An Outlook on Microalgal Biofuels

René H. Wijffels and Maria J. Barbosa

Science 329, 796 (2010);
DOI: 10.1126/science.1189003

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6. A. Uslu, A. P. C. Faaij, P. C. A. Bergman, Energy 33, 1206 17. E. Searcy, P. C. Flynn, E. Ghafoori, A. Kumar, 31. M. Gronalt, P. Rauch, Biomass Bioenergy 31, 393
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PERSPECTIVE
power plants. In Japan, the government financed
a large research project entitled “Biological CO2

An Outlook on Microalgal Biofuels

Fixation and Utilization” from 1990 to 1999 (3).
These programs yielded some successes—such as
promising lipid production strains, open produc-
tion systems (raceway ponds), and principles for
René H. Wijffels1 and Maria J. Barbosa2
photobioreactor design (the use of fiber optics to
bring light inside the systems)—that are still the
Microalgae are considered one of the most promising feedstocks for biofuels. The productivity focus of research today, but none has proven
of these photosynthetic microorganisms in converting carbon dioxide into carbon-rich lipids, only a economical on a large scale.
step or two away from biodiesel, greatly exceeds that of agricultural oleaginous crops, without competing There have been several critical issues that
for arable land. Worldwide, research and demonstration programs are being carried out to develop the combined have had a large influence on stim-
technology needed to expand algal lipid production from a craft to a major industrial process. Although ulating the resurgence of algal biofuels research.
microalgae are not yet produced at large scale for bulk applications, recent advances—particularly in The world has experienced record crude oil prices,
the methods of systems biology, genetic engineering, and biorefining—present opportunities to increasing energy demand, and environmental
develop this process in a sustainable and economical way within the next 10 to 15 years. concerns that have pushed biofuels research in
general to the fore. In the narrower context of
he concept of using algae to make fuels

T was already being discussed 50 years ago

(1), but a concerted effort began with the
oil crisis in the 1970s. Large research programs
in Japan and the United States focused on devel-
oping microalgal energy production systems. From
1978 to 1996, the U.S. Department of Energy’s
Office of Fuels Development funded a program to
develop renewable transportation fuels from algae
(2). The main focus of the program, known as the
Aquatic Species Program (ASP), was the produc-
tion of biodiesel from high-lipid-content algae
grown in ponds, using waste CO2 from coal-fired
Imax: 1800 µmol photons m-2 s-1 Imax: 400 µmol photons m-2 s-1
1 (direct sunlight) (diluting effect)
Wageningen University, Bioprocess Engineering, Post Office Box
8129, 6700 EV Wageningen, Netherlands. 2Wageningen Uni-
versity and Research Center, Food and Biobased Research, Post
Office Box 17, 6700 AA Wageningen, Netherlands. E-mail: Fig. 1. The principle of light dilution. The light intensity (I) striking closely spaced vertical panels is much
[email protected] (R.H.W.); [email protected] (M.J.B.) lower than the intensity striking a horizontal reactor on the same surface.

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 SPECIALSECTION
biofuels, the food versus fuel debate and research portfolio should cover the
a virtual explosion in biotechnology re- whole chain of process development in
sulted in a substantial commitment to the an integrated and iterative way, including
development of algal biofuels by the in- fundamental biology, systems biology,
dustrial and governmental sectors. The re- metabolic modeling, strain development,
cent investments in microalgae for fuels bioprocess engineering, scale-up, biore-
are well justified by the potential that these fineries, integrated production chain, and
microorganisms offer through their high- the whole system design, including logis-
er lipid productivities per ground area than tics (14). The main objective is to reduce
oleaginous agricultural crops, as well as production costs and energy requirements
lack of competition for arable land. while maximizing lipid productivity and
Faced with stresses such as nutrient to increase the biomass value by making
deprivation, algae store chemical energy use of all algal biomass components. For
in the form of oils such as neutral lipids or cost and energy reduction and maximi-
triglycerides (4). The algal oil can be ex- zation of lipid productivity cell proper-
tracted from the organisms and converted ties, bioreactor design, efficiency in
into biodiesel by transesterification with supply, and use of nutrients and resources

