 1986, 11, 61-74.
(41) Zittelli, G. C.; Lavista, F.; Bastianini, A.; Rodolfi, L.; Vincenzini,
M.; Tredici, M. R. Production of eicosapentaenoic acid by Nan-
nochloropsis sp. cultures in outdoor tubular photobioreactors. J.
Biotechnol. 1999, 70, 299-312.
(42) Olaizola, M. Commercial production of astaxanthin from Heama-
tococcus pluVialis using 25,000 liter outdoor photobioreactors. J.
Appl. Phycol. 2000, 12, 499-506.
(43) Gudin, C.; Chaumont, D. Solar biotechnology study and develop-
ment of tubular solar receptors for controlled production of
photosynthetic cellular biomass for methane production and specific
exocellular biomass. Sol. Energy R&D Eur. Community, Ser. E 1984,
(44) Chaumont, D.; Thepenier, C.; Gudin, C.; Junjas, C. Scaling up a
tubular photobioreactor for continuous culture of Porphyridium
cruentum from laboratory to pilot plant (1981-1987). In Algal
Biotechnology; Stadler, T., Mollion, J., Verdus, M.-C., Karamanos,
Y., Morvan, H., Christiaen, D., Eds.; Elsevier: New York, 1988;
(45) Grima, E. M.; Pe ´rez, J. A. S.; Camacho, F. G.; Sa ´nchez, J. L. G.;
Ferna ´ndez, F. G. A.; Alonso, D. L. Outdoor cultivation of Isochrysis
galbana ALII-4 in a closed tubular photobioreactor. J. Biotechnol.
1994, 37, 159-166.
(46) Miro ´n, A. S.; Go ´mez, A. C.; Camacho, F. G.; Grima, E. M.; Chisti,
Y. Comparative evaluation of compact photobioreactors for large-
scale monoculture of microalgae. J. Biotechnol. 1999, 70, 249-
(47) Tredici, M. R.; Zittelli, G. C. Efficiency of sunlight utilization:
tubular versus flat photobioreactors. Biotechnol. Bioeng. 1998, 57,
(48) Tredici, M. R. Closed photobioreactors: basic and applied aspects.
In Proceedings of Marine Biotechnology: Basics and Applications,
Matalascan ˜as, Spain, 2003; p 1.
(49) Robinson L. F.; Morrison A. W.; Bamforth M. R. Improvements
relating to biosynthesis. European Patent 261,872, 1988.
(50) Chrismada, T.; Borowitzka, M. A. Effect of cell density and
irradiance on growth, proximate composition and eicosapentaenoic
acid production of Phaeodactylum tricornutm grown in a tubular
photobioreactor. J. Appl. Phycol. 1994, 6, 67-74.
(51) Morita, M.; Watanable, Y.; Saiki, H. Investigation of photobiore-
actor design for enhancing the photosynthetic productivity of
microalgae. Biotechnol. Bioeng. 2000, 69, 693-698.
(52) Morita, M.; Watanable, Y.; Okawa, T.; Saiki, H. Photosynthetic
productivity of conical helical tubular photobioreactors incorporating
Chlorella sp. under various culture medium flow conditions.
Biotechnol. Bioeng. 2001, 74, 135-144.
(53) Pirt, S. J.; Lee, Y. K.; Walach, M. R.; Pirt, M. W.; Balyuzi, H.
H. M.; Bazin, M. J. A tubular bioreactor for photosynthetic
production of biomass from carbon-dioxide-design and performance.
J. Chem. Technol. Biotechnol. B 1983, 33, 35-58.
(54) Richmond, A.; Cheng-Wu, Z. Optimization of a flat plate glass
reactor for mass production of Nannochloropsis sp. outdoors. J.
Biotechnol. 2001, 85, 259-269.
(55) Iqbal, M.; Grey, D.; Stepan-Sarkissian, F.; Fowler, M. W. A flat-
sided photobioreactor for continuous culturing microalgae. Aquac-
ulture Eng. 1993, 12, 183-190.
(56) Tredici, M. R.; Carlozzi, P.; Zittelli, G. C.; Materassi, R. A vertical
alveolar panel (VAP) for outdoor mass cultivation of microalgae
and cyanobacteria. Bioresour. Technol. 1991, 38, 153-159.
