Microalgae: The Potential for Carbon Capture

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Microalgae: The Potential for Carbon Capture Richard Sayre

Keywords: microalgae, carbon dioxide, biofuel, biomass, global warming

T

he most abundant and sustainable source of energy

for Earth is the sun. More than 3800 zettajoules (1 zettajoule = 1 3 1021 joules) of solar energy are absorbed by Earth’s atmosphere and surface annually. About 0.05% of this energy is captured in biomass each year through the process of photosynthesis (Hill et al. 2006, Lewis and Nocera 2006, Zhu et al. 2008). The production, decomposition, and accumulation of biomass play a central role in the global carbon cycle. In a well-balanced ecosystem, carbon capture from photosynthesis, carbon deposition in the soil and oceans, and carbon release from biological and geological sources are in equilibrium. Since the beginning of the industrial age (in the 1850s), however, this equilibrium has been perturbed by increasing carbon emissions from the combustion of fossil fuel and biomass, and from reduced carbon uptake as a result of global deforestation and the loss of arable land. Currently, more than 80% of the energy produced globally each year is generated through the combustion of fossil fuels. Direct carbon combustion for energy production generates more than 24 gigatons of carbon dioxide (CO2) annually (Lewis and Nocera 2006). As a result, atmospheric CO2 concentrations have risen from 295 parts per million (ppm) to 380 ppm over the last 100 years, and have contributed substantially to global warming, climate change, and resultant biological extinctions (Lewis and Nocera 2006, Battisti and Naylor 2008). The most environmentally sustainable way to reduce greenhouse gas emissions associated with energy production is to generate energy from carbon-neutral or reduced-carbon-emission sources. Wind, geothermal, solar, hydroelectric, ocean wave, and biofuel energy are being developed as more sustainable alternative energy sources when compared with the combustion of fossil fuels

(Schiermeier et al. 2008). In contrast to other renewable energy systems, biomass products can be converted into energy-dense, liquid-storage fuels that are compatible with the current petroleum-based energy infrastructure. Attempting to meet all of our energy demands using biomass-derived fuels, however, is not sustainable using current arable land. The total energy consumed by humans accounts for more than 26% of the global solar energy captured in biomass each year (Long et al. 2004, Lewis and Nocera 2006). The limitations of available arable land and the demands for food, fiber, and environmental sustainability constrain the use of crops or plants for biofuel production. Since biofuels have the potential to reduce our global carbon footprint, however, they are an attractive part of the mix of sustainable energy solutions. In addition, oil-based biofuels are one of the few renewable, energy-dense fuels that can replace the petroleum-based fuels used by the aviation and long-haul shipping sectors. The first generation of biofuel production systems (starch- and sugar-based ethanol production) demonstrated the feasibility of generating liquid transportation fuels from renewable sources, but at initially low energy-conversion efficiencies and high cost. Fermentation of biomass to produce ethanol emits substantial carbon and yields a fuel that has only about half the energy density of oil-based fuels. Two-thirds of the carbon in sugars fermented for ethanol production is emitted as CO2, and additional energy inputs associated with the use of fertilizers, pesticides, herbicides, and soil tillage, as well as irrigation, deforestation, increased soil respiration, erosion, and transportation of the feedstock, all reduce the net carbon-capture efficiency of alcohol fuels derived from biomass (Hill et al. 2006). For corn-based ethanol biofuel systems it takes at least 10 years of production from one site

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There is growing recognition that microalgae are among the most productive biological systems for generating biomass and capturing carbon. Further efficiencies are gained by harvesting 100% of the biomass, much more than is possible in terrestrial biomass production systems. Microalgae’s ability to transport bicarbonate into cells makes them well suited to capture carbon. Carbon dioxide– or bicarbonate-capturing efficiencies as high as 90% have been reported in open ponds. The scale of microalgal production facilities necessary to capture carbon-dioxide (CO2) emissions from stationary point sources such as power stations and cement kilns is also manageable; thus, microalgae can potentially be exploited for CO2 capture and sequestration. In this article, I discuss possible strategies using microalgae to sequester CO2 with reduced environmental consequences.

