3516

Ind. Eng. Chem. Res. 2010, 49, 35163526

Photobioreactor Design for Commercial Biofuel Production from Microalgae

Aditya M. Kunjapur* and R. Bruce Eldridge
Process Science and Technology Center, UniVersity of Texas, Austin, Texas 78712

This review paper describes systems used to cultivate microalgae for biofuel production. It addresses general
design considerations pertaining to reactors that use natural light and photosynthetic growth mechanisms,
with an emphasis on large-scale reactors. Important design aspects include lighting, mixing, water consumption,
CO2 consumption, O2 removal, nutrient supply, temperature, and pH. Though open pond reactors are the
most affordable option, they provide insufficient control of nearly all growth conditions. In contrast, a variety
of closed reactors offer substantial control, but few feature the likelihood for levels of productivity that offset
their high cost. One of the greatest challenges of closed photobioreactor design is how to increase reactor
size in order to benefit from economy of scale and produce meaningful quantities of biofuel. This paper also
highlights the concept of combining open and closed systems and concludes with a discussion regarding a
possible optimal reactor configuration.
1. Introduction
Many strains of photosynthetic microalgae produce lipids that
can be converted into various types of biofuel, such as biodiesel
or jet fuel.1 The potential of using photosynthetic microalgae
to produce biofuel is of particular interest at this time. Americas
deepening dependence on foreign sources of petroleum-based
fuel jeopardizes the national economy and national security.
Increasing CO2 emissions may promote climate change. Rising
demand for energy from developing nations threatens the
availability of sustainable energy for future generations. Commercial biofuel production using algae could mitigate all of these
issues: algae can be cultivated in the United States, algae
consume CO2 during photosynthesis (ideally resulting in a
carbon neutral fuel), and increased biofuel production would
supplement nonrenewable energy sources.2 Microalgae are
already produced commercially for a variety of other applications, which include human nutrition, animal feed, aquaculture,
pigments, and cosmetics.3
Algae can also be cultivated using photoautotrophic (or
photosynthetic), heterotrophic, or mixotrophic growth techniques. Heterotrophic growth is based on the cellular consumption of organic carbon instead of light, and mixtrophic growth
uses the combination of these energy sources. Although some
authors, such as Lee,4 have discussed advantages of heterotrophic and mixotrophic growth, these methods are not
described here. As Chisti noted, heterotrophic growth mechanisms are not as efficient as photosynthetic growth mechanisms
because the carbon source used to feed the algae was ultimately
derived from another plant by photosynthesis. In addition, the
carbon source may compete with food sources for human
consumption.5 Henceforth, the generic term algae will be used
to describe photosynthetic microalgae and the term photobioreactor will be used to describe a system that uses light to
grow algae via only the photosynthetic mode of cultivation.
Algae can be grown with exposure to natural or artificial light.
Artificial lighting techniques have provided insight into how
algae respond to varying light conditions, and these insights
are briefly discussed in the design considerations section of this
paper. However, this paper does not focus on growth systems
that rely on artificial lighting because of energy efficiency
* To whom correspondence should be addressed. Tel.: (713)-7025587. Fax: (512)-471-1720. E-mail: aditya.kunjapur@mail.utexas.edu.

considerations. The energy used to power the artificial lighting

was once derived from sunlight. This energy necessarily
experienced losses along every stage of its transformation to
and from electrical energy, and these losses are not incurred by
natural light.
The two major classes of algae growth systems are open
ponds and closed reactors. However, prior to the analysis of
specific photobioreactor configurations, general design considerations are presented so that reactor designs can be evaluated
and compared effectively. During the description of these
factors, individual reactor types may be mentioned in order to
better explain the design aspect. Following the discussion of
design considerations, these reactor types will be discussed in
detail.
2. Photobioreactor Design Considerations
Numerous aspects influence the growth and lipid content of
algae. The reaction driving the initial conversion of sunlight
into stored energy is photosynthesis. Therefore, all of the
components involved in photosynthesis contribute to growth.
The factors discussed in this paper are lighting, mixing, water,
CO2, O2 removal, nutrient supply, temperature, and pH. The
list is not comprehensive, and the final topic within this section
addresses other critical issues, such as genetic engineering and
reactor maintenance. It is important to note that in each category
the precise conditions for optimal growth depend on the strain
of algae selected for cultivation.
2.1. Lighting. An optimal reactor enhances light intensity/
penetration, as well as the wavelength of light and the frequency
of cellular exposure to light.
The level of light intensity is critical because at a certain
level algae experience light saturation and dissipate the excess
energy as heat.6 Light saturation can be mitigated by the spatial
dilution of light, which is the distribution of solar radiation on
a greater photosynthetic surface area. Spatial dilution of light
also reduces mutual shading of cells in the culture, which results
in higher growth rates and lower content of accessory pigments.7
Thus, a design principle for photobioreactor designs is to
maximize the surface area to volume ratio, which can be used
for comparison between reactors. Designs resulting in a ratio
value of 400 m2/m3 were state-of-the-art in the year 2008.8
Beyond the surface area and volume, the unique geometry of a
reactor influences the light distribution. In a tubular reactor, for

10.1021/ie901459u 2010 American Chemical Society

Published on Web 03/23/2010

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3517

Figure 1. Rectangular airlift reactor with separate light collection. (Reprinted with kind permission from ref 9. Copyright 2003 John Wiley and Sons.)

example, the light gradient is primarily determined by the

diameter of the tube and the biomass density in the medium.9
The biomass density affects both the light intensity and the light
penetration. Optimal cell density is specific to each strain and
needs to be maintained in order for light intensity and light
penetration to remain at optimal levels.10 Park and Lee described
an important operating parameter known as the critical cell
density, which is the maximum cell concentration without
mutual shading in algal cultures.11
The wavelength of light used to cultivate algae is also a design
factor because some experiments have shown that cultures grow
differently when exposed to different colors of light. However,
optimizing this aspect in systems illuminated by natural light
is much more challenging than in systems illuminated by
artificial light, where the wavelength of light shone can be
selected. Unfortunately, more than 50% of the incident solar
radiation from natural light cannot be used by photosynthesis.12
When natural light is the growth rate limiting factor, the upper
limit in the light conversion efficiency of a large-scale culture
may result in a maximum potential yield of 30-40 g/m2 d.13
Matthijs et al. found that red light matched perfectly with the
requirements of the first excited state of pigments present in
the light-harvesting antenna complexes (LHC) central to photosynthesis in green algae. He also noted that the addition of
blue light to the red LED light did not change the growth
properties.14
Light and dark cycles strongly influence the growth of algae.
In both open ponds and outdoor closed reactors, natural light is
subject to changes in time of day, weather, season, and
geography.12 Unfortunately, all reactors using natural light are
subject to the absence of light during nighttime. According to
Chisti, biomass losses might reach as high as 25% during the
night, depending on the light intensity during the day, the
temperature during the day, and the temperature at night.5
Janssen et al. noted that the length of the light/dark cycles
experienced by algae influenced photosynthetic efficiency.
Cycles on the order of milliseconds increased the photosynthetic
efficiency (PE) of Dunaliella tertiolecta, but cycles on the order
of seconds lowered the PE compared to continuous lighting.15
The time length of the dark reactions in photosynthesis may
serve as the rate-limiting step for photosynthesis and growth in

