A matter of detail: Assessing the true potential of microalgal biofuels

The Fine Print of Microalgal Biofuels I want to point out what I believe to be an argumentative flaw commonly encountered in the literature on the use of algae for the production of biofuels, namely, the tendency to bundle all species and all strains of microalgae into a single entity of interest to biotechnology. Although this might seem innocuous on the surface, it has deep implications when used to encourage the development of microalgal chemicals, and biofuels in particular. Microalgae, as a group, hold great potential for commercializing a variety of products, including hydrocarbons, and should continue to be investigated from the perspective of industrial biotechnology. But to say that microalgae, again as a group, will solve the world's energy problems is at odds with the principles of process engineering and design, which must be obeyed when attempting to bring the aforementioned potential into tangible fruition. Nevertheless, various scientific and non-scientific sources substantiate algae's potential by citing their high oil content, their fast growth rate, their high photosynthetic efficiency, their ability to grow in saline or brackish water, their capacity to fix gases that are considered emissions, their ease of separation from water by methods unavailable to many other microbes, their ability to produce fine chemicals that could subsidize the cost of production, etc. (Duffy et al., 2009; Pollack, 2010; Schmidt, 2012; Wald, 2008; Wijffels and Barbosa, 2010). Furthermore, there are methodical and comprehensive analyses that study the design and economics of such processes, based on the same premises, the results of which are often used to tout the promise of microalgal biofuels. By leaving the species unspecified, however, the assumptions used in those analyses are for the most part plainly inaccurate. To the untrained reader, the claims might appear completely justifiable. After all, there are algal species that can survive in salt concentrations of 5 M (e.g., Dunaliella spp.) (Evans and Kates, 1984), species that have productivities of 30 g/m2/day (e.g., Chlorella vulgaris) (Hirano et al., 1997), species that show hydrocarbon contents above 50% (e.g., Botryococcus braunii) (Metzger and Largeau, 2005), species that produce valuable chemicals (e.g., Haematococcus spp.) (Lorenz and Cysewski, 2000), species that can be induced to autoflocculate (e.g., Scenedesmus dimorphus) (Sukenik and Shelef, 1984), among others. But to consider a process based on these assumptions, which have never been reported in the same strain, naturally-occurring or genetically modified, and to evaluate the economics of biofuel production based on these assumptions, strains credulity. As an analogy, lignocellulosic ethanol could probably be a widespread product today if one could design and build a process that used a microbe with the growth rate of Escherichia coli, the ethanol tolerance of Saccharomyces cerevisiae, the thermophilic nature of Sulfolobus acidocaldarius, and the cellulolytic activity of Trichoderma reesei. I do not (and cannot) refute that an “ideal” microalgal strain harboring an optimal combination of traits could be potentially found or even engineered, but that is yet to happen. Unfortunately, those strongly supporting microalgae are all too familiar with this line of reasoning, which is similarly employed when describing the location where a potential facility would be built. There are places in the world with sufficient year-round levels of sunlight, that are close to plenty of water, in the vicinity of carbon intensive industries that can supply inexpensive CO2, and with developed road and rail networks that can support distribution of the raw materials and end products. But by no stretch of the imagination are these locations commonplace. Alarmed by the prevalence of this logic, I believe it to be essential that the readers and reviewers of such studies stop ignoring the commonsensical notion that “the devil is in the details.” The potential of microalgal biofuels will be realized only if we address ways to solve the problems that are raised when those details are considered, and not brushed off as unimportant. Daniel Klein-Marcuschamer Physical Biosciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Rd MS 978-4121, Berkeley, California, 94720 Deconstruction Division, Joint BioEnergy Institute, 5885 Hollis St., Emeryville, California, 94608 University of Queensland, Australian Institute for Bioengineering and Nanotechnology, St Lucia, Australia References Duffy JE, Canuel EA, Adey W, Swaddle JP. 2009. Biofuels: algae. Science 326:1345a. Evans RW, Kates M. 1984. Lipid composition of halophilic species of Dunaliella from the dead sea. Arch Microbiol 140:50–56. Hirano A, Ueda R, Hirayama S, Ogushi Y. 1997. CO2 fixation and ethanol production with microalgal photosynthesis and intracellular anaerobic fermentation. Energy 22:137–142. Lorenz RT, Cysewski GR. 2000. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167. Metzger P, Largeau C. 2005. Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66:486–496. Pollack A. 2010. Exploring algae as fuel. The New York Times. Available at: http://www.nytimes.com/2010/07/26/business/energy-environment/26algae.html Schmidt M. 2012. The green gold rush. Nature. Available at: http://blogs.nature.com/tradesecrets/2012/04/23/the-green-gold-rush Sukenik A, Shelef G. 1984. Algal autoflocculation–verification and proposed mechanism. Biotechnol Bioeng 26:142–147. Wald ML. 2008. Colorado company to take algae-based fuel to the next level. The New York Times Green Blog. Available at: http://green.blogs.nytimes.com/2008/11/11/colorado-company-to-take-algae-based-fuel-to-the-next-level/ Wijffels RH, Barbosa, MJ. 2010. An outlook on microalgal biofuels. Science 329:796–799. Acknowledgements The author would like to thank the DoE Joint BioEnergy Institute (http://www.jbei.org) supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research, through contract DE-AC02- 05CH11231 between Lawrence Berkeley National Laboratory and the US Department of Energy. Support from the Australian Institute of Bioengineering and Nanotechnology, at the University of Queensland, is also acknowledged. Special thanks to Prof. Harvey Blanch. The author declares no conflicting financial interests. The Problems With Algal Fuels… Production of algal oil and its conversion to useable fuels has been demonstrated repeatedly (Chisti, 2010, 2012; Chisti and Yan, 2011), but commercial production remains elusive. Algal fuels are expensive, but this will change as the technology develops. Economic competitiveness of course does not mean an environmentally sustainable production, or an ability to produce at a sufficiently large scale to meaningfully displace petroleum fuels. Microalgae are photosynthetically more efficient compared with land plants (Chisti, 2010, 2012); nevertheless, algal oil places unsustainable demands on freshwater and fertilizers as the scale of production is increased (Pate et al., 2011). Insufficiency of low-cost concentrated CO2 is a major impediment to production of algal fuels at any substantial scale (Pate et al., 2011). Producing a ton of algal biomass requires a minimum of 1.83 tons of CO2 (Chisti, 2007), but this needs to be at a concentration that is at least 100-fold greater than the concentration in the ambient atmosphere. Fossil fuel burning power plants are the main potential sources of concentrated CO2. In 2011, the US power plants emitted 2,209 MT of CO2. No more than 10% of this is likely to be accessible for producing algal biomass, as an emitting facility must be in a climatic region suitable for growing algae and have nearby the necessary land and water resources required for algal culture. If no other resource limits production, the available CO2 could be used to produce at most 120.7 MT of algal biomass. Assuming a fairly consistently attainable oil content of 40% by weight in the biomass (Chisti, 2012), nearly 48.3 MT of algal crude oil could be produced. In terms of energy content, a barrel of petroleum roughly equates to 1.25 barrels of crude algal oil (Chisti, 2012). Assuming an oil density of 887 kg m−3, as for palm oil, 48.3 MT of algal crude is equivalent to 273.9 million barrels of petroleum, or around 14.5 days of US petroleum consumption. Mechanisms for concentrating CO2 from the dilute levels in the atmosphere for supplying to algal cultures would be necessary for algal fuels to have any hope of displacing petroleum derived fuels to a level of >5%. Algal biomass contains roughly 1.2% phosphorous (P) by weight. Producing 120.7 MT of biomass as constrained by the supply of CO2, will require nearly 3.7 MT of P, or around 2.5-fold the current US production for agriculture. Therefore, methods of recycling P would be necessary for producing algal fuels. Similarly, producing 120.7 MT of algal biomass will require >85% of the current US consumption of fixed nitrogen (N) to be diverted from agriculture to growing algae. Clearly, nutrient recycling is a key requirement for sustainable production of algal fuels. An alternative is to engineer algae to fix nitrogen. Until an ability to fix nitrogen is engineered, a recycling of nitrogen through anaerobic digestion of residual algal biomass will be necessary for sustainable production of algal fuels. Anaerobic digestion is essential also for recycling the phosphorous. Production of algal fuels requires fossil energy. Substantially more energy must be recovered in the fuel compared to the fossil energy used in its production. In short, the energy ratio of the fuel must substantially exceed unity. Preferably, the energy ratio should be 8, or more, as is possible to achieve for bioethanol derived from sugarcane (Chisti, 2008). Estimates suggest an energy ratio of <1 for algal fuels in many cases. Energy ratio may be improved by reducing the energy requirements of growing the algae (Sompech et al., 2012), harvesting the biomass, extracting the oil and processing it to useable fuels; recovering energy from the spent biomass by anaerobic digestion; and improving the efficiency of photosynthesis via genetic and metabolic engineering (Stephenson et al., 2011). Advances are being made in all these areas. In nutrient sufficient conditions, the productivity of algae is severely constrained by the design of the culture system. Existing commercial outdoor ponds located in some of the most suitable climates can achieve a maximum annual averaged biomass productivity of only around 86.7 tons per hectare per year (Chisti, 2012). This productivity is much lower than what is biologically possible for algae (Chisti, 2012). This low