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178 Eng. Life Sci. 2009, 9, No.

3, 178–189

Ling Xu1,2 Review


Pamela J. Weathers3,4
Xue-Rong Xiong5 Microalgal bioreactors: Challenges and
Chun-Zhao Liu1
opportunities
1
National Key Laboratory of
Biochemical Engineering, Cultivating and harvesting of products from microalgae has led to increasing
Institute of Process commercial interest in their use for producing valuable substances for food, feed,
Engineering, Chinese cosmetics, pharmaceuticals, and biodiesel, as well as for mitigation of pollution
Academy of Sciences, and rising CO2 in the environment. This review outlines different bioreactors and
Beijing 100190, P. R. China their current status, and points out their advantages and disadvantages.
2
School of Biotechnology, Compared with open-air systems, there are distinct advantages to using closed
Jiangnan University, Wuxi systems, but technical challenges still remain. In view of potential applications,
214122, P. R. China development of a more controllable, economical, and efficient closed culturing
3
Department Biology/
system is needed. Further developments still depend on continued research
Biotechnology, Worcester in the design of photobioreactors and break-throughs in microalgal culturing
Polytechnic Institute, technologies.
Worcester, MA 01609, USA
Keywords: Microalgae / Photobioreactor / Scale-up
4
Arkansas Bioscience
Institute, Arkansas State Received: December 8, 2008; revised: May 23, 2009; accepted: May 29, 2009
University, State University, DOI: 10.1002/elsc.200800111
AR 72467, USA
5
Division of Industrial
Biotechnology, Bureau of
Life Sciences and
Biotechnology, Chinese
Academy of Sciences,
Beijing 100864, P. R. China

1 Introduction biotechnology because algae offer a number of advantages


from an industry perspective. These include ease of culture and
Microalgae are unique and potentially valuable microorgan- harvesting of products [1], greater photosynthetic efficiency
isms because they are the light-harvesting ‘‘cell factories’’ that than terrestrial plants [15], higher biomass productivities,
convert carbon dioxide into biomass or a variety of bioactive faster growth rates than higher plants, and higher rates of CO2
compounds. Although many can grow heterotrophically, all fixation and O2 production [14].
microalgae are photoautotrophs, requiring mainly sun, water, Commercial culture of microalgae has440 years history
and inorganic nutrients for growth. Compared to higher with some of the main species grown being Spirulina for health
plants, microalgae are simple in structure, being unicellular, food, Dunaliella salina and Haematococcus pluvialis for
filamentous or colonial, and energy is directed via photo- carotenoid production, and several species for aquaculture
synthesis into growth and reproduction; they do not need to [10, 16, 17]. While in the past natural waters (lakes, lagoons,
establish and maintain complex tissues and organs [1]. ponds) or artificial ponds were used to grow algae, more
Microalgae have the potential to produce valuable substances recently closed photobioreactors have been employed [10, 18].
for the food, feed, cosmetic, pharmaceutical, and waste treat- Open-culture systems have almost always been located
ment industries [2–10]. More recently these photosynthetic outdoors and rely on natural light for illumination. Although
microbes have also become the focus of considerable attention they are inexpensive to install and run, open systems suffer
as a potential source of oils for biodiesel production [11–14]. from many problems: cultures are not axenic so contaminants
Indeed, the cultivation and harvest of products from micro- may out compete the desired algal species; predators like
algae has led to an increased commercial interest in their rotifers can decimate the algal culture, and vagaries of weather
can make proper control of nutrients, light intensity, and CO2
at best challenging [10]. Closed photobioreactors, on the other
Correspondence: Dr. Chun-Zhao Liu (czliu@home.ipe.ac.cn), National hand, have been used to axenically grow photosynthetic
Key Laboratory of Biochemical Engineering, Institute of Process Engi- microorganisms such as microalgae, cyanobacteria, plant
neering, Chinese Academy of Sciences, Beijing 100190, P. R. China. cells, and photosynthetic bacteria for various research and

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
Eng. Life Sci. 2009, 9, No. 3, 178–189 Microalgal Bioreactors 179