general.16 The optimal dark period depends on the photon flux

density of the previous light period and the fluid residence time
in zones of different irradiance.17 Formulas that describe light
and dark frequency values in various types of closed reactors
can be found in the literature.9 Such formulas and other
quantitative models for light analysis are not included in order
to maintain brevity. Likewise, predictive equations that model
mass transfer or other design parameters are excluded here but
can be found in referenced papers.
The combination of factors such as the length of the light
and dark cycles and the light intensity result in the overall light
regime in a photobioreactor. Light regime strongly influences
photoacclimation, which describes the physiological responses
of cells to rapid changes in light intensity. An example of a
common response to light intensity alteration is a change in
chlorophyll pigment content. However, a sudden surge of light
can be fatal for many species of algae.18 Thus, it is important
to consider light regime and photoacclimation when designing
a reactor, particularly in order to maximize the photosynthetic
efficiency.
Because light is the exclusive source of energy in the
photosynthetic mode of cultivation, an important calculation can
be performed if solar radiation per area data is available for the
location of cultivation. On the basis of this data and other values
such as photosynthetic efficiency, the maximum theoretical oil
yield per area can be determined. The maximum theoretical oil
yield per area is especially useful for comparison between actual
and ideal reactor performance when the oil yield and area of a
reactor in operation are known. However, reactor area does not
directly contribute to oil yield when light is collected externally
from the site of algal cultivation, which some authors have
advocated.9 Figure 1 depicts a rectangular reactor that collects
light externally. Experiments conducted by Feuermann et al.19
and Zijffers et al.20 suggested that natural light can efficiently
be collected at a separate location and delivered to a photobioreactor using fiber optic cables. Zijffers et al. employed the
light guide technology in a flat-plate reactor known as the Green
Solar Collector.20 The schematic of this reactor is shown in
Figure 2. In such a design, light must enter the light guides and
experience total internal reflection. It must also refract out of
the guide when surrounded by the algal suspension. In order to

3518

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 2. Cross-section of the photobioreactor (Green Solar Collector).

The numbers indicate the following: 1: linear Fresnel lens, 2: light guide,
3: flat-panel reactor compartment, 4: perforated tube for aeration, 5: water
jacket. The letters indicate the following: A: legs holding the lens, X: axis
of rotation of the lens, Y: axis of rotation of the legs A.20 (Reprinted
with kind permission from ref 20. Copyright 2008 Springer Science +
Business Media.)

achieve this, a light guide surrounded by air and accepting all

possible angles on the top surface must have a refractive index
higher than 1.415. Polymethylmethacrylate (PMMA) is recommended as an ideal material for this application. The light guide
should be flat at the top surface of the entrance and triangular
at the bottom surface within the reactor in order to ensure that
maximal light enters and leaves the guide respectively. Light
intensity is then determined by the ratio of the surface of the
lens to the surface of the light guide in the reactor.20
Light-emitting diodes (LEDs) have been used frequently in
the literature as the sole light source for many photobioreactors.
Because much of the LED literature has provided insight into
light effects in general, some results of algae grown using
artificial lighting systems will be discussed. Matthijs et al. found
that the use of flashing LEDs in indoor algal culture yielded a
major gain in energy economy compared to luminescent light
sources.14 Gordon and Polle16 advocated a lighting technique
using LEDs that pulsed on the order of tens to hundreds of
microseconds while also increasing the instantaneous photonic
flux. The authors noted that though flashing of light might not
always improve productivity, optimal pulsing could dramatically
improve productivity. The use of LEDs to produce a flashing
light will increase operating costs, but the authors claimed that
the costs could be offset by greater increases in productivity.16
Although much of the literature supports the flashing light effect,
some authors have cautioned against accepting it. Pulz and
Scheibenbogen12 cited some experiments that may leave the
effect of flashing light inconclusive. However, it is possible that
in these experiments the light was not flashing at a frequency
within the effective range.
2.2. Mixing. The level of mixing in a reactor strongly
contributes to the growth of algae. In fact, Suh and Lee stated
that when environmental conditions do not limit growth rates,
mixing is the most influential factor contributing to algae growth
rates.21 Mixing affects growth in two primary ways. Mixing
improves productivity by increasing the frequency of cell
exposure to light and dark volumes of the reactor and by
increasing mass transfer between the nutrients and cells.22
Mixing attempts to distribute radiation evenly to all cells in
the culture and reduce diffusion barriers around the cells.10

Figure 3. A. Dual sparging photobioreactor with CO2 additions separated

from flow of air for mixing: a, culture outlet; b, air outlet through condenser;
c, medium inlet; d, medium reservoir; e, glass cylinder; f, pH electrode; g,
automatic titration device; h, solenoid valve; i, perforated membrane sparger;
j, air pump; k, orifice sparger; l, light tubes; m, mirror; n, air filter. B. Bottom
part of photobioreactor operated as ordinary bubble column with CO2 mixed
with flow of air formixing. Annotations as in A. C. Bottom part of
photobioreactor operated in stirred bioreactor configuration. CO2 is mixed
with flow of air for mixing: o, impeller; other annotations as in A.25
(Reprinted with kind permission from ref 25. Copyright 1998 Springer
Science + Business Media.)

Mixing and lighting are closely related, as mixing is often

responsible for inducing the light and dark cycles beneficial to
algae growth. Similarly, mixing offers little benefit if lighting
is poor. The significance of this relationship was verified by
Richmond, who described that the rate of mixing did not affect
productivity when cultures were exposed to low light and low
cell density.10 Ugwu et al. demonstrated that the installation of
static mixers in tubular reactors succeeded in increasing light
utilization and biomass yields when the reactor was scaled up
by increasing the tube diameter.23
A review by Ugwu et al.24 listed some of the factors that
influence the overall mass transfer coefficient (kLa) in a reactor,
which is a key comparison parameter between reactors. The
coefficient depends on the agitation rate, type of sparger,
surfactants/antifoam agents, and temperature. The use of fine
spargers could result in the formation of large bubbles, which
leads to poor mass transfer because of the reduced contact area
between liquid and gas. The size of the bubbles and the gas
bubble velocity are dependent on the liquid flow rate. Bubble
size may be reduced with the installation of static mixers or
baffles.24
Eriksen et al. described a closed reactor with a dual orifice
and perforated membrane sparger system which separates the
CO2 supply from the air supply used for mixing.25 Figure 3
displays the experimental apparatus. This separation resulted
in five times the magnitude of transfer of CO2 from gas phase
to liquid phase relative to conventional sparging. Eriksen et al.
described many advantages achieved by combining two types
of spargers in the dual sparging bioreactor. First, the small
size of the bubbles from the membrane sparger increased the
CO2 mass transfer coefficient. Second, the separate addition
of CO2 also improved mass transfer by increasing the gradient
of CO2 partial pressure between the liquid and gas phase. Third,
the large air bubbles generated turbulence that reduced wall
growth. The dual sparging bioreactor also displayed a high
degree of reliability since there were no equipment failures and
limited maintenance was required.25 According to a review by