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short-chain alcohols (5) or by hydrogena- need to be improved, and to make use of
tion of fatty acids into linear hydrocar- all biomass ingredients, a biorefinery
bons (6). Algae also synthesize other fuel infrastructure needs to be established.
products, such as hydrogen (7), ethanol In microbial fermentations, substan-
(8) and long-chain hydrocarbons, that re- tial improvements in productivity have
semble crude oil (9), or the algal biomass been obtained through both technolog-
can be converted to biogas through an- ical (reactor design, process control,
aerobic fermentation (1). harvesting, and extraction) and strain im-
Despite this potential, the production provements. As an example, the present
capacity for microalgae is presently lim- productivity of penicillin synthesis by
ited in comparison to land-based energy fungi is 5000 times as high as it was 50
crops. The current worldwide microalgal years ago (15). Commercial production
manufacturing infrastructure (producing of microalgae is still based on traditional
the equivalent of ~5000 tons of dry algal technologies using a few strains. There
biomass) is devoted to extraction of high- are many more species yet to explore; in
value products such as carotenoids and addition, genetic engineering offers the
w-3 fatty acids used for food and feed possibility for strain improvement. High
ingredients. The total market volume is lipid productivity is essential for the com-
€1.25 billion, implying an average market mercial production of biodiesel from mi-
price for microalgae of €250/kg dry bio- croalgae. In nonstressed growing algae,
mass (10). As an example for compari- lipids are mostly present in the form of
son with land-based oleaginous crops, the phospholipids in the cell membranes.
world production of palm oil is nearly 40 Some microalgae, when exposed to stress
million tons, with a market value of conditions (e.g., nutrient deprivation or
~ 0.50 €/kg (11). high light intensities), accumulate lipids
Production of microalgae for biofuels in the form of triacylglycerols in so-called
needs to take place on a much larger oil bodies. This accumulation occurs at
scale at much lower costs. If all transport the expense of energy used for growth,
fuels were to be replaced by biodiesel in leading to a decrease in growth rate and
Europe, there would be an annual need a consequent decrease in productivity.
for nearly 0.4 billion m3 (12). If this bio- Knowledge of the biosynthesis mecha-
diesel were to be supplied through micro- Fig. 2. Development of low-cost photobioreactors. Flat-panel reac- nism of triacylglycerols and their accu-
algae, 9.25 million ha (almost the surface tors from (A) Proviron, Belgium [reproduced with permission from mulation in oil bodies is limited and often
area of Portugal) would be needed to (29)], (B) Solix Biofuels, USA (reproduced with permission from Bio- based on analogies with higher plants
supply the European market, assuming a mass Magazine), and (C) Green Wall Panel reactors from Fotosintetica (4). If the mechanism were known, it
productivity of 40,000 liters per ha per & Microbiologica S.r.l., Italy. could open the possibility of inducing lipid
year. This productivity is based on a 3% accumulation in oil bodies without having
solar energy conversion to biomass (theoretical between researchers in the field over technology to apply a stress factor. More broadly, detailed in-
maximum is 9%) and a biomass oil content of readiness and the prospects for productivity en- sight into metabolic pathways may lead to strat-
50%, under the solar conditions of Portugal. A leap hancement, with some parties pressing for scale-up egies to induce lipid accumulation based on process
in the development of microalgae technology is and commercialization now, while others cautious- conditions, defined nutrient regimens, and/or the
therefore required; on a practical level, the scale ly stress the need for additional research leading to use of metabolic engineering techniques. For this
of production needs to increase at least 3 orders of more careful step-by-step development (13). purpose, well-annotated genomes need to be
magnitude, with a concomitant decrease in the cost We believe a multidisciplinary approach will available.
of production by a factor of 10. In the past few be required to realize the full potential of micro- There are still very few algae for which full
years, there has been a rather polarized debate algae as a biofuels feedstock. A comprehensive or near-full genome sequences have been obtained

www.sciencemag.org SCIENCE VOL 329 13 AUGUST 2010 797

 Scaling Up Alternative Energy
be reduced considerably. Microalgae can also be
grown on seawater; even deserts would be suit-
able if there is access to salt aquifers. Growth
could also take place in confined systems on large
water surfaces such as lakes or seas, assuming
there is adequate protection from the wind.
The production of large quantities of biomass
also requires a large amount of CO2. A total of
1.8 tons of CO2 is needed to produce 1 ton of
algal biomass (25). This means that 1.3 billion
tons of CO2 would be required for the production
of 0.4 billion m3 of biodiesel to supply the Euro-
pean transportation market. The European Union
produces about 4 billion tons of CO2, (26) so
production of microalgae could go some way
toward relieving this CO2 excess. However, the
distance across which CO2 may need to be