level of productivity is mostly a consequence of the inability of sunlight to penetrate most of the volume of a culture pond (Chisti, 2012). A practical upper limit to algal oil productivity of conventional raceways is about 37,000 L/ha year (Chisti, 2012). Estimates of the theoretical maximum productivity of algal crude oil (Weyer et al., 2010) suggest that there is much scope for improving the observed productivity. Genetic and metabolic engineering will be essential for sustainable production of algal fuels, for example, by: increasing the photosynthetic productivity of the biomass and oils; modifying the oil profile and quantity produced per cell; enabling oil release from the cell into the culture broth; improving the penetration of sunlight in an algal suspension; and enhancing the ability of the cells to withstand an elevated salinity. All this is potentially feasible without too high a metabolic cost. Genetic and genomic methods are already being applied to improve production and recovery of algal fuels (Waltz, 2009), although much remains to be done in all the key areas. In summary, production of sufficient algal oil to displace about 5% of the total annual US petroleum consumption is potentially feasible if the inorganic nutrients are recycled, energy is recovered from the spent biomass, the CO2 supply bottleneck is overcome, and the cost of producing the algal biomass with an oil content of ≥40% is reduced to about $0.25/kg on a dry basis (Chisti, 2012). All this may be possible with sustained research and development spanning many years. Yusuf Chisti School of Engineering, Massey University, Palmerston North, New Zealand Y.Chisti@massey.ac.nz References Chisti Y. 2007. Biodiesel from microalgae. Biotechnol Adv 25:294–306. Chisti Y. 2008. Biodiesel from microalgae beats bioethanol. Trends Biotechnol 26:126–131. Chisti Y. 2010. Fuels from microalgae. Biofuels 1:233–235. Chisti Y, Yan J. 2011. Algal biofuels—A status report. Appl Energy 88:3277–3279. Chisti Y. 2012. Raceways-based production of algal crude oil. In: Posten C, Walter C, editors. Microalgal biotechnology: Potential and production. Berlin: de Gruyter. p 113–146. Pate R, Klise G, Wu B. 2011. Resource demand implications for US algae biofuels production scale-up. Appl Energy 88:3377–3388. Sompech K, Chisti Y, Srinophakun T. 2012. Design of raceway ponds for producing microalgae. Biofuels 3:387–397. Stephenson PG, Moore CM, Terry MJ, Zubkov MV, Bibby TS. 2011. Improving photosynthesis for algal biofuels: toward a green revolution. Trends Biotechnol 29:615–623. Waltz E. 2009. Biotech's green gold? Nature Biotechnol 27: 15–18. Weyer KM, Bush DR, Darzins A, Willson BD. 2010. maximum algal oil production. Microalgae for Biofuels and This only microalgal biomass production sunlight and CO2 for production of biofuels and Microalgae biomass, about tons is produced in mostly of the raceway The main microalgae species produced of are about and Chlorella about in from to a tons annual for of total world production, which is for products, with for and Chlorella biomass of and Dunaliella and Haematococcus sources of and are also produced but in much tons of biomass and for much In produced microalgae biomass, mostly for products, is of in production scale and in than required for the production of biofuels or the of most of the of research and in the an and of and A of biofuels production by Chisti a in the that or or are to ponds in culture cell lower harvesting and even and are the production for biofuels and other microalgae even in the algal biofuels ponds (e.g., Wijffels and Barbosa, 2010). requirements in and in such limit growth to compared to for raceway ponds et al., without this any of for production as would be required for economics of and of compared to a a commercial have been the at than but all a to years. one a in producing high biomass. have no ponds in terms of if based on the by the their water or energy or even to will be used for scale but at of the total is not a major cost in biomass production. tons of dry or biofuels produced per hectare in 1 year a in this with many literature based on theoretical or that often exceed year or year (Chisti, et al., 2011). The most that and be is about these production such productivities will require a including algal strains with reduced content of harvesting in green in for but with a photosynthetic at high Although of research interest for et al., 2009), no strains have yet demonstrated to improved productivities sunlight in outdoor In any a source of CO2 power processes, is required to microalgae, a major compared to production can be with and for algal biomass production and for and et al., 2012; et al., 2010). these require many production and assumptions, about the of CO2 sources (e.g., power ethanol and suitable and sufficient available water, with the of any of these the potential of this A resource study et al., 2011), used by to that algae oil might of fuels. This CO2 and freshwater on land and sunlight where large CO2 such as from fossil power are located with the other requirements for algae production, CO2 is to a of to and in algae productivity et al., power with their lower CO2 concentrations are than power plants as to and into the algal cultures is a major in energy In for major in CO2 from power plants are not are being by a of and in which ethanol or other