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3519

Janssen et al., sparger design does not effectively increase

mixing in bubble-column reactors, but spargers can improve
air-lift reactors if applied to the annulus rather than the inner
cylinder.
The level of mixing has to be optimized carefully because
high levels of mixing will result in cell death from shear.
Barbosa et al. found that bubble formation is the main cause
for cell death in gas-sparged reactors, and gas entrance velocity
could be used as a measure for estimating cell damage in these
reactors. Surprisingly, bubble bursting and bubble rising were
proven not to contribute to cell death. Barbosa et al. recommended keeping the gas velocity at the sparger lower than the
critical value by increasing the number of nozzles and/or
increasing the nozzle diameter in order to minimize shear-related
cell death.26
2.3. Water Consumption. A noteworthy benefit of producing fuel from many strains of algae, as opposed to conventional
crops, is that the cultivation does not have to require freshwater.
Water supplies, particularly freshwater supplies, are under
pressure in many parts of the globe, and greater biofuel production places an additional burden on those supplies.27 Thus, water
consumption is a key comparison parameter among reactor
options.
Wogan28 mentioned that algae can grow in a much wider
range of water sources than other terrestrial crops. Studies have
shown that algae can grow in fresh drinking water, saline or
brackish water, and even wastewater effluent.29 Strains of
microalgae are generally divided into two categories based on
whether they grow optimally in freshwater or saltwater. The
level of salinity influences the overall productivity as well as
individual production rates of lipids and carbohydrates in each
strain of algae.30 A few examples of strains and their optimum
salinity values are included to provide a sense of how saline
the growth media can be. Abu-Rezq et al. found optimum
production conditions for species of Nannochloropsis, Tetraselmis, and Isochrysis. The optimum salinity range was 20-40
ppt for Nannochloropsis, 20-35 ppt for Tetraselmis, and 25-35
ppt for Isochrysis.31
As mentioned earlier, wastewater can be used to cultivate
algae. Using wastewater for this application provides two
significant benefits: algae receive an inexpensive medium rich
in required nutrients and the wastewater is further treated in
the process.28 Wastewater effluent generally contains high
concentrations of nitrogen and phosphorus, and unwanted algae
growth and eutrophication occur when other water bodies
receive the effluent. The nitrogen and phosphorus concentrations
can instead be minimized by passing the wastewater through
an algal reactor.32
A major disadvantage of open ponds is the loss of water to
the atmosphere by evaporation.8 When water evaporates from
the reactor, the concentrations of all species present increases,
and this can be a particular problem with saltwater ponds as
the salinity could rise above tolerable values.
2.4. CO2 Consumption. In addition to light and water,
carbon dioxide is necessary for photosynthesis to occur. However, an excess of CO2 can also be detrimental to photosynthesis
and cell growth. Lee and Tay33 found that Chlorella cells
exposed to high CO2 partial pressures (pCO2) experienced
declining growth rates. CO2 can be supplied via diffusion
through a gas permeable membrane in order to provide sufficient
CO2 to the entire culture while preventing CO2 inhibition at
high gaseous pCO2.33 CO2 concentrations from 1% to 5% (by
volume) often lead to maximum growth. Despite this, laboratories routinely aerate algal cultures with 5-15% CO2, or even

Figure 4. Tubular reactor equipped with airlift system. (Reprinted with

kind permission from ref 36. Copyright 2001 Elsevier.)

pure CO2.21 In the review by Schenk et al.,8 it was stated that

a pCO2 value of at least 0.15 kPa is required to prevent kinetic
CO2 uptake limitation. In addition, a ratio of about 1.7-1.8 g
CO2/g dry biomass is required.5,8
Flue gas is a desirable source of CO2 because it reduces
greenhouse gas emissions as well as the cost of algal biofuel
production.34 Flue gas from typical coal-fired power plants
contain up to 13% CO2.5 Doucha et al.34 studied the performance
of a closed reactor utilizing flue gas as a source of CO2 versus
a reactor utilizing pure CO2. An infrared-analyzer that measures
the bypass concentration of CO2 in the gas phase can be used
to regulate the flow rate of flue gas. A pCO2 higher than 0.1 kPa
was maintained at the downstream end of the reactor in order
to prevent growth limitation by CO2. Surprisingly, productivities
and photosynthetic efficiencies were very similar under conditions of pure CO2 versus flue gas. Because CO2 concentration
in flue gas was relatively low, the efficiency of CO2 mass
transfer was lower for flue gas than it was for pure CO2. In
addition, the authors found that the presence of NOx and CO in
flue gas did not inhibit the growth of microalgae.34
The cost of CO2 has to be considered when evaluating the
economics of biofuel production from microalgae. A review by
Carvalho et al.35 suggested that because supplying CO2 continuously is expensive, it may be necessary to supply it discontinuously.
The authors recommended using hollow-fiber membranes, which
may improve mass transfer and reduce costs.35
2.5. O2 Removal. A high presence of oxygen around algae
cells is undesirable. The combination of intense sunlight and
high oxygen concentration results in photooxidative damage to
algal cells.5 As a general guideline, oxygen concentrations
should be maintained below 400% of air saturation value.5
Because oxygen does not build up substantially in open ponds,
this is one aspect in which open ponds perform better than closed
reactors.
Because of the constraint on the concentration of dissolved
oxygen, tube length is limited in horizontal tubular reactors.
This restriction makes it very difficult for tubular reactors to be
scaled-up. In a tubular reactor designed by Molina et al., the
algae culture regularly returned to an airlift zone where the
accumulated oxygen from photosynthesis was stripped by air.
A gas-liquid separator in the upper part of the airlift column
prevented gas bubbles from recirculating into the horizontal loop
of the airlift reactor.36 Figure 4 is an illustration of the
photobioreactor configuration used.

3520

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

The time taken by the fluid to travel the length of the degasser
must at least equal the time required by the oxygen bubbles to
rise out.36 If practical, the capture and sale of this oxygen
stripped from the reactors may be an opportunity to reduce the
cost of biofuel production.
2.6. Nutrient Supply. In order to grow, algae require more
than the reactants in the photosynthesis reaction. Two major
nutrients are nitrogen and phosphorus, which both play a role
in controlling growth rates and lipid production. Other essential
nutrients are carbon, hydrogen, oxygen, sulfur, calcium, magnesium, sodium, potassium, and chlorine. Nutrients needed in
minute quantities include iron, boron, manganese, copper, molybdenum, vanadium, cobalt, nickel, silicon, and selenium.21
An analysis of a common medium known as N-8 revealed
the deficiency of iron, magnesium, sulfur, and nitrogen at high
cell concentrations. Additional experiments showed that the
separate addition of each of the four elements did not improve
culture performance, but that balanced supplementation resulted
in improved performance. The experimenters therefore asserted
that balancing the nutrients based on the elemental composition
of the biomass should be the basis for effective medium
design.37 However, Chisti noted that some nutrients need to be
present in excess. For example, phosphorus must be supplied
in excess because the phosphates react with metal ions.5
Applying stress in the form of limited nutrients (especially
N or P) can increase lipid percentages within the biomass.
However, this stress application also curtails the growth rate
and thus may lower overall lipid production. The trade-off
between productivity and lipid content stems from the high
metabolic cost of lipid biosynthesis. Rodolfi et al. described
three different situations of nutrient supply: nutrient-sufficient,
nutrient-limited, and nutrient-deficient. The first case should be
evident, but the difference between the latter two cases may be
subtle. Nutrient limitation occurs when cells are grown in an
environment of a constant, but insufficient, supply of a limiting
nutrient, to which the cells generally adapt. Nutrient deficiency
is characterized by the cultures reliance on endogenous reserves
because there are no nutrients in the environment. Rodolfi et
al. compared the growth of a few robust strains under all three
conditions, with the nutrient-deficient scenario applied to
microalgae previously grown in a nutrient-sufficient environment. The authors found that the genus Nannochloropsis was
an exception to the rule and had both enhanced lipid content
and lipid productivity in an N-deficient environment.38
2.7. Temperature. Temperatures experienced by algae grown
outdoors can vary as much as the extreme outdoor temperatures
characteristic to the geographic region of cultivation. Although
algae may be able to grow at a variety of temperatures, optimal
growth is limited to a narrow range specific to each strain. For
example, Abu-Rezq et al. found that the optimum temperature
range for Nannochloropsis, Tetraselmis, and Isochrysis was
19-21, 19-21, and 24-26 C, respectively.31
Seasonal and even daily fluctuations in temperature can
interfere with algae production. Temperatures can reach as high
as 30 C higher than ambient temperature in a closed photobioreactor without temperature control equipment.21 Evaporate
cooling or shading techniques are employed frequently to inhibit
temperatures of that magnitude. In addition, a lower temperature
appears to reduce the loss of biomass due to respiration during
the night.5
2.8. pH. Each strain of algae also has a narrow optimal range
of pH. The pH of the medium is linked to the concentration of
CO2. Suh and Lee21 mentioned that pH increases steadily in
the medium as CO2 is consumed during flow downstream in a