Downloaded from www.sciencemag.org on May 18, 2012

transported in this context is a matter of concern.
The main nutrients needed for the production
of microalgae are nitrogen and phosphorus. The
biomass of the algae consists of 7% nitrogen and
1% phosphorus. Consequently, for the European
biofuel market ~25 million tons of nitrogen and 4
million tons of phosphorus are needed. This is
Fig. 3. The ideal photosynthetic cell factory for production of biofuels. about twice the amount that is presently produced
as fertilizer in Europe (27). For sustainable pro-
[e.g., Chlamydomonas reinhardtii (16), Thalassiosira This can be done by stacking the reactor units duction of biodiesel from microalgae, it will be
pseudonana (17), and Phaeodactylum tricornutum vertically (Fig. 1): Narrow spacing in the stacks important to make use of residual nutrient sources
(18)], and transfection systems have barely been minimizes loss of light to the ground surface (21). (about 8 million tons of nitrogen in Europe) and to
developed. Currently, there are about 10 differ- However, if not combined with a short light path, recycle nutrients as much as possible.
ent algal species that can be transformed (19). this setup leads to voluminous reactor systems After production, the biomass needs to be
However, sophisticated metabolic engineering, with low volumetric productivity and low harvested, the lipids extracted, and the remain-
whereby several genes are overexpressed or biomass concentration (23). To reduce investment ing cell components recovered. Harvesting of
down-regulated in a single organism, is currently costs of these systems, vertical panels can be microalgae is currently expensive because of
only really possible with C. reinhardtii. We expect made from thin plastic films such as polyethylene the high energy requirements and capital costs
that the genome of more algal strains will be (Fig. 2). There are examples of thin film systems involved. Because most microalgae are small
sequenced in the near future, due to the present submerged in large water volumes for good tem- individual cells, centrifugation is often used as a
high interest in the field, enlargement of the perature control and a lower associated energy preferred harvesting method. However, as the
scientific community, and the availability of fast requirement for cooling (14). We expect that in biomass concentration is generally low (<3 g/L),
and reliable technologies for genome sequencing. the coming years many systems will be devel- centrifugation of diluted streams requires a large
The main inputs required in addition to the oped based on these design principles (Fig. 2). capacity of the centrifuge, which makes the pro-
algae themselves are sunlight, water, CO2, ni- Improvements are to be expected in material cess energy-demanding and expensive. Floccula-
trogen, and phosphorus. Large-scale cultivation lifetime (polyethylene has a lifetime of ~1 year), tion, followed by sedimentation and flotation,
of microalgae for biofuel production must be ease of cleaning, and energy requirements (for before centrifugation or filtration will substantially
based on sunlight as the sole source of light en- example, the energy requirement for cooling can reduce harvesting costs and energy requirements.
ergy. Especially when working in summertime, be further reduced by reflecting the near-infrared Ideally, algae would flocculate spontaneously at
and/or when working at lower latitudes, sunlight portion of the light incident on the reactor sur- a certain stage of the process. After harvesting,
intensities are high and often oversaturate the face, which otherwise heats the system without the oil needs to be extracted. The cells are first
photosynthetic cycle, limiting growth and lead- contributing to photosynthesis). disrupted, and then the oil can be extracted with
ing to a drop in productivity. In recent years, much Water usage is another important parameter. organic solvents or with more environmentally
effort was put into increasing photosynthetic For the production of 1 liter of biofuel from fuel benign, but more expensive, solvents (e.g., super-
efficiency of microalgae under oversaturating crops, approximately 10,000 liters of water are critical CO2). Most microalgae strains are, in
light (the normal condition on a sunny day) by needed (24). Microalgae need much less water. general, relatively small and have a thick cell
developing new strains with smaller antenna sizes For photosynthesis alone, ~0.75 liter of water is wall. For this reason, very harsh conditions need
(20) and by decreasing the light path of photo- needed per kg of biomass produced (25). Per liter to be used (e.g., mechanical, chemical, and phys-
bioreactors while increasing mixing (turbulence) of biofuel, assuming a lipid content of 50%, 1.5 ical stress) to break the cells for extraction of
in high cell density cultures (21, 22). Turbulence liters of water are required. In practice, water use the products, which may affect the functional-
requires high energy input and therefore is not in production systems is much larger because ity of cell compounds like proteins. Excretion of
suitable for large-scale production of biofuels water is also used for cooling closed systems, the oils, in a manner similar to what naturally
from microalgae. One strategy to obtain high and fresh water needs to be added to open ponds occurs in the microalgae Botryococcus braunii,
photosynthetic efficiencies under bright sunlight to compensate for evaporation. If closed sys- will lead to a simplified biorefinery and improve
in systems with lower energy requirements is to tems are used and cooled with a large saltwater the downstream economics. However, it will not
reduce the light intensity at the reactor surface. buffer via heat exchangers, freshwater usage can provide a complete solution because the remaining