biotechnological applications. A comparison of open and mizing cost efficient mass transfer of CO2 to cells in an
closed systems for microalgae is shown in Table 1. Photo- aqueous environment is not a trivial task for large-scale liquid
bioreactors used for the cultivation of microalgae are either culture systems as is anticipated for outdoor algal cultures.
naturally or artificially illuminated. Algal culture systems with Furthermore, many algae can also grow heterotrophically and
naturally illuminated large surface areas include open although this is a benefit in terms of remediation of liquid
ponds, flat-plate, horizontal/serpentine tubular airlift, and waste streams, the presence of any reduced carbon can also
inclined tubular photobioreactors [19]. Generally, laboratory- wreak havoc in nonaxenic algal systems because microbial
scale photobioreactors are usually artificially illuminated contaminants with their faster growth rates can easily outpace
with fluorescent or other types of lamps. Closed reactors can algal growth. Consequently the supply of carbon to microalgal
be sited indoors or outdoors, and offer better control of mass culture systems represents a principal difficulty and
culture conditions. Unfortunately they are also usually limitation in obtaining cost effective production of algal
more expensive to install. As a result they are under intensive biomass [27–30].
study in an effort to reduce costs to better facilitate their The few commercial species that are currently being
use especially for low value products like algal oils for successfully cultured in large open ponds are extremophiles
biodiesel. growing in a highly selective environment (high pH, salinity,
Although cultivation of microalgae seems easy, there are or temperature). These conditions preclude the growth of most
many challenges including: (i) minimizing contamination (ii) other algae and even many bacteria.
efficient provision of carbon dioxide and light; (iii) controlling For the future of microalgal biotechnology, however, it
cultivation conditions; (iv) reducing capital and production remains important to develop large-scale photobioreactors
costs; and (v) minimizing space requirements [20, 21]. For that can be operated under defined, optimal conditions with
instance, although the high light intensity of full sunlight capability for sterilization, and with minimal contamination
would seem desirable, it can lead to photoinhibition, yielding risks. Although it is difficult to compare open ponds with
toxic photo products including H2O2, O-2, 1O .
2 , OH, and closed systems or with indoor photobioreactors, the general
triplet chlorophyll, and even damage the Photosystem II consensus suggests that open systems may predominate for
reaction center [22, 23]. Low light intensities, on the other mass cultivation of algae for low value products like biofuels,
hand may limit photosynthetic activity and thus, biomass while photobioreactors will be more useful for production of
productivity. Whereas many algae can become somewhat high value products like therapeutics [31].
acclimated to different light intensities, the level of sensitivity In this review, we have divided microalgal bioreactors
to light varies with species [7]. Indeed we have observed that at described in the literature into classes according to their
very low light intensities Botryococcus braunii grows much geometric features, indicated their advantages and disadvan-
better than Chlorella vulgaris which grows much better at the tages, and compared their overall performance. The purpose of
higher intensities that inhibit B. braunii (unpublished results). this review is to outline the current status and recent devel-
This variable light response has therefore required develop- opments in the technology used to culture microalgae while
ment of novel concepts in both design and operation of also noting challenges and opportunities.
photobioreactors aimed at exploiting the full range of photo-
synthetic biochemistry [24–26]. For example, transparent flat
angled culture systems have been developed and tested to 2 Open-air cultivation systems
maximize light incidence to the culture [24].
Another challenge to be met is optimal CO2 feeding of Open-air cultivation systems comprise natural or artificial
cultures. Algae are photoautotrophs using CO2 as a carbon ponds, raceway ponds, and so-called inclined surface systems
source and this can aid in CO2 mitigation of the environment driven by paddle wheels, usually operating at water depths of
and reduction of global warming. On the other hand, maxi- 15–30 cm [16]. They represent the classical processes used for
production of algal biomass. Although different types of open
reactors have been put into operation since the late fifties by
Table 1. A comparison of open and closed systems for microalgae
[18, 97]. different groups, the most commonly used systems include
shallow big ponds, tanks, circular ponds, and raceway ponds.
Open systems Closed systems Raceway-shaped culture ponds are used in Israel, the United
States of America, China and other countries. A raceway pond
Contamination risk High Low
CO2 losses High Low
consists of a closed loop recirculation channel that is typically
Evaporative losses High Low about 0.3 m deep (Fig. 1) [32]. Nutrient fertilizer is added and
Light use efficiency Poor Excellent the culture is agitated by a paddle wheel [7, 33]. The largest
Area/volume ratio Low High raceway-based biomass production facility located in Calipa-
Area required High Low tria, CA, USA occupies an area of 440,000 m2 to grow Spirulina
Process control Difficult Easy [34].
Biomass productivities Low High Compared to the classical flat ‘raceway’ pond, an inclined
Investment costs Low High surface offers two advantages: better turbulent flow, and
Operation costs Low High shallower culture depth (the mean depth of the culture in the
Harvesting costs High Relatively low
inclined slope is 3.5 cm). This reduces the thermal inertia of
Scale-up Easy Difficult
the culture allowing a more rapid increase of its temperature

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
180 L. Xu et al. Eng. Life Sci. 2009, 9, No. 3, 178–189

Reference
Table 2. Comparison of different closed microalgal culture systems. Photon flux density (PFD), photosynthetic efficiency (PE), light path or diameter (D), volume (V), biomass

[107]
[51]
[41]
[42]
[98]

[63]
[74]
[67]
[86]
[74]
[75]
concentration (Cx), volumetric productivity (Pvolumetric), areal productivity (Pareal), superficial gas velocity (ug), overall mass transfer coefficiency (kLa) , power supply (P).