reactor. The pH affects the liquid chemistry of polar compounds

and the availability of nutrients such as iron, organic acids, and
even CO2.39,40 Because pH is so influential, Suh and Lee stated
that commercial pH controllers must be used in reactors to
optimize growth.21
2.9. Other Considerations. Tredici and Zittelli asserted that
a sustainable production process, which relies on a homogeneous
and stable environment for microalgae cells, is more important
in industrial applications than high yields.7 When evaluating a
proposed reactor configuration, it is important to consider the
production process as a whole. For instance, a major advantage
of high cellular lipid content is the improved efficiency of oil
extraction and other downstream processing.38 The ease of
integration of the reactor design with downstream processes is
another key comparison parameter to reflect upon.
Techniques rooted in biology, rather than reactor design, can
have a dramatic impact on the economics of algae production.
Chisti suggested that genetic engineering may have the greatest
likelihood of improving the economics of biofuel production
from microalgae.5 Genetic engineering could enhance fuel
production in a variety of ways, including improving photosynthetic efficiency, increasing biomass productivity, increasing
cellular lipid content, and improving temperature tolerance of
algae to reduce cooling expenses.41 In addition, genetic engineering could increase algal cells tolerance to light saturation,
photoinhibition, and photooxidation.5
Rodolfi et al. mentioned that a strain should be highly
productive in outdoor culture and adaptable to the varying
conditions of an outdoor environment. The authors asserted that
there may be many suitable strains of microalgae among the
thousands of natural strains available, and that for immediate
purposes, there is no need to genetically modify microalgae.
Genetic engineering can improve productivity and economics,
but it will require long-term research and funding, as well as
overcoming regulations against the release of genetically
modified organisms.38
In addition, Pulz and Gross presented several reasons to be
wary of genetic engineering. First, the authors claimed that
increases in lipid content and other valuable cellular components
are inherently constrained by cellular metabolism. Second,
genetically modified algae may have a variety of detrimental
effects on the environment. Finally, Pulz and Gross argued that
genetically modified algae are not as fit as natural strains and
thus unlikely to overcome competition without the aid of other
agents.42
Nevertheless, genetic engineering has tremendous potential
and has already achieved successes in the laboratory. For
example, Mussgnug et al.6 described experiments that altered
the light harvesting complexes (LHCs), which were mentioned
earlier in the Lighting section. The purpose of the LHCs is to
capture solar energy and control the flow of the excitation energy
to the photosynthetic reaction centers. They also facilitate the
dissipation of light energy as heat or fluorescence when
irradiation exceeds photosynthetic capacity. This second trait
is especially undesirable in algal bioreactors because it reduces
efficiency. To resolve this issue, the authors used RNAi
technology to create a mutant of C. reinhardtii (referred to as
Stm3LR3) that significantly down regulated the amount of LHCI
and LHCII complexes. Their experiments, which were successful, also showed that the reduction was permanent, something
that had not previously been reported in literature. The strain
of Stm3LR3 resulted in a decrease in dissipation of captured
light energy, an increase in photosynthetic quantum yield, and
reduced sensitivity of the system to photoinhibition. Further-

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3521

Figure 5. Schematic of a raceway pond. (Reprinted with kind permission

from ref 5. Copyright 2007 Elsevier.)

more, despite the reductions in the LHC proteins, the remaining

pigments were sufficient to drive photosynthesis efficiently and
promoted increased cell growth and replication compared to the
parent strain at elevated light conditions. The use of down
regulated LHC strains of algae is expected to result in a myriad
of benefits for algae production: reduction in energy losses,
increase in overall photosynthetic efficiency, improvement in
light penetration, increase in the optimally illuminated cell
proportion, and an increase in overall productivity.6
Geography also plays a role in reactor selection and assessing
the feasibility of biofuel production from algae, since certain
regions of the world are better suited than others. In the United
States, the southwest and several southern states are good
locations to cultivate algae. As Wogan28 observed, Texas is wellsuited for commercial algae production. The state is abundant
in CO2 production, saline aquifers, and sunlight. Texas also
contains many resources unique to the energy and refining
industries. Borowitzka argued that geographic factors also
influence the selection of a reactor, including the cost of land
and climate at the reactor site.43 For example, Betatene Ltd.,
which produces D. salina in Australia, uses large open ponds
up to 250 ha in size. For their application, even mixing devices
are unnecessary. Open ponds provide optimal growth in this
case because land costs are low, seawater is free, and the climate
allows production throughout the year.44 However, large open
ponds have often proven unsuccessful in other regions.
3. Open Ponds
The most common growth systems used for commercial
purposes are open pond reactors. According to Borowitzka,44
the four most common types of commercial cultivation systems
are large open ponds, circular ponds with rotating components
for mixing, raceway ponds, and large bags. Open ponds are
frequently designed like raceway ponds, which feature paddlewheels and baffles to promote mixing. Figures 5 and 6 illustrate
examples of raceway ponds in schematic and pilot-scale forms.
Optimal pond depth is a trade-off between keeping the pond
shallow enough to provide sufficient light to the culture but deep
enough to enhance mixing and remain unaffected by evaporation.44 Open ponds, along with most closed photobioreactors,
must be connected to some form of a harvesting system, which
collects the algae cells for biomass concentration, cell lysis, and
oil extraction.5
From 1980 to 1996, the U.S. Department of Energy conducted
a research effort within their Biofuels Program, known as the
Aquatic Species Program (ASP). The ASP research focused on

Figure 6. Seambiotic pilot-scale raceway ponds. (Reprinted with kind

permission from ref 59. Copyright 2008 Seambiotic.)

using open pond raceway systems to grow microalgae to

produce biodiesel. The 1000 m2 ponds located in a test site in
New Mexico succeeded in generating single day biomass
productivities as high as 50 g/m2 d. Conclusions from this
extensive study are summarized in the ASP final report.1
Detailed economic studies of open pond reactors are not found
widely in the literature but are abundant in the ASP report. The
results, though outdated, provide a sense of the range of costs
potentially associated with open ponds and the immense
variability of price based on what the pond may be equipped
with. The first notable analysis, by Benemann et al.45 in 1978,
was based on assumptions including 40 ha growth ponds with
multiple channels and productivities ranging from 6-18 g/m2 d.
The analysis did not consider species control, wastewater
treatment, nutrients, or the utilization of algal biomass. Design
aspects that were considered in the analysis included harvesting,
earthworks, pumps to move and lift the water, the supply
channels and piping required, transfer structures, settling ponds,
and ducting for CO2. Total capital costs were estimated (in 1978
dollars) at about $9,000/ha, without contingencies or engineering. Annualized costs were estimated at about $2,000/ha based
on a 15% per annum capital charge, $700/ha operating costs
for labor/nutrients, and free CO2.45
Benemann et al.46 conducted another analysis in 1982 that
was more thorough and featured paddle wheel mixing for the
40 ha ponds. Productivities were estimated to be twice as high,
but centrifugation and solvent extraction steps were now
considered. A power plant that would provide the CO2 was
assumed to be only 5 km away. Several scenarios were analyzed,
and total estimated capital costs ranged from $24,520 to $44,585/
ha (in 1982 dollars). Estimates of annual operating costs plus
return on investment ranged from $9,830 to $20,385/ha.46
These analyses were followed up with a study by Neenan et
al.47 in 1986, which included preliminary considerations of
downstream processing costs and an overall price per gallon of
biodiesel. Important assumptions were 30% lipid content in the
algal biomass, and a 17 g/m2 d average biomass productivity.
The overall projected system costs were $43,283/ha of ponds
and $433/mt of algal biomass produced (in 1986 dollars).47
Finally, the ASP report discussed a fourth analysis by
Weissman and Goebel48 in 1987. Due to the comprehensive
nature of the analysis, the many assumptions that were used
are not included here. The focus of the open pond design
appeared to be to maximize productivity with little emphasis
on cost reduction. The estimated capital cost was $72,000/ha

3522

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 7. Conceptual tubular reactor.