biofuels into the growth require to product that has not been at scale the the of algal producing biofuels or with high is also not to their large in their these and microalgae biomass production could a to the of and sustainable biofuels and as as million of algal production producing year of biomass, not resource and productivity would produce as much as the million hectare US and about 10% of on an equivalent of world petroleum much of this biomass would be produced resources for biofuels and production. cost microalgae biomass production for and fuels will not be will require strains and low cost harvesting processes, location at and will not be a for the problems of oil, or low-cost microalgae production could to all and also have in fertilizers and chemicals production. development on and et al., A major of microalgae is that their for much more research and development of such than is possible with Engineering, California, References and of microalgae ponds for conversion of CO2 to biomass. to US A. production and of CO2 with microalgae. In: editors. a growth in green energy and products. of the biomass of the p T. 2012. for microalgae oil production. Microalgal biomass for potential for of and Chisti Y. Biodiesel from microalgae. Adv R, productivities in and of Appl J. A and of Energy Biosciences C. Berkeley, 2010. by the on energy. A for industrial P, J. at the of species from report. of ponds and Bioeng National microalgae biofuel production potential and resource Wijffels RH, MJ. An outlook on microalgal biofuels. Science Biofuels for a the to from developed from that to to in technology many has for which in the to the ability to use materials and technology is to natural and improve of microalgae are in such as sustainable and production of products. from microalgae are a such as from microalgae. The is for biofuels and are their is that biofuels can be produced from microalgae, but it is if commercial will be is that microalgae at large scale can achieve high productivity for of (e.g., et al., Existing commercial microalgae to their product to In the of biofuels the potential is the of various fossil fuels. and research are to for the production of biofuels from microalgae biomass. The main process requirements production, conversion and The end must be into the fossil fuel supply and the process must be and a microalgae to biofuel process a commercial key to be the total and the total process energy on energy biofuels should an and equivalent biofuel fossil derived fuel. should be that fuels are not energy (e.g., et al., 2012). There has been an of literature on the many of producing biofuels from microalgae, but more is required on the Microalgae biofuels will be with the development of a which all materials that appear in of and from other The technology must be and and have to be considered and an rate of is to microalgae biofuels the are at commercial the production of microalgae is in ponds with a of to an between and and a of to The required energy to these ponds at the and is et al., 2010). There are available on productivities in large scale raceway but much that in dry and in can be that photosynthetic of various microalgae are it is to that annual of to of microalgae can be produced per hectare of pond There are large of water required to these ponds and with process and to water is required per of biomass. this for large of water, which is to all producing or products, it is that water brackish or should be used as the culture to (e.g., et al., 2012). The for production of microalgae biofuels is not productivities but sustainable of P, and to growth et al., 2011). the concentrations of microalgae cultures are than in The required concentration for processing is by the product and Microalgae species that are suitable for biofuels are as which are too for a and have a to the culture The in a biomass recovery is likely to of a (e.g., by or is often as concentrations can be with a are et al., 2012). scope for development of harvesting and that which are and with such as and By and into an a lower energy consumption of has been et al., This combination can the biomass from to and of of the culture of the is required for efficient This can be with as the volume is of the technology could potentially have an energy consumption of and the biomass to To the biofuel from the it is to have a process producing a crude oil that can be to an oil or for use as a fuel. is to and and has the ability to all the of microalgae and via a and the from and to and needs to be for maximum energy oil is from the product via a separation The and of the oil are on and process conditions, but have an energy content of of a equivalent fuel. There is a of available to the total energy the of it to be the technology to be into a microalgae biofuels production studies have that that as various microalgae to biofuel are being commercial in a fuel is Engineering, University of Australia References CM, 2012. The energy on for algal results for a research production Algal from to of K, of microalgae by the design, and Appl Energy 2010. A technology and engineering of algae biofuel production. Energy Biosciences at: S, 2012. and microalgae biomass. In: editors. for biofuels and energy. p B. the microalgal or RW, 2012. Environmental of algal biofuel technology Y. 2011. on production from water and nutrients