Nannochloropsis

Haematococcus
Phaeodactylum
Phaeodactylum

Phaeodactylum

Phaeodactylum
Algal strain

Chaetoceros

Chaetoceros
Dunaliella
Spirulina

Monodus
(w m 3)

42000

a) Calculated from biomass yield on light energy by using a value of 218.8 kJ mol 1 photons [108] and a specific energy content of biomass of 25 kJ g-1 [109]
130
--
--

--
--
--
--

--
--
--
P
(  10 3s 1)

20-25
Figure 1. Aerial schematic view of a raceway pond [7].

kLa

6
4
--

--
--
--
--

--
--
--
(m s 1)
during the morning. In order to better control temperature

0.017
0.30
0.41

0.01

0.01
and use solar irradiance, an open pond was coupled with an

0.4
ug

--

--
--
--

--
appropriately sized and oriented flat panel and thus the algal
productivity increased in the outdoor culture [35]. Recent

(g L 1 day 1)
research showed that carbon dioxide absorption by algae

Pvolumetric

0.03-0.20
could be further enhanced by 78% by installing a specially

b) Calculated from biomass concentration (cell mL 1) by using a value of 2.228 g dry weight per 1  109 cells [75]
0.225
0.62
1.19
1.38

1.38

3.31

4.09
0.80
designed carbon dioxide sparging system in an outdoor race-

1.5

--
way pond [36].
An open culture unit affords ready access to sunlight, and is day 1)
easier to build and operate than most closed systems; open
systems have been studied considerably over the past forty years
2

[7, 37]. As a result, however, a number of major drawbacks have

11.25
Pareal
(g m

31.8
20
been identified [17, 35, 36, 38] including: (i) only a small
--

--
--

--
--
--
--
--
number of algal species can be grown in large scale successfully;
(g L 1)

0.9–1.0
0.4–1.4
5.60 b)

6.77 b)
1.77 b)
(ii) wild microbial predators are a problem; (iii) there are
3.26
2.38
3.03

significant evaporative losses and water conservation therefore


7.3
2.6
Cx

--

becomes an issue; (iv) CO2 is not used efficiently; (v) a large


area of land is required, so only unproductive or waste land can
200

200
170

170
(L)

5.5

3.4

1.9
75

64
V

3
be used; (vi) biomass productivity is lower than that in closed
cultivation systems; and (vii) costs of harvesting algal biomass
(cm)

1.2

are still high. Although efforts have been made to improve open
10
79

21
79
10
D

6
3
3
3

ponds with temperature control systems, supplies of appropriate


6.8 a)

6.8 a)

nutrients, optimization of pond depth, CO2 injection systems,


13.4
(%)

8.0

4.8
PE

--

--
--
--

--
--

etc [39], productivity remains fairly low compared to closed


systems. Because of these limitations, focus has shifted to
s 1)

development of cost effective closed cultivation systems which


are described next.
2
(mı̀mol m

1289
1135
1000
1000
PFD

120

500

3 Closed cultivation systems


72

72
20
--

--
Artificial

Artificial

Artificial

Artificial

Unlike open-air systems, closed photobioreactors are aimed at


source
Light

mainly axenic single-species culture of microalgae. Photo-


Sun

Sun

Sun

bioreactors have been used successfully for producing large


quantities of microalgal biomass [7], and their design config-
Photobioreactor

Tubular reactor

urations include horizontal or serpentine tube, flat-plate,


Bubble column

Airlift reactor

bubble column, airlift column and stirred tank. A comparison


Flat plate

of performance is shown in Table 2. As shown in the table,


photosynthetic efficiency in tubular reactors was higher
type

than those in other systems. For the outdoor culture of

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
Eng. Life Sci. 2009, 9, No. 3, 178–189 Microalgal Bioreactors 181