Figure 9. Conceptual FP reactor.

Figure 8. Conceptual column reactor.

(in 1987 dollars) for a system with an average productivity of

30 g/m2 d. The estimated annual cost of biomass production at
the previous productivity was $273/mt.48
The previous discussion should illustrate that open pond costs
can vary widely depending on the complexity of the design.
Nevertheless, the ASP report concluded that all alternatives to
open pond designs were cost-prohibitive at the time.1 In a 2006
review by Carvalho et al.,35 the authors also noted that recent
literature did not contain many details about production costs
and that these details would be necessary before reactor types
could be compared effectively.
Open ponds present significant technical challenges in addition to economic challenges. A major problem with open ponds
is the presence of competition and predation, as it is very
difficult to maintain a monoculture of one desired strain of algae
in an outdoor open environment. According to reviews by Lee
and Borowitzka, the most successful commercial strains of algae
grown in open ponds all thrive in extreme environments that
inhibit competition. For example, Dunaliella, Spirulina, and
Chlorella strains grow in environments exceptionally high in
salinity, alkalinity, and nutrients, respectively.4,44 Loss of water
to evaporation is yet another hindrance to the success of open
ponds. However, at the heart of the problem with open ponds
is the inadequate control of the design parameters necessary
for optimal algae growth.
4. Closed Photobioreactors
The literature often suggests that open ponds may have been
overemphasized21 and that they have reached a plateau in
productivity.35 Several authors articulated the need for closed
systems in order to achieve future advances in large-scale algae
production. They argued that as costs are reduced in the future,
closed systems will become the reactors of choice for biofuel
production.8,44
Numerous types of enclosed photobioreactors have been
designed in an attempt to best control the growth factors discussed earlier. The three main categories most generally suitable
for large-scale cultivation are tubular/horizontal, column/vertical,
and flat plate or flat panel (FP) reactors.49 The next set of Figures
7-9 displays the three main types of closed reactors in conceptual form.

Many other designs are not suitable for large-scale production

of biofuel and thus have been omitted from this discussion.
Though large-scale designs are the focus, the majority of
experiments comparing the designs were performed at laboratory
scale. In addition, the large-scale closed system examples
retrieved from the literature were often used to cultivate algae
for a purpose other than biofuel production. However, the insight
gained from analyzing these examples is relevant to the
application of biofuel production.
Some reactor designs included in literature deviate from the
conventional three types of closed reactors, but these have shown
limited promise. Borowitzka44 described a cylindrically shaped
helical tubular design known as the BIOCOIL that was
supposedly the most promising design at that time (1999).
However, limited discussion of the BIOCOIL during recent
years suggests that it no longer has potential. Watanabe and
Hall noted that the design has radiation losses in the central
area of the reactor. The authors attempted to improve it by
constructing a laboratory-scale cone-shaped helical tubular
reactor. This design supposedly increased the illuminated surface
area while covering the same area on the ground as a regular
tubular or FP reactor.50 Little has been reported on the ability
of the cone-shaped design to be scaled up. Algae have also been
cultivated in bag type reactors. However, according to Borowitzka, the big bag system suffers from the need to be operated
indoors for adequate temperature control. If installed indoors,
the large bags cannot be sufficiently illuminated by artificial
lighting, and mixing is generally insufficient.44
The concept of closed systems resulting in higher productivities is not supported unanimously in the literature. In a review
by Lee,4 the author claimed that 25 years worth of data show
that volumetric productivity and cost of production are not better
in closed systems compared to open ponds. However, the
majority of the literature reviewed for this paper contained
results contrary to that claim.
4.1. Closed Reactor Comparisons. Many key reactor comparison parameters were mentioned earlier along with design
considerations. Tredici et al. asserted that photosynthetic efficiency (PE) should be used in conjunction with volumetric
productivity when evaluating systems operated under similar
climactic conditions. The authors claimed that the PE is
significantly higher in tubular reactors compared to FP reactors
because their curved surface resulted in the spatial dilution of
light.7 Although some authors have claimed that FP reactors
may have greater photosynthetic efficiency,9 the results of
Tredici et al. are convincing and it appears that PE is a drawback
for FP reactors. Another drawback for FP reactors is that cell
damage may occur because of the high stress resulting from
aeration, a problem that has never been reported in tubular
reactors. However, FP reactors have advantages over other
closed reactors. In FP reactors, the oxygen path is much shorter
than in tubular reactors.49 A shorter oxygen path results in FP

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3523

Table 1. Typical Advantages and Disadvantages of the Three Main

Types of Closed Reactors
reactor type

typical advantages

typical disadvantages

FP

shortest oxygen path

low power consumption

low photosynthetic efficiency

shear damage from aeration

tubular

high volumetric
biomass density

oxygen accumulation
photoinhibition
most land use

vertical

Figure 10. Schematic representation of the reactors used: a bubble column

(BC), an airlift reactor (ALR), and an airlift reactor with helical flow
promoter (ALR+HFP).52 (Reprinted with kind permission from ref 52.
Copyright 2000 John Wiley and Sons.)

reactors having lower accumulation of dissolved oxygen concentrations than horizontal reactors.24 FP reactors also consume
less power than tubular reactors to achieve similar or greater
mass transfer capacity.49 Power consumption is another important criterion for comparison among reactor types.
Sanchez Miron et al.51 compared tubular and column reactors
and arrived at many significant conclusions. Tubular reactors
have very limited possibility for commercial scale applications,
whereas column reactors do have potential. Bubble column
reactors performed better than tubular reactors because they are
supposedly more suited for scale-up, require less energy for
cooling because of the low surface to volume ratio, and overall
outperform tubular reactors throughout the year. Under high
light intensity, vertical reactors experience less photoinhibition,
and under low light intensity, a vertical orientation captures more
reflected light.51 A vertical orientation also requires less land
area.17 Molina et al. asserted that, for tubular reactors, a twolayered loop with the lower set of tubes displaced horizontally
in between the upper set of tubes maximizes efficiency of land
use.36
Vertical reactors appear to best satisfy the design considerations outlined earlier in this paper, at least at laboratory scale.
There are two main types of vertical reactors: air-lift reactors
and bubble column reactors. Vertical air-lift reactors improve
gas exchange, liquid flow, and exposure of cells to light.17 Airlift reactors circulate the culture without moving parts or
mechanical pumping, which reduces the potential for contamination and for cell damage due to shear. The tubular photobioreactor of Molina et al., depicted earlier in Figure 4, was
air-lift driven. The air-lift both circulated the fluid through the
loop and stripped oxygen from the culture.36
Experiments involving different types of column reactors have
provided conflicting results. Merchuk et al.52 compared the
performance of an airlift reactor equipped with helical flow
promoters (ALR + HFP) to the performance of a bubble column
reactor, both at bench-scale. Figure 10 illustrates the benchscale reactors.
The authors found that the ALR + HFP performed the best
with regard to biomass production because improved fluid
dynamics led to less air and CO2 consumption, which significantly reduced operating costs.52 In a review by Janssen et al.,9
the authors analyzed pneumatically agitated vertical column
reactors, tubular reactors, and flat panel reactors. The authors
concluded that bubble column and air-lift reactors appear to
have similar light regimes and productivity, but that bubble