(57) Tredici, M. R.; Materassi, R. From open ponds to vertical alveolar
panels: the Italian experience in the development of reactors for
the mass cultivation of phototrophic microorganisms. J. Appl. Phycol.
1992, 4, 221-231.
(58) Tredici, M. R.; Zittelli, G. C.; Biagiolini, S.; Materassi, R. Novel
photobioreactor for the mass cultivation of Spirulina spp. Bull. Inst.
Oceanogr. 1993, 89-96.
(59) Tredici M. R. Bioreactors, photo. In Encyclopedia of Bioprocess
Technology: fermentation, biocatalysis and bioseparation; Flick-
inger, M.C., Drew, S.W., Eds.; Wiley: New York, 1999; Vol 1, pp
(60) Puspararaj, B.; Pelosi, E.; Tredici, M. R.; Pinzani, E.; Materassi,
R. An integrated culture system for outdoor production of microalgae
and cyanobacteria. J. Appl. Phycol. 1997, 9, 113-119.
(61) Pohl, P.; Kohlhase, M.; Martin, M. Photobioreactors for the axenic
mass cultivation of microalgae. In Algal Biotechnology; Stadler, T.,
Mollion, J., Verdus, M.-C., Karamanos, Y., Morvan, H., Christiaen,
D., Eds.; Elsevier: New York, 1988; pp 209-218.
(62) Ogbonna, J. C.; Soejima, T.; Tanaka, H. An integrated solar and
artificial light system for internal illumination of photobioreactors.
J. Biotechnol. 1999, 70, 289-297.
(63) Eriksen, N. T.; Geest, T.; Iversen, J. J. L. Phototrophic growth in
the lumostat: a photo-bioreactor with on-line optimization of light
intensity. J. Appl. Phycol. 1996, 8, 345-352.
(64) Grima, E. M.; Perez, J. A. S.; Camacho, F. G.; Sanchez, J. L. G.;
Alonso, D. L. n-3 PUFA productivity in chemostat cultures of
microalgae. Appl. Microbiol. Biotechnol. 1993, 38, 599-605.
(65) Grima, E. M.; Camacho, F. G.; Perez, J. A. S.; Sanchez, J. L. G.
Biochemical productivity and fatty acid profiles of Isochrysis galbana
Parke and Tetraselmis sp. as a function of incident light intensity.
Process Biochem. 1994, 29, 119-126.
(66) Grima, E. M.; Perez, J. A. S.; Camacho, F. G.; Sevilla, J. M. F.;
Fernandez, F. G. A. Effect of growth-rate on the eicosapentaenoic
acid and docosahexaenoic acid content of Isochrysis galbana in
chemostat culture. Appl. Microbiol. Biotechnol. 1994, 41, 23-27.
(67) Grima, E. M.; Camacho, E. G.; Perez, J. A. S.; Fernandez, E. G.
A.; Sevilla, J. M. F. Growth yield determination in a chemostat
culture of the marine microalga Isochrysis galbana. J. Appl. Phycol.
1996, 8, 529-534.
(68) Meireles, L. A.; Azevedo, J. L.; Cunha, J. P.; Malcata, F. X. On-
line determination of biomass in a microalga bioreactor using a novel
computerized flow injection analysis system. Biotechnol. Prog. 2002,
(69) Becker, E. W. Large-scale cultivation. In Microalgae: Biotech-
nology and Microbiology; Becker, E. W., Ed.; Cambridge University
Press: New York, 1994; pp 63-171.
(70) Richmond, A. Technological aspects of mass cultivation-a general
outline. In CRC Handbook of Microalgal Mass Culture; Richmond,
A., Ed.; CRC Press: Boca Raton, FL, 1986; pp 245-264.
(71) Goldman, J. C.; Dennett, M. R.; Riley, C. B. Inorganic carbon
sources and biomass regulation in intensive microalgal cultures.
Biotechnol. Bioeng. 1981, 23, 995-1014.
(72) Talbot, P.; Gortares, M. P.; Lencki, R. W.; de la Noue, J.
Absorption of CO2 in algal mass culture systems: a different
characterization approach. Biotechnol. Bioeng. 1991, 37, 834-842.
(73) Grima, E. M.; Sanchez-Perez, J. A.; Garcia-Camacho, F.; Robles-
Medina, A. Gas-liquid transfer of atmospheric CO2 in microalgal
cultures. Chem. Technol. Biotechnol. 1993, 56, 329-337.