Phaeodactylum, better biomass concentration and areal gradient in carbon fixation can lead to pH gradients; a high
productivity were obtained in the 5-L flat plate reactor. Its rate of CO2 fixation results in hydroxide ion build-up in the
volume, however, was smaller than that of the tubular reactor. medium reaching a pH as high as 11. On the other hand,
For pilot-scale cultivation of Chaetoceros, high volumetric inadequate fixation of CO2 sparged into the culture medium
productivity was achieved in pneumatically agitated photo- may result in acidification from carbonic acid formation. A
bioreactors and the airlift system showed better performance. well functioning photobioreactor will have a well balanced pH;
the rising hydroxyl ion produced from photosynthesis is
counterbalanced by increased carbonic acid production from
3.1 Tubular photobioreactors CO2 sparging.
Besides diameter and tube length, mixing is also problematic
Fully closed tubular photobioreactors are potentially attractive in extended tubes [40]. Ugwu et al., however, were able to
for large-scale axenic culture of microalgae and is one of the improve mass transfer in tubular reactors by installing internal
more suitable types for outdoor mass culture [19, 40]. Tubular static mixers to enhance mixing [52, 53]. For the above reasons,
photobioreactors consist of an array of straight, coiled, or therefore, tubular photobioreactors cannot be scaled up inde-
looped transparent tubes that are usually made of transparent finitely, and large-scale production plants would likely have to
plastic or glass [41–43]. Algae are circulated through the tubes rely in part on an assemblage of modular reactor units [9].
by a pump, or airlift technology [44]. Use of an airlift device
seems to offer some advantages: it allows CO2 and O2 to be
exchanged between the liquid medium and the aeration gas; 3.2 Flat plate photobioreactors
potential cell damage associated with mechanical pumping
may be minimized; and circulation is achieved without moving When one considers the laminar morphology of plant leaves, they
parts. In some cases the temperature of the tubular photo- are well evolved solar collectors, and thus, plate type geometries
bioreactor is reported to be better controlled by floating or seem to have been modeled similarly with a high surface/volume
submerging the tubes on or in a pool of water [31]. ratio. Compared to tubular bioreactors, however, there are some
Gudin and Chaumont were the first to develop a 100 m2 advantages with respect to compactness: their narrow U-turns may
tubular reactor made of polyethylene tubes for the cultivation use less space than coiled tubes, and their wall thickness can be
of the red alga, Porphyridium cruentum, and Torzillo et al. thinner than tubular bioreactor [31]. The cultures in these
explored the development of a tubular photobioreactor for photobioreactors are also mixed with air introduced via a perfo-
outdoor mass production of Spirulina platensis [45, 46]. rated tube at the bottom of the reactor. Usually, the panels are
Instead of being laid horizontally on the ground, the helical illuminated mainly on one side by direct sunlight and have the
tubular system rises vertically as an arrangement of transpar- added advantage that they can be positioned vertically or inclined
ent, coiled polyethylene tubes arranged around an open at an optimum angle facing the sun [54, 10].
circular framework [47, 48]. Other variants of tubular Flat plate bioreactors, first described by Samson and Leduy,
photobioreactors exist such the conical helical tubular were illuminated by fluorescence lamps on both sides and agitated
photobioreactor (CHTP) [49, 50], which has been used to by aeration [55]. Tredici et al. further developed the idea by
mass culture Chlorella sp. with the productivity per installation fabricating the photobioreactors from commercially available
area of 26.6 g (m2 d) 1 in a single basic unit and 31.0 g panels of transparent sheets partitioned to form a rigid alveolar
(m2  d) 1 in a four-unit system [50]. panel [56]. The flat inclined modular photobioreactor (FIMP), a
Tube diameter is limited (generally 0.1 m). Increasing tube tilted flat plate photobioreactor, was angled to provide maximum
diameter results in a decrease in the surface/volume ratio, and exposure of the culture to solar irradiance as well as for substantial
this factor has a strong impact on the culture. As the algae control of temperature. This type of flat plate reactor was also
grow and increase in density, they begin to shade one another
and this translates to a volumetric reduction in biomass per
unit of incident light [32].
The tube length, on the other hand, mainly influences the
circulation of the cultivation medium inside the reactor, i.e.
the residence time [51]. Scaling up a tubular photobioreactor
hypothetically can be achieved by either increasing the length
or diameter of the tube [40, 44]. As mentioned above, increase
in diameter is not desirable, however, there are also limitations
to increasing the length of the tubes. Tubes that are too long
allow the O2 produced by photosynthesis to accumulate,
thereby possibly exceeding that of air saturation, and this in
turn can inhibit photosynthesis via mechanisms previously
described [22]. Indeed oxygen concentrations above 35 mg/L
are toxic to most microalgae [10].
In long tubes, a decreasing CO2 gradient will also become
established between gas entry and exit leading to depletion Figure 2. Scheme showing solar orientation of a flat-plate
before exit, thereby starving some algae for carbon. Such a photobioreactor system for outdoor culture [62].

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
182 L. Xu et al. Eng. Life Sci. 2009, 9, No. 3, 178–189