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 SPECIALSECTION
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longer be necessary. If strains are developed that
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limited and degassing is no longer required. 16. S. S. Merchant et al., Science 318, 245 (2007). in collaboration with industry, Wageningen UR has been
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and feed ingredients. Despite algae’s high suit-
ability for biorefining due to the varied composi-
tion of its biomass, the coproduction of multiple REVIEW
products from microalgae remains a challenge.
Research is needed to explore mild cell disrup-
tion, extraction, and separation technologies that Generating the Option of a
Two-Stage Nuclear Renaissance
retain the functionality of the different cell com-
ponents (e.g., proteins, carbohydrates, w-3 fatty
acids, pigments, and vitamins). Biorefining is
important not only for cost efficiency but also Robin W. Grimes1 and William J. Nuttall2
for the supply of food compounds. The algal bio-
mass that could theoretically supply 0.4 bil-
lion m3 of biodiesel to the European market Concerns about climate change, security of supply, and depleting fossil fuel reserves have spurred a
consists of 40% protein; thus, the total amount revival of interest in nuclear power generation in Europe and North America, while other regions continue
of protein produced as a by-product would ex- or initiate an expansion. We suggest that the first stage of this process will include replacing or extending
ceed 0.3 billion tons. This is about 40 times as the life of existing nuclear power plants, with continued incremental improvements in efficiency and
much as the amount of soy protein (18 million reliability. After 2030, a large-scale second period of construction would allow nuclear energy to
tons of soy beans with ~40% of proteins in 2008) contribute substantially to the decarbonization of electricity generation. For nuclear energy to be
presently imported into Europe (11). Therefore, sustainable, new large-scale fuel cycles will be required that may include fuel reprocessing. Here,
the production of microalgae for fuels would we explore the opportunities and constraints in both time periods and suggests ways in which
place no pressure on the availability of rich ag- measures taken today might, at modest cost, provide more options in the decades to come. Careful
ricultural areas for production of proteins; on the long-term planning, along with parallel efforts aimed at containing waste products and avoiding
contrary, there is even the possibility of an over- diversion of material into weapons production, can ensure that nuclear power generation
production of proteins. remains a carbon-neutral option.
In closing, we reiterate our belief that 10 to
15 years is a reasonable projection for the de- n North America and Europe, the develop- technology on two time scales (Fig. 1): first, those
velopment of a sustainable and economically
viable process for the commercial production of
biofuels from algal biomass. It is important that
I ment of nuclear power stalled after the March
1979 Three Mile Island accident in Pennsyl-
vania, and until recently the building of addition-
of immediate concern and consequence, and sec-
ond, matters that will dominate in the longer term
(beyond about 2030), when nuclear development
further technology development be done in close al nuclear reactors was not likely. Yet today, a could once more stall. The immediate future also
collaboration with environmental scientists. The nuclear renaissance is underway, and globally 52 indicates continued growth of nuclear energy in
production processes should be subjected to life- reactors are under construction (1). How nuclear the Middle East, East Asia, South Asia, and
cycle analysis (28) and monitored for their im- energy found itself in a state of decline is well elsewhere.
pact on biodiversity. documented. Will it continue to move forward If the global electricity system is to be large-
and avoid another collapse? ly decarbonized over the first half of this century,
References and Notes
1. W. J. Oswald, C. G. Golueke, Adv. Appl. Microbiol. 2, 223
In this article, we assess technological re- then two key challenges must also be surmounted.
(1960). sponses and opportunities for nuclear generation One will be to develop civil nuclear programs in
2. J. Sheehan, T. Dunahay, J. Benemann, P. Roesler, A Look
1
all parts of the world without risking the pro-
Back at the U.S. Department of Energy’s Aquatic Species Centre for Nuclear Engineering, Department of Materials, Im- liferation of nuclear weapons technologies (2).
Program: Biodiesel from Algae (Department of Energy, perial College London, London HA9 8DT, UK. E-mail: rgrimes@
Golden, CO, 1998). imperial.ac.uk 2Cambridge Judge Business School, Cambridge The other will be to deal with nuclear waste in
3. N. Usui, M. Ikenouchi, Energy Convers. Manage. 38 CB2 1AG, UK, and Engineering Department, Cambridge as safe a manner as possible. Settling on policy
(suppl. 1), S487 (1997). University, Cambridge CB2 1PZ, UK. E-mail: [email protected] options has proved extremely difficult in many

www.sciencemag.org SCIENCE VOL 329 13 AUGUST 2010 799

 Corrections & CLarifications

erratum Post date 12 November 2010

Perspectives: “An outlook on microalgal biofuels” by R. H. Wijffels and M. J. Barbosa

(13 August, p. 796). The text attributed the following parameter to C. de Fraiture, M.
Giordano, Y. Liao, Water Pol. 10 (suppl. 1), 67 (2008): “For the production of 1 liter of
biofuel from fuel crops, approximately 10,000 liters of water are needed.” In fact, the de
Fraiture paper states: “It takes on average roughly 2,500 l[iters] of crop evapotranspiration

Downloaded from www.sciencemag.org on May 18, 2012

and 820 l[iters] of irrigation water withdrawn to produce one liter of biofuel. But regional
variation is large.”

www.sciencemag.org SCIENCE erratum post date 12 NOVEMBER 2010 1