(74) Ferreira, B. S.; Fernandes, H. L.; Reis, A.; Mateus, M. Mi-
croporous hollow fibres for carbon dioxide absorption: mass transfer
model fitting and the supplying of carbon dioxide to microalgal
cultures. Chem. Technol. Biotechnol. 1998, 71, 61-70.
(75) Carvalho, A. P.; Malcata, F. X. Transfer of carbon dioxide within
cultures of microalgae: plain bubbling versus hollow-fiber modules.
Biotechnol. Prog. 2001, 17, 265-272.
(76) Lee, Y.-K.; Hing, H.-K. Supplying CO2to photosynthetic algal
cultures by diffusion through gas-permeable membranes. Appl.
Microbiol. Biotechnol. 1989, 31, 298-301.
Biotechnol. Prog., 2006, Vol. 22, No. 6
(77) Aunins, J. G.; Henzler, H. Aeration in cell culture bioreactors. In
Biotechnology; Stephanopoulos, G., Ed.; Wiley-VCH: Weinheim,
1993; Vol. 3 (Bioprocessing), p 223.
(78) Gallagher, S. L.; Tharakan, J. T.; Chau, P. C. An intercalated-
spiral wound hollow fiber bioreactor for the culture of mammalian
cells. Biotechnol. Tech. 1987, 1, 91-96.
(79) Chen, F.; Johns, M. R. A strategy for high cell density culture of
heterotrophic microalgae with inhibitory substrates. J. Appl. Phycol.
1995, 7, 43-46.
(80) Marsot, P.; Cembella, A. D.; Mouhri, K. Croissance de la biomasse
azote ´e du Phaeodactylum tricornutum (Bacillariophyceae) en culture
discontinue dialysante et non-dialysante. Can. J. Microbiol. 1992,
(81) Markov, S. A.; Bazin, M. J.; Hall, D. O. Hydrogen photoproduc-
tion and carbon dioxide uptake by immobilized Anabaena Variabilis
in a hollow-fiber photobioreactor. Enzyme Microb. Technol. 1995,
(82) Pirt, S. J.; Panikov, N.; Lee, Y.-K. The miniloop: a small-scale
air-lift microbial culture vessel and photobiological reactor. J. Chem.
Technol. Biotechnol. 1979, 29, 437-441.
(83) Pirt, S. J. Microbial photosynthesis in the harnessing of solar-
energy. J. Chem. Technol. Biotechnol. 1982, 32, 198-202.
(84) Laws, E. A.; Terry, K. L.; Wickman, J.; Chalup, M. S. A simple
algal production system designed to utilize the flashing light effect.
Biotechnol. Bioeng. 1983, 25, 2319-2335.
(85) Laws, E. A.; Taguchi, S.; Harata, J.; Pang, L. High algal
production rates achieved in a shallow outdoor flume. Biotechnol.
Bioeng. 1986, 28, 191-197.
(86) Laws, E. A.; Taguchi, S.; Harata, J.; Pang, L. Optimization of
microalgal production in a shallow outdoor flume. Biotechnol.
Bioeng. 1988, 32, 140-147.
(87) Lee, C.-G.; Palsson, B. Ø. High-density algal photobioreactors
using light-emitting diodes. Biotechnol. Bioeng. 1994, 44, 1161-
(88) Muller-Feuga, A.; Gue ´des, R. L.; Herve ´, A.; Durand, P. Com-
parison of artificial light photobioreactors and other production
systems using Porphyridium cruentum. J. Appl. Phycol. 1998, 10,
(89) Fuentes, M. M. R.; Sa ´nchez, J. L. G.; Sevilla, J. M. F.; Ferna ´ndez,
F. G. A.; Pe ´rez, J. A. S.; Grima, E. M. Outdoor continuous culture
of Phorphyridium cruentum in a tubular photobioreactor: quantitative
analysis of the daily cyclic variation of culture parameters. J.
Biotechnol. 1999, 70, 271-288.
(90) Ferna ´ndez, A. F. G.; Sevilla, J. M. F.; Pe ´rez, J. A. S.; Molina-
Grima, E.; Chisti, Y. Airlift-driven external-loop tubular photobiore-
actors for outdoor production of microalgae: assessment of design
and performance. Chem. Eng. Sci. 2001, 56, 2721-2732.