made of transparent glass glued with silicon rubber so that the light [63]. In contrast Spirulina plufensis grown in a flat plate photo-
path of the flat plate photobioreactor can be easily changed [57]. bioreactor decreased from 51.1 g m 2 day 1 to 33.6 g m 2 day 1
By maintaining a high optimum culture density of 4g L 1, the in areal productivity as the light path increased from 1.3 cm to
FIMP enhanced the eicosapentaenoic acid productivity of Monodus 10.4 cm [57]. Each microalgal culture appears to have an opti-
subterraneus to 58.9 mg (L  day) 1 [58]. However, scale up was mum light path that is a compromise between the growth inhi-
difficult. To achieve maximum productivity, a 35% enhancement bition in deep layers due to insufficient illumination and the light
compared to the vertical system, the tilt angle had to be adjusted inhibition or saturation effect in superficial layers. Furthermore,
four times a year [59] and this increased operation costs. Even if a there is a conflict between biomass concentration and light
fixed tilt angle was instead used, the higher capital cost of the tilt penetration and thus the light path is also limited by biomass
design did not compensate for the 17% increase in productivity of concentration.
Spirulina platensis [60]. Flat plate photobioreactors are used for mass production of
For the above reasons, horizontal and vertical flat plate microalgae in outdoor and indoor culture systems because of
photobioreactors were more commonly used for the cultivation advantages including high illumination surface area, low
of microalgae. A vertical system requires proper solar orientation accumulation of dissolved oxygen compared to horizontal
to maximize irradiance. When compared to an east/west orien- tubular photobioreactors and due to their modular design
tation, the decrease in irradiance from top to bottom of the convenience in scale-up. Doucha et al. [64] described an
channels was less than for a north/south orientated flat plate optimized large-scale flat plate photobioreactor module of
reactor (Fig. 2). Algal cultures also grew better in the north/south 1000 m2, and one commercially available flat plate photo-
orientated system [61]. As an apparent contradiction to this bioreactor has a reported capacity of 6000 L [31, 61].
finding, however, Kurano and Miyachi obtained higher algal Although high biomass concentrations (480 g L 1) can be
growth when they placed their flat plate reactor in the east/west reached in narrow light path flat panels [65], there are some
orientation [62]. These apparently conflicting studies were limitations. There is some degree of algal wall adhesion; there is
recently explained by Sierra et al. Solar radiation increases with potential for high stress damage associated with aeration; systems
respect to the earth’s latitude. The east/west orientated flat plates are not amenable to sterilization; and they are incompatible with
intercept more solar radiation than the north/south for latitudes off the shelf industrial fermentation equipment [19, 60, 61].
above 351N, while for latitudes below 351N to the equator, the Temperature control is also a problem and sprinkler systems are
result is the reverse [60]. often used for evaporative cooling [57]. A recent study provided an
In vertical flat plate photobioreactors there are some added alternative remedy for temperature control by using a heat
benefits with regard to light [57, 60, 61, 63]. For example, the exchanger consisting of stainless steel tubes located inside the flat
proportion of microalgal productivity attributed to diffuse and/or plate reactor [60]. The overall heat transfer coefficient for the
reflected radiation (62%) was larger than that of direct radiation internal heat exchanger was much higher than that between the
(38%) [57]. The amount of light per unit volume is determined culture and the external environment, with maximal values of 505
by the penetration depth of the incident light path of a plate and 37 Wm 2 K 1, respectively [60]. To attain the same mass
system, but is variable with algal species. For example, volumetric transfer capacity, the power supply of 53 Wm 3 for the flat
(g L 1 day 1) productivity of Nannochloropsis sp. increased47 plate reactor [60] was much lower than the 2000–3000 Wm 3 [41,
fold when the light path was decreased from 17 to 1.3 cm, with 42, 66] required for tubular photobioreactors. Unfortunately it was
peak areal (g m 2 day 1) productivity at a light path of 10 cm still higher than the 40 W m 3 needed in bubble columns [67].

A B
PFD
Liquid flow

Air / CO2
Figure 3. Schematic of airlift photobioreactor (A) and growing microalgal cultures in these airlift reactors (B). PFD, photon flux density.

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Eng. Life Sci. 2009, 9, No. 3, 178–189 Microalgal Bioreactors 183