greatest gas exchange

best exposure to
light/dark cycles
least land use
high photosynthetic
efficiency

support costs
scalability

column reactors perform better at higher superficial gas velocities (above 0.05 m/s) and at column heights greater than the
2.32 m. used for comparison. The authors also claimed that
tubular reactors display equal or lesser photosynthetic efficiency
than bubble column or air-lift reactors, but that the biomass
density is twice as high.9 Finally, in a review by Eriksen et al.,
the authors noted that airlift and bubble column reactors may
be superior to stirred tank reactors because of the absence of
moving mechanical components, which require greater maintenance.53 The advantages and disadvantages of different types
of reactors are compared in Table 1. Table 1 reveals that each
of the most common reactor types exhibit tradeoffs between
key design parameters. Vertical reactors generally feature the
least land use among the three closed reactor types and high
photosynthetic efficiency, at least on the small scales most often
described in the literature. Excluding cost, these two measures
of performance may be the most important when selecting a
reactor configuration. However, vertical reactors are most
susceptible to scalability challenges, thus making it difficult to
determine the preferred reactor type among these choices for
commercial scale applications.
4.2. Closed Reactor Scalability. According to Sierra et al.,
flat panel and tubular photobioreactors have been scaled-up to
sizes exceeding 1000 L, but vertical reactors are limited to an
optimum size of 125 L.49 There are limited examples of largescale applications of air-lift reactors. Vunjak-Novakovic et al.
described the design and operation of a pilot-scale triangular
air-lift unit fed by flue gas. The pilot-scale unit was composed
of 30 ALRs, each containing a volume of 30 L. The system
was installed and tested under actual conditions on the roof of
the Cogeneration Power Plant at the Massachusetts Institute of
Technology.54 Figure 11 contains images of the triangular airlift reactor configuration:
Tubular reactors can be scaled-up by either increasing the
length or diameter of the tubes. Either route presents technical
challenges. An increase in tube length results in unacceptable
concentrations of dissolved oxygen along the tubes. In contrast,
increasing the tube diameter may be more promising as long
as the entire culture can be illuminated sufficiently. However,
one of the major problems of increasing the diameter is light
stratification.23,36 Molina et al. noted that scale-up of the airlift driven tubular reactor discussed earlier would be challenging.36 However, Chisti was optimistic about the scale-up of
tubular reactors and claimed that only tubular photobioreactors
and raceway ponds are suitable for large-scale production.5
Janssen et al. concluded that scale-up of closed systems is
only possible by increasing the number of small units in a
production scheme. This method becomes extremely expensive,
since each unit requires a variety of devices that control the
wide range of growth factors discussed earlier in this paper. In

3524

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 11. Inclined-tube ALR configuration: (A) schematic presentation of one airlift triangle. Solid arrows indicate the direction of the gas flow, and
open arrows indicate the direction of the liquid flow (B) An array of 30 ALRs, each with a volume of 30 L, with an algal culture grown on a flue gas. Inset:
installation of the array of ALRs on the roof of the MIT Cogeneration Power Plant.54 (Reprinted with kind permission from ref 54. Copyright 2005
American Chemical Society.)

Figure 12. Commercial-scale photobioreactor facility in Klotze, Germany.

(Reprinted with kind permission from ref 3. Copyright 2006 Society of
Fermentation and Bioengineering.)

addition, maintaining a monoculture in all of the units becomes

challenging as the number of units to monitor and service
grows.9
Commercial-scale closed photobioreactors have not been
widely reported in scientific literature. Closed systems for commercial applications began in Japan, Israel, and Germany.3
Janssen et al. claimed to describe the worlds largest example
of a closed reactor system as of the year 2003. The 700 m3
tubular production system in Klotze, Germany, consisted of 20
separate 35 m3 units. Chlorella Vulgaris was mechanically
pumped through horizontal glass tubes with 4 cm diameter and
25 000 m of length for each unit. The authors questioned the
estimated productivity of 150 tons of biomass per year, and no
other figures were reported in the review.9 A review by Spolaore
et al.3 also mentioned the Klotze facility and states a production
rate of 130-150 tons dry biomass/y. Figure 12 is an image of
the Klotze facility.
The review by Janssen et al. also claimed to describe the
largest flat panel reactor example, which was studied by
Richmond and Cheng-Wu.55 The large-scale reactor described
was composed of individual units of 200 L, and the units were
connected as illustrated in Figure 13.
4.3. Closed Reactor Economics. The paramount advantages
of closed systems are the greater control of design parameters
and the growth of algae essentially as a monoculture. However,
economics are currently a major drawback for closed systems.

Between 2002 and 2004, $100/m2 was an estimate of photobioreactor capital costs used in the literature, with the expectation of significant cost reductions as technology improved.56
In a review by Schenk et al., the authors claimed that reactor
costs should not exceed $15/m2 based on energy costs and
productivities from 2008. The estimated setup costs for closed
reactors were generally ten times higher than for open ponds.8
In a review by Chisti,5 direct comparisons were made between
the production costs of hypothetical facilities producing 100 000
kg of biomass annually using either photobioreactors or raceway
ponds. Chisti found that the estimated production costs were
$2.95 and $3.80/kg of biomass for closed reactors and raceway
ponds, respectively. Under a scaled-up scenario of 10 000 tons
of biomass produced per year, the estimated production costs
were $0.47 and $0.60/kg of biomass for closed versus open
reactors.5 Note that this analysis did not consider the capital
costs involved with creating either facility, but it did show that
production costs are expected to be lower in closed systems.
Because of economic considerations, many authors have concluded that closed reactors can only be used for the production
of high-value products.12,35
The ASP report contained an important conclusion regarding
the evaluation of the potential economics of algae production,
whether it involved open or closed systems. The report asserts
that high value byproducts or coproducts, such as pigments,
vitamins, or specialty chemicals created from the remaining
biomass, should be excluded from the cost analysis. These
products would be produced in such large amounts that they
would saturate potential markets. An exception would be large
byproduct markets such as for animal feeds, and indeed, the
authors believed that a likely route for commercial scale
production will utilize specialty foods and animal feeds coproduction.1 However, Chisti argued that most of the biomass
remaining after oil extraction should be made into biogas using
anaerobic digestion. The resulting biogas would then be used
to meet the energy needs of growing and processing algae in
the same facility. Economic benefits from using this approach
include the sale of surplus energy, nutrient-rich fertilizer, and
irrigation water all produced while making biogas.41
5. Combinations of Open and Closed Systems
Some authors believe that combining open and closed reactors
is the most effective configuration for growing algae.8 Huntley

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3525

Figure 13. A schematic drawing of 2 units, 200 L each, connected together. (a) point of connection of two reactor units, (b) inner supports, (c) braces for
keeping together the front and back plates, (d) distance between the bottom of the reactor and the inner supports, (e) passage made between the two units
to create a common volume between units.55 (Reprinted with kind permission from ref 55. Copyright 2001 Elsevier.)