(91) Marsot, P.; Fournier, R.; Blais, C. Culture a ` dialyse: emploi de
fibres creuses dialysantes pour la culture massive de phytoplankton.
Can. J. Fish. Aquat. Sci. 1981, 38, 905-911.
(92) Camacho, F. G.; Go ´mez, A. C.; Ferna ´ndez, F. G. A.; Sevilla, J.
F.; Grima, E. M. Use of concentric-tube airlift photobioreactors for
microalgal outdoor mass cultures. Enzyme Microb. Technol. 1999,
(93) Heussler, P.; Castillo, S. J.; Merino, M. F.; Vasquez, V. V.
Improvements in pond construction and CO2 supply for the mass
production of microalgae. Arch. Hydrobiol. Beih. Ergebn. Limnol.
1978, 11, 254-258.
(94) Sa ´nchez, J. L. G.; Berenguel, M.; Rodrı ´guez, F.; Sevilla, J. M.
F.; Alias, C. B.; Ferna ´ndez, F. G. A. Minimization of carbon losses
in pilot-scale outdoor photobioreactors by model-based predictive
control. Biotechnol. Bioeng. 2003, 84, 533-543.
(95) Berenguel, M.; Rodrı ´guez, F.; Acie ´n, F. G.; Garcı ´a, J. L. Model
predictive control of pH in tubular photobioreactors. J. Process
Control 2004, 14, 377-387.
(96) Oswald, W. J. Large-scale algal culture systems (engineering
aspects). In Micro-Algal Biotechnology; Borowitzka, M. A., Borow-
itzka, L. J., Eds.; Cambridge University Press: New York, 1988;
(97) Camacho, F. G.; Go ´mez, A. C.; Sobczuk, T. M.; Grima, E. M.
Effects of mechanical and hydrodynamic stress in agitated, sparged
cultures of Porphyridium cruentum. Process Biochem. 2000, 35,
(98) Singh, G. Reactor design for plant cell culture of food ingredients
and additives. Food Technol. 1997, 51, 62-66.
(99) Degen, J.; Uebele, A.; Retze, A.; Schmid-Staiger, U.; Tro ¨sch, W.
A novel airlift photobioreactor with baffles for improved light
utilization through the flashing light effect. J. Biotechnol. 2001, 92,
(100) Laws, E. A.; Taguchi, S.; Hirata, J.; Pang, L. Continued studies
of high algal productivities in a shallow flume. Biomass 1987, 11,
(101) Pirt, S. J.; Lee, Y. K.; Richmond, A.; Watts-Pirt, M. The
photosynthetic efficiency of Chlorella biomass growth with reference
to solar energy utilization. J. Chem. Technol. Biotechnol. 1980, 30,
(102) Sandnes, J. M.; Ringstad, T.; Wenner, D.; Heyerdahl, P. H.;
Ka ¨llqvist, T.; Gisler¢d, H. R. Real-time monitoring and automatic
density control of large-scale microalgal cultures using near infrared
(NIR) optical density sensors. J. Biotechnol. 2006, 122, 209-215.
(103) Dubinsky, Z.; Matsukawa, R.; Karube, I. Photobiological aspects
of algal mass culture. J. Mar. Biotechnol. 1985, 2, 61-65.
(104) Evers, E. G. A model for light-limited continuous cultures-
growth, shading, and maintenance. Biotechnol. Bioeng. 1991, 38,
(105) You, T.; Barnett, S. M. Effect of light quality on production of
extracellular polysaccharides and growth rate of Porphyridium
cruentum. Biochem. Eng. J. 2004, 19, 251-258.
(106) Simmer, J.; Tichy, V.; Doucha, J. What kind of lamp for the
cultivation of algae? J. Appl. Phycol. 1994, 6, 309-313.
(107) Li, J.; Xu, N. S.; Su, W. W. Online estimation of stirred-tank
microalgal photobioreactor cultures based on dissolved oxygen
measurement. Biochem. Eng. J. 2003, 14, 51-65.
(108) Hejazi, M. A.; Wijffels, R. H. Milking of microalgae. TIBTECH
2004, 22, 189-194.
Received March 7, 2006. Accepted August 3, 2006.
Biotechnol. Prog., 2006, Vol. 22, No. 6