3.3 Airlift and bubble-column photobioreactors and downcomer column) [70]. In this system, a capillary sparger
was used to provide a swirling motion to minimize cell adhesion
Airlift and bubble-column bioreactors are simple devices that to the wall with an effect similar to the previously described
have been used in bioprocessing, wastewater treatment, and helical flow promoter in an airlift reactor [70, 76]. This modular
the chemical process industry. These vertical column photo- design facilitated easy, long term operation and a 120-L prototype
bioreactors are compact, low-cost, and easy to operate axeni- has been implemented for microalgal production in a commercial
cally [68, 69]. Pneumatically agitated bubble columns and hatchery.
airlift devices attain the requisite mass transfer coefficient of Considering the high mass transfer, low energy costs, and
0.006 s 1 and liquid circulation velocity at a relatively low extremely low physical stress, some bubble column photo-
power input for practicable culture of microalgae [69, 70]. bioreactors are equipped with a rubber membrane diffuser or
Camacho et al. reported that the maximum biomass volu- dual spargers to improve the mass transfer of gases: provision of
metric productivity of Phaeodactylum tricornutum obtained in CO2 and removal of O2 [78, 79]. In the case of dual sparging, the
vertically oriented concentric-tube airlift photobioreactors efficiency of CO2 transfer increased fivefold relative to that of
(ALP) was about half of that obtained by a horizontal-loop conventional sparging [79]. Bubble size, however, apparently is
tubular photobioreactor (HLTP) [71]. A similar result was also crucial for minimizing shear damage to cells. When Rocha
obtained in a bubble column, where the volumetric biomass et al. grew Nannochloropsis gaditana using small vs. large
productivity was about 60% of that in HLTP for Phaeodacty- bubbles, they found better algal growth with larger bubbles and as
lum tricornutum grown under identical conditions [43]. air flow rate (vvm) was increased the cells suffered more shear
Compared to bubble column photobioreactors, air-lift with smaller vs. larger bubbles [80]. Berberoglu et al. recently
photobioreactors (Fig. 3) showed superior growth of micro- used Mie theory and experimental data to show that bubbles may
algae. At a low aeration rate of 1 L min 1, cultures of Undaria also offer an advantage. Bubbles produced via sparging of
pinnatifida and Porphyridium Sp. grown in an airlift reactor Anabaena variabilis appeared to increase light penetration into a
attained 3350% higher growth rates than when grown in a culture by up to 20% as a result of light scattering [81]. It is,
bubble column [72, 73]. Diatom yields were also about double therefore, probably wise to measure the effect of bubbles on each
in an airlift device than in a bubble column [74]. It appears species of alga being grown in air sparged reactors.
that, in contrast to a bubble column where cell flow patterns Aeration rate is restricted by considerations of shear sensitivity.
are more random, the airlift system produces a more homo- There is an upper limit on the acceptable level of turbulence,
geneous flow pattern that moves cells from dark (riser) to light because algal species are affected differently by hydrodynamic
(downcomer) zones [75]. Thus, cells in a bubble column may stress [69, 82]. Generally, increasing aeration rate increases
reside in high or in low light intensities for a long time without mixing, liquid circulation, and gas-liquid mass transfer in bubble
circulation. Furthermore, cell sedimentation occurred in the column and airlift reactors. While a high superficial gas velocity
bubble column while cells remained more uniformly suspen- increases mixing, it also aids in preventing oxygen accumulation
ded in the medium of the airlift photobioreactor [72, 75]. and provides good gas-liquid mass transfer for efficient use of
When large-scale diatom cultivation was compared in both CO2 [69]. Not surprisingly some microalgal species also suffer
bubble column and airlift photobioreactors, there was no negative effects from an increase in superficial gas velocity due to
significant different in the specific growth rate, which was the high shear stress caused by high aeration rate. For example,
2.46  10 2 h 1 and 2.58  10 2 h 1 for bubble column and when Haematococcus pluvialis was cultivated in an airlift bior-
airlift reactor, respectively [74]. This may be the result of the eactor with different superficial gas velocities, results indicated
non-ideal flow pattern in the airlift system and the internal that the maximum cell density declined to about 10% of the
circulation within the riser itself. optimum level when the velocity was increased from 0.4 cm s 1
One of the costs of growing algal cultures in airlift and to 3 cm s 1 [75]. This was likely from the higher shear stress on
bubble column reactors is that of the added gases. Merchuk H. pluvialis as the gas flow rate was increased, and probably
et al. compared Porphyridium culture in an airlift photo- resulted in cell damage. It was determined that shear stress varied
bioreactor with that in a bubble column reactor. By adding a in the airlift with the radius of the culture column and increased
helical flow promoter to the airlift system, the cost of gases with respect to the superficial gas velocity in the riser; in the
for the production per kg microalgal biomass was 50% of that downcomer, however, shear was quite uniform and much lower.
in the bubble column to achieve the same specific growth High shear stress also was observed in the top and bottom regions
rate [76]. of an airlift bioreactor, and changing the size of the top and
Bubble column and airlift photobioreactors are also used for bottom clearance greatly altered the flow structure and shear
microalgal production in aquaculture. A new bubble column stress in these regions [83]. These changes may significantly affect
design using PVC bristles to help dislodge the adhesive diatom airlift bioreactor performance, particularly in applications invol-
being cultivated resulted in algal biomass increasing 20% ving stress sensitive microalgae.
compared to growth in a bubble column without bristles [77]. Vertical column photobioreactors, especially the airlift
This modification will likely prove useful for the mass production photobioreactor, possess some advantages for microalgal
of other microalgae that are highly adhesive. Another photo- cultivation: no moving parts, low power consumption, high
bioreactor design that uses an external loop airlift with a swirl mass transfer rate, good solids suspension, homogeneous
flow has been reported for continuous microalgal production. shear, rapid mixing, and with the vertical orientation, less land
This system consists of a succession of modules, each one being is required [71, 84, 85]. With scale-up, however, penetration of
composed of two vertical interconnected columns (riser column light into the reactor decreases exponentially with distance

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
184 L. Xu et al. Eng. Life Sci. 2009, 9, No. 3, 178–189