and Redalje,56 as well as Olaizola,57 described a two-stage

commercial-scale production system that was in continuous
operation from December 1997 to September 2001. The
Aquasearch facility, located in Hawaii, was designed to
maximize the production of astaxanthin from Haematococcus
pluVialis, but the strain also produces oil under the same
conditions. The facility featured 25 000 L closed photobioreactors and 50 000 L open ponds, with a total capacity of over
600 000 L equally divided between photobioreactors and ponds.
During the final year of operation, the average areal productivity
was 10.2 g/m2 d, which corresponded to a photosynthetic
efficiency of 3.0%.56
The two-stage process began with growth in an industrialscale closed reactor. The highly controlled environment in this
step maximized cell growth. Next, the algae were exposed to
nutrient deprivation by being transferred to an open pond reactor.
Finally, the stress increased the lipid content of each cell. An
important guideline to adhere to when considering a hybrid
reactor scheme is minimizing the residence time of the algae
in the open pond, where they are vulnerable to contamination.56
Rodolfi et al. also considered a similar two stage process, in
which 22% of the hypothetical plant is dedicated to biomass
production under N-sufficiency and the remainder is devoted
to oil production under N-deprivation.38
Similar to the reactor configurations discussed earlier, critical
drawbacks are present with the two-stage approach. The capital
and operating costs for both a commercial-scale closed reactor
and a commercial-scale open pond are likely to be significantly
higher than for one reactor. In a review by Vasudevan and
Briggs, it was observed that because the facility described by
Huntley and Redalje produced astaxanthin, which is a highvalue product, the economics were significantly better than the
economics based on primarily biofuel production.58 In addition,
the land requirements are much greater than for one reactor and
the increased land use reduces the productivity per area.
6. Conclusion
The cultivation of microalgae for biofuel production requires
high levels of biomass productivity per area and minimal costs.
Major technical and economic challenges impede the selection
of an optimal reactor type at the commercial scale. Without
detailed economic considerations, closed reactors appear to
perform better than open ponds because they maintain favorable
growth conditions and are less vulnerable to contamination. The

best reactor type, based on photosynthetic efficiency and areal

productivity, appears to be column reactors, at least on the small
scale used in experiments from the literature. However, technical
constraints prevent the size of this reactor type from being
increased to commercial scale without the use of multiple small
units, which are unlikely to be economical. Combinations of
open and closed reactors seem promising from a productivity
perspective. However, there is not enough economic information
available to assess whether the increased productivity can offset
the extra capital investment required, particularly with regard
to biofuel applications. Thus, at this time, no specific reactor
type is optimal for the commercial cultivation of microalgae
for biofuel production. This agrees with the general conclusion
arrived at by other authors.12,35
Literature Cited
(1) Sheehan, J.; Dunahay, T.; Benemann, J.; Roessler, P. A Look Back
at the U.S. Department of Energys Aquatic Species Program: Biodiesel
from Algae; U.S. Department of Energy, 1998. doi: 10.2172/15003040.
(2) Demirbas, A. Importance of biodiesel as transportation fuel. Energy
Policy 2007, 35 (9), 46614670.
(3) Spolaore, P.; Joannis-Cassan, C.; Duran, E.; Isambert, A. Commercial
applications of microalgae. J. Biosci. Bioeng. 2006, 101 (2), 8796.
(4) Lee, Y. K. Microalgal mass culture systems and methods: Their
limitation and potential. J. Appl. Phycol. 2001, 13 (4), 307315.
(5) Chisti, Y. Biodiesel from microalgae. Biotechnol. AdV. 2007, 25 (3),
294306.
(6) Mussgnug, J. H.; Thomas-Hall, S.; Rupprecht, J.; Foo, A.; Klassen,
V.; McDowall, A.; Schenk, P. M.; Kruse, O.; Hankamer, B. Engineering
photosynthetic light capture: impacts on improved solar energy to biomass
conversion. Plant Biotechnol. J. 2007, 5 (6), 802814.
(7) Tredici, M. R.; Zittelli, G. C. Efficiency of sunlight utilization:
Tubular versus flat photobioreactors. Biotechnol. Bioeng. 1998, 57 (2), 187
197.
(8) Schenk, P. M.; Thomas-Hall, S. R.; Stephens, E.; Marx, U. C.;
Mussgnug, J. H.; Posten, C.; Kruse, O.; Hankamer, B. Second generation
biofuels: High-efficiency microalgae for biodiesel production. Bioenergy
Res. 2008, 1 (1), 19391234.
(9) Janssen, M.; Tramper, J.; Mur, L. R.; Wijffels, R. H. Enclosed
outdoor photobioreactors: Light regime, photosynthetic efficiency, scaleup, and future prospects. Biotechnol. Bioeng. 2003, 81 (2), 193210.
(10) Richmond, A. Principles for attaining maximal microalgal productivity in photobioreactors: an overview. Hydrobiologia 2004, 512 (1-3),
3337.
(11) Park, K.-H.; Lee, C.-G. Effectiveness of flashing light for increasing
photosynthetic efficiency of microalgal cultures over a critical cell density.
Biotechnol. Bioprocess Eng. 2001, 6, 189193.
(12) Pulz, O.; Scheibenbogen, K. Photobioreactors: Design and performance with respect to light energy input. AdV. Biochem. Eng./Biotechnol.
1998, 59, 123152.

3526

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

(13) Goldman, J. C. Outdoor Algal Mass-Cultures 0.2. Photosynthetic

Yield Limitations. Water Res. 1979, 13 (2), 119136.
(14) Matthijs, H. C. P.; Balke, H.; VanHes, U. M.; Kroon, B. M. A.;
Mur, L. R.; Binot, R. A. Application of light-emitting diodes in bioreactors:
Flashing light effects and energy economy in algal culture (Chlorella
pyrenoidosa). Biotechnol. Bioeng. 1996, 50 (1), 98107.
(15) Janssen, M.; Slenders, P.; Tramper, J.; Mur, L. R.; Wijffels, R. H.
Photosynthetic efficiency of Dunaliella tertiolecta under short light/dark
cycles. Enzyme Microbial. Technol. 2001, 29 (4-5), 298305.
(16) Gordon, J. M.; Polle, J. E. W. Ultrahigh bioproductivity from algae.
Appl. Microbiol. Biotechnol. 2007, 76 (5), 969975.
(17) Camacho, F. G.; Gomez, A. C.; Fernandez, F. G. A.; Sevilla, J. F.;
Grima, E. M. Use of concentric-tube airlift photobioreactors for microalgal
outdoor mass cultures. Enzyme Microbial. Technol. 1999, 24 (3-4), 164
172.
(18) Zu, N.; Richmond, A. Light-path length and population density in
photoacclimation of Nannochloropsis sp. (Eustigmatophyceae). J. Appl.
Phycol. 2000, 12 (3-5), 349354.
(19) Feuermann, D.; Gordon, J. M.; Huleihil, M. Solar fiber-optic minidisit-concentrators: First experimental results and field experience. Solar
Energy 2002, 72 (6), 459472.
(20) Zijffers, J. W. F.; Janssen, M.; Tramper, J.; Wijffels, R. H. Design
process of an area-efficient photobioreactor. Marine Biotechnol. 2008, 10
(4), 404415.
(21) Suh, I. S.; Lee, C. G. Photobioreactor engineering: Design and
performance. Biotechnol. Bioprocess Eng. 2003, 8 (6), 313321.
(22) Qiang, H.; Richmond, A. Productivity and photosynthetic efficiency
of Spirulina platensis as affected by light intensity, algal density and rate
of mixing in a flat plate photobioreactor. J. Appl. Phycol. 1996, 8 (2), 139
145.
(23) Ugwu, C. U.; Ogbonna, J. C.; Tanaka, H. Characterization of light
utilization and biomass yields of Chlorella sorokiniana in inclined outdoor
tubular photobioreactors equipped with static mixers. Process Biochem.
2005, 40 (11), 34063411.
(24) Ugwu, C. U.; Aoyagi, H.; Uchiyama, H. Photobioreactors for mass
cultivation of algae. Bioresour. Technol. 2008, 99 (10), 40214028.
(25) Eriksen, N. T.; Poulsen, B. R.; Iversen, J. J. L. Dual sparging
laboratory-scale photobioreactor for continuous production of microalgae.
J. Appl. Phycol. 1998, 10 (4), 377382.
(26) Barbosa, M. J.; Hadiyanto; Wijffels, R. H. Overcoming shear stress
of microalgae cultures in sparged photobioreactors. Biotechnol. Bioeng.
2004, 85 (1), 7885.
(27) Berndes, G. Bioenergy and water--the implications of large-scale
bioenergy production for water use and supply. Global EnViron. Change
2002, 12 (4), 253271.
(28) Wogan, D. M.; Silva, A. K. D.; Webber, M. E.; Stautberg, E. Algae:
Pond Powered Biofuels; ATI CleanEnergy Incubator, The University of
Texas at Austin: Austin, November 19 , 2008; pp 1-23.
(29) Yun, Y.-S.; Lee, S. B.; Park, J. M.; Lee, C.-I.; Yang, J.-W. Carbon
Dioxide Fixation by Algal Cultivation Using Wastewater Nutrients. J. Chem.
Technol. Biotechnol. 1997, 69 (4), 451455.
(30) Rao, A. R.; Dayananda, C.; Sarada, R.; Shamala, T. R.; Ravishankar,
G. A. Effect of salinity on growth of green alga Botryococcus braunii and
its constituents. Bioresour. Technol. 2007, 98 (3), 560564.
(31) Abu-Rezq, T. S.; Al-Musallam, L.; Al-Shimmari, J.; Dias, P.
Optimum production conditions for different high-quality marine algae.
Hydrobiologia 1999, 403, 97107.
(32) Aslan, Sebnem; Kapdan, I. K. Batch kinetics of nitrogen and
phosphorus removal from synthetic wastewater by algae. Ecol. Eng. 2006,
28 (1), 6470.
(33) Lee, Y.-K.; Tay, H.-S. High CO2 partial pressure depresses
productivity and bioenergetic growth yield of Chlorella pyrenoidosa culture.
J. Appl. Phycol. 1991, 3, 95101.
(34) Doucha, J.; Straka, F.; Livansky, K. Utilization of flue gas for
cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer
photobioreactor. J. Appl. Phycol. 2005, 17 (5), 403412.
(35) Carvalho, A. P.; Meireles, L. A.; Malcata, F. X. Microalgal reactors:
A review of enclosed system designs and performances. Biotechnol. Prog.
2006, 22 (6), 14901506.
(36) Molina, E.; Fernandez, J.; Acien, F. G.; Chisti, Y. Tubular
photobioreactor design for algal cultures. J. Biotechnol. 2001, 92 (2), 113
131.