from the light source [86] and may pose a problem when these reactor designs and this depends in part on developments
scaling-up these bioreactors. Like tubular reactors, increasing in material science.
the diameter of the column has limitations. Large-scale The idea of placing a light source inside the cultivation
outdoor culture of Phaeodactylum tricornutum in bubble vessels has been repeatedly exploited by researchers. A photo-
columns showed that the optimal dimensions of vertical bioreactor using three concentric glass cylinders, with a light
column photobioreactors are about 0.2 m diameter and 4 m source mounted on the axis within them was described by
column height [43]. In addition to considerations of space Tsygankov [91], where Rhodobacter capsulatus was grown in the
demands and ease of cleaning, an optimum column diameter device at biomass concentrations up to 550 mg L-1 without light
must be determined as a compromise between productivity limitation. Patino et al. further investigated the growth of
and capital cost [70]. Chlorella vulgaris using an internal light source from either a
150-W xenon lamp or a fluorescent flat lamp fitted into a special
housing (Oriel, 60100) [92]. A cooling system and easy orien-
3.4 Stirred tank reactor tation of the light was provided by an F/4.4 ellipsoidal AlMgF2
reflector. As mentioned previously, optical fibers have also been
Stirred tank reactors (STR) were originally proposed to grow used to collect and distribute solar and artificial light into stirred
microalgae photoautotrophically using artificial light sources or tank photobioreactors [93] and have been used for mass culti-
sun light mainly because the STR was an industry and labora- vation of microalgae including Chlorella sorokiniana, C. vulgaris,
tory standard [31, 87, 88]. As an example, a Hydraulically and Phaeodactylum tricornutum [94–96]; a cell density of l09
Integrated Serial Turbidostat Algal Reactor (HISTAR) system, cells mL 1 (30 g L 1) for C. vulgaris was achieved [96].
which had a total volume of 3.6 m3, was used to grow Sele- Although optical fiber assisted internal-illumination is a
nastrum capricornutum Printz. HISTAR consisted of two sealed promising technology for providing light in closed photo-
turbidostats and a series of open, hydraulically connected, bioreactors, low efficiencies in light delivery via optical fibers
continuous flow stirred-tank reactors (CFSTRs). The CFSTRs has been reported;450% of the light was lost in transport
functioned as a biomass amplifier of the inoculated culture [89]. through the fibers [94]. The major advantages of using optical
This system was recently used to establish a deterministic model fibers for internally-illuminated photobioreactors are that they
to predict microalgal productivity in order to establish practical can be heat sterilized and are stable to the mechanical agitation
feasibility for large scale application; however, subsequent methods used in a conventional stir tank. Although adding
implementation has not yet been reported. considerably to capital costs, use of optical fibers for illumi-
nation allows for scale-up while maintaining an efficient light
supply and constant productivity [94, 99].
4 Approaches for lighting photobioreactors
The outermost layer of algae in the reactor can at times have so 5 Scaling up
much light that growth is photo inhibited. On the other hand,
the innermost layer of algae might not have enough light Biomass productivities per area in reported photobioreactors
because of self-shading and, this reduces the volumetric are limited by suboptimal circumstances in the reactor, limit-
biomass productivity per unit of incident light. Thus, efficient ing biological efficiency, or by a suboptimal design limiting
use of light in the culture is a major constraint in photo- light supply into the reactor. Design and scale-up methodol-
bioreactors and makes their scale-up difficult. A number of ogies for photobioreactors still have to be improved to achieve
different options have been studied to improve light penetra- efficient light provision, minimize carbon dioxide losses, and
tion and control in photobioreactors. ensuring efficient mixing and removal of photosynthetically
It is possible to enhance light intensity into a reactor by generated oxygen [21, 100, 101]. Among the closed photo-
using an irradiance oriented (tilted) type of culture system or bioreactors, the tubular and flat plate designs have been
by using optical fibers for added internal-illumination. The tilt applied in large-scale microalgal cultivation while the bubble
flat plate photobioreactor has succeeded in some microalgal column is more widely used in aquaculture. Although the
cultivations with higher cell densities than that of a vertical flat airlift photobioreactor showed prior performance in algal
plate [57–59]. However, the tilt system seems difficult to scale- culture than the bubble column, no significant difference was
up due to its complex operation and higher cost, which do not observed in large-scale culture. Thus, the challenge is to also
compensate for increases in productivity [60]. develop effective scale-up methods to enable large scale
Recently, the Green Solar Collector (GSC), a light-and area- photobioreactors to function as well as at the laboratory scale.
efficient photobioreactor with light redistributing plates and Computational fluid dynamics (CFD) can be used to
external light collection, was introduced for microalgal optimize the structural configuration of photobioreactors for
production [90]. It increased light capture efficiency by 57% scale-up. By using principles of fluid dynamics the cost,
except in winter. However, the production costs of the GSC are workload, and design period can all probably be reduced. Yu
expected to be higher than those of conventional outdoor et al. recently applied CFD methods to the inner structure
photobioreactors, such as horizontal and vertical tubes or parameter optimization of an airlift flat-panel photobioreactor
vertical panels, even despite ease of construction and main- through a volume increase from 15 L to 300 L [102]. A model
tenance and the use of cheap materials (PMMA) in GSC. was developed to predict algal cell growth and then experi-
Therefore, economy of scales may significantly reduce costs of mentally confirmed.

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Eng. Life Sci. 2009, 9, No. 3, 178–189 Microalgal Bioreactors 185

Modularization is another option for scale-up. The wider tubular reactors, deeper ponds, etc., with an anticipated
advantage to this approach is the use of a relatively small scale reduction in cost.
reactor where light limitations, carbon dioxide losses, and Metabolically engineered algae are also likely candidates for
inefficient mixing can be minimized or even eliminated. culture in photobioreactors with some potential for impacting
Furthermore, a modular system provides redundancy; if one reactor design, but this mainly depends on the product being
module becomes contaminated or suffers a mechanical produced. For example, Spoehr and Milner first showed that
problem, the entire process is not lost. Recently, a 120-L nitrogen starved Chlorella were able to produce up to 85% of
multimodule photobioreactor, consisting of 18 elementary their biomass as lipids, and many other algae show a similar
modules each with a 6.1 L working volume was commercialized response [7]. Using this type of algae for biofuel production
[70]. Although this is much too small a capacity for some might thus, require a two step process: rapid growth in
products like biofuels, it is reasonable for high value products medium replete with nitrogen, followed by a second step in
like therapeutics. Further developments in scaling to nitrogen deficient medium where growth essentially stops, but
large, reliable systems depend on continued research in algae shift into lipid metabolism. One remedy would be to use
photobioreactors and a break-through in the design of culture two reactors in series to accommodate fuel production. On the
systems, where high photosynthetic efficiencies and effective other hand, a metabolically engineered alga that constitutively
mass transfer are possessed and maintained in large scale and produces high levels of lipids would require only 1 reactor, and
at high light intensities during long term operation. if coupled with a modified LHCII the reactor could also be
designed with a longer light path.
Clearly one of the nontechnical implications of using trans-
6 The role of transgenic algae in genic algae is that of public and environmental concerns about
photobioreactor operation the safety of growing huge volumes of genetically modified cells
especially in outdoor reactors. Given the current at best tepid
Until recently the potential for using transgenic algae for over public acceptance of genetically modified crops, one must assume
production of useful compounds has not been realistic. that similar resistance may be encountered towards large outdoor
Recently, however, methods for obtaining stable transformed algal cultivation systems. Use of transgenic algae, therefore, may
algal lines are now much better developed [103] and have led preclude use of open ponds and instead mandate focus on either
to speculation that a number of interesting algal species can outdoor or indoor fully enclosed photobioreactors. Indeed use of
now be metabolically engineered to produce nutraceuticals, closed systems would help to defuse public concerns, but such
pharmaceutical proteins, and lipids and hydrocarbons systems would likely be expected to follow the guidelines expected
for biofuels [1, 104, 105]. Consequently, it is important to of any released genetically modified species. Although it would
consider how genetically altered microalgae might impact not impact actual photobioreactor design, the overall system
photobioreactor design and operation. Some interesting recent would probably have to also include spill containment technology
results provide insight on how reactor design might have to be to preclude escape of any transgenic alga into the environment
changed. and water systems.
As described earlier, one of the drawbacks to growing
microalgae in outdoor systems is their photoinhibition by high
light intensity. Recent work by Mussgnug et al. (2007) has 7 Conclusions
focused on altering the light harvesting complex (LCHI and
LHCII) of photosystems I and II (PSI and PSII), respectively, Of the many types of culture systems proposed for microalgal
to minimize this problem [106]. Using Chlamydomonas rein- culturing, open pond systems have dominated. However, during
hardtii, they employed RNAi technology to down regulate the the past decades, great progress has been made in bioengineering
expression of the light harvesting complex (LHC) proteins. and biotechnology for efficient microalgal mass production.
Compared to wild type, the genetically altered algal strain, Thus, several types of closed culture systems, such as tubular or
Stm3LR3, showed about a 30% improvement in photo- flat plate photobioreactors show promise for application in large
synthetic efficiency. Although photon conversion into chemical scale microalgal culture for bioenergy, aqua- and agricultural
energy can be inefficient, of primary concern here is uses. Difficulties arise with scale-up because relative volumes of
that at high light intensities, the cells nearest the wall of light and dark zones change as the tube diameter or the plate
the reactor receive such high light intensity that they become thickness increases and the large area of land required. New
photoinhibited and can waste up to 90% of the incident developments in lighting and its control and in scale-up are
light energy as fluorescence and heat [106]. Cells behind the needed to make closed culture systems cheaper, controllable and
surface cells, therefore, receive decreased amounts of light not more efficient. The future of microalgal biotechnology appears
only from this wasted energy, but also from shading. While promising, and innovative processes and products are expected to
mixing helps to establish more homogeneity to obviate the emerge over the next few years.
latter, the overall efficiency of the reactor is greatly impaired.
By reducing the sensitivity of PSII to high light intensity,
less of the incident light energy is wasted, so there is better Acknowledgements
light penetration into the reactor. With greater light penetra-
tion, it would be possible to increase the depth of the culture This work was financially supported in part by the National
and this could result in use of larger reactor volumes, e.g. Basic Research Program (973 Program) of China

& 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim http://www.els-journal.com
186 L. Xu et al. Eng. Life Sci. 2009, 9, No. 3, 178–189

(No.2007CB714301) and the Knowledge Innovation Program [18] O. Pulz, Photobioreactors: production systems for photo-
of the Chinese Academy of Sciences (No. KGCX2-YW-337). PJ trophic microorganisms, Appl. Microbiol. Biotechnol. 2001,
Weathers is partially supported by a US Department of Energy 57, 287–293.
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mass cultivation of algae, Bioresour. Technol. 2008, 99,
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Conflict of interest [20] K. Marxen, K. H. Vanselow, S. Lippemeier, R. Hintze,
A. Ruser, U. P. Hansen, A photobioreactor system for
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Phycol. 2005, 17, 535–549.
[21] E. M. Grima, F. G. A. Fernandez, F. G. Camacho, Y. Chisti,
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