(37) Mandalam, R. K.; Palsson, B. O. Elemental balancing of biomass

and medium composition enhances growth capacity in high-density Chlorella
vulgaris cultures. Biotechnol. Bioeng. 1998, 59 (5), 605611.
(38) Rodolfi, L.; Zittelli, G. C.; Bassi, N.; Padovani, G.; Biondi, N.;
Bonini, G.; Tredici, M. R. Microalgae for Oil: Strain Selection, Induction
of Lipid Synthesis and Outdoor Mass Cultivation in a Low-Cost Photobioreactor. Biotechnol. Bioeng. 2009, 102 (1), 100112.
(39) Coleman, J. R.; Colman, B. Inorganic carbon accumulation and
photosynthesis in a blue-green alga as a function of external pH. J. Phycol
1981, (27), 28.
(40) Lee, Y. K.; Pirt, S. J. CO2 absorption rate in an algal culture: Effect
of pH. Plant. Physiol. 1984, (67), 917921.
(41) Chisti, Y. Biodiesel from microalgae beats bioethanol. Trends
Biotechnol. 2008, 26 (3), 126131.
(42) Pulz, O.; Gross, W. Valuable products from biotechnology of
microalgae. Appl. Microbiol. Biotechnol. 2004, 65 (6), 635648.
(43) Borowitzka, M. A. Algal biotechnology products and processes:
matching science and economics. J. Appl. Phycol. 1992, 4 (3), 267279.
(44) Borowitzka, M. A. Commercial production of microalgae: ponds,
tanks, tubes and fermenters. J. Biotechnol. 1999, 70 (1-3), 313321.
(45) Benemann, J. R. P., P.; Oswald, W. J. Cost analysis of microalgae
biomass systems; HCP/t1-605-01 Under Contract EX-78-X-01-1 605; Final
Report prepared for the U.S. Dept. of Energy, 1978.
(46) Benemann, J. R. A., D.C.; Weissman, J. C. Microalgae as a source
of liquid fuels, appendix: technical feasibility analysis; Final Report, U.S.
Department of Energy: Washington, D. C., 1982; p 126.
(47) Neenan, B. F., D.; Hill, A.; McIntosh, R.; Terry, K. Fuels from
microalgae: Technology status, potential, and research requirements; SERI/
SP-231-2550; Report, Solar Energy Research Institute: Golden, CO: 1986;
p 158.
(48) Weissman, J. C. ; Goebel, R. P. Design and analysis of pond systems
for the purpose of producing fuels; SERI/STR-231-2840; Report, Solar
Energy Research Institute: Golden, CO: 1987.
(49) Sierra, E.; Acien, F. G.; Fernandez, J. M.; Garcia, J. L.; Gonzalez,
C.; Molina, E. Characterization of a flat plate photobioreactor for the
production of microalgae. Chem. Eng. J. 2008, 138 (1-3), 136147.
(50) Watanabe, Y.; Hall, D. O. Photosynthetic production of the
filamentous cyanobacterium Spirulina platensis in a cone shaped helical
tubular photobioreactor. Appl. Microbiol. Biotechnol. 1996, 44 (6), 693
698.
(51) Sanchez Miron, A.; Contreras Gomez, A.; Garca Camacho, F.;
Molina Grima, E.; Chisti, Y. Comparative evaluation of compact photobioreactors for large-scale monoculture of microalgae. J. Biotechnol.
Biotechnol. Aspects Marine Sponges 1999, 70 (1-3), 249270.
(52) Merchuk, J C.; Mukmenev, M. G., I. Comparison of photobioreactors for cultivation of the red microalga Porphyridium sp. J. Chem.
Technol. Biotechnol. 2000, 75 (12), 11191126.
(53) Eriksen, N. T. The technology of microalgal culturing. Biotechnol.
Lett. 2008, 30 (9), 15251536.
(54) Vunjak-Novakovic, G.; Kim, Y.; Wu, X. X.; Berzin, I.; Merchuk,
J. C. Air-lift bioreactors for algal growth on flue gas: Mathematical modeling
and pilot-plant studies. Ind. Eng. Chem. Res. 2005, 44 (16), 61546163.
(55) Richmond, A.; Cheng-Wu, Z. Optimization of a flat plate glass
reactor for mass production of Nannochloropsis sp outdoors. J. Biotechnol.
2001, 85 (3), 259269.
(56) Huntley, M. E.; Redalje, D. G. CO2 mitigation and renewable oil
from photosynthetic microbes: A new appraisal. Mitigation Adapt. Strat.
Global Change 2007, 12 (4), 573608.
(57) Olaizola, M. Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J. Appl.
Phycol. 2000, 12 (3-5), 499506.
(58) Vasudevan, P. T.; Briggs, M. Biodiesel production-current state of
the art and challenges. J. Ind. Microbiol. Biotechnol. 2008, 35 (5), 421
430.
(59) Seambiotic. http://www.seambiotic.com (accessed July 6, 2009).

ReceiVed for reView September 16, 2009

ReVised manuscript receiVed February 26, 2010
Accepted March 1, 2010
IE901459U