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Microalgal biofuel systems Recently, there has been substantial interest and investment in the development of microalgae to produce biofuels. Advantages of microalgae-based biofuels are greater

Figure 1. Microalgal carbon capture and biomass production. www.biosciencemag.org

production yields and available land area (compared with terrestrial crops); algae’s ability to capture CO2 as bicarbonate in ponds, reducing atmospheric CO2 emissions; and reduced competition for land, particularly arable land used for food production (figure 1). Algae are estimated to produce two- to tenfold more biomass per unit land area than the best terrestrial systems (Chisti 2008, Packer 2009, Pienkos and Darzins 2009, Mata et al. 2010, Stephens et al. 2010, Weyer et al. 2010). There are several reasons for the greater biomass yields of algae versus land plants. Generally, algae have higher photosynthetic efficiency than land plants because of greater abilities to capture light and convert it to usable chemical energy (Melis 2009, Weyer et al. 2010). Under ideal growth conditions algae direct most of their energy into cell division (6- to 12-hour cycle), allowing for rapid biomass accumulation. Also, unlike plants, unicellular algae do not partition large amounts of biomass into supportive structures such as stems and roots that are energetically expensive to produce and often difficult to harvest and process for biofuel production. In addition, algae have carbonconcentrating mechanisms that suppress photorespiration (Spalding 2008, Jansson and Northen 2010). With algae, all the biomass can be harvested at any time of the year, rather than seasonally. In contrast, only a portion of the total biomass of terrestrial crops (corn cob, soybean seed) is harvested once a year. When algae are grown under stressful conditions (e.g., low nitrogen) or in the presence of supplemental reductants (sugar, glycerol), the metabolism of some species is redirected toward the production and accumulation of energy-dense storage compounds such as lipids. Many unicellular algae are facultatively capable of producing up to 60% of neutral lipids (triacylglycerol [TAG]) per gram of dry weight, making them one of the most efficient biofuel production systems known (Sheehan et al. 1998, Weyer et al. 2010). Significantly, algal biofuel production systems can be tightly controlled and optimized. Temperature, pH, and nutrient and CO2 concentrations can be monitored and optimized for maximum biomass and oil yields. In addition, it may be possible to control light quantity and quality (wavelength) by altering pond depth or using frequencyshifting fluorophores to increase photosynthetically active radiation, respectively. This level of environmental control is difficult to achieve with land plants that have fixed plant architectures in soil open environments. The major constraints facing biofuel production from algae can be divided into biomass production, harvesting, and extraction systems, October 2010 / Vol. 60 No. 9 • BioScience 723


before the net carbon balance is positive (Searchinger et al. 2008). Further complicating matters is the fact that many first-generation biofuel systems use food crops. Competition for feedstocks such as corn and soybeans for food and energy production has the potential to affect global food prices. Cellulosics and hemicellulosics are among the most abundant biopolymers in nature; converting them into sugars using advanced enzyme catalysts promises to grow the available carbon resources for fuel production and to reduce the land area required for biofuel production (Pauly and Keegstra 2008). Hemicellulosic and cellulosic biofuel production systems enable the conversion of nearly all sugar-based plant polymers into fuels (ethanol, butanol, diesel). Plants that produce high levels of cellulosic biomass, such as Miscanthus and switchgrass, are being developed as second-generation biofuel crops. These biofuel crops do not compete directly with food production, require less agronomic (fertilizer, plowing, pesticide) inputs, and have lower environmental impacts than first-generation biofuels. However, some biofuel crops (Miscanthus) have the potential to be invasive species that may disrupt the biological integrity of local ecosystems (Raghu et al. 2008). Overall, the energy efficiency, environmental sustainability, and economics of various renewable fuel production systems must be collectively evaluated to make informed decisions to identify the best energy production systems for each location and market.

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Carbon capture by photosynthesis One of the more attractive features of algal biomass production is the potential to trap gaseous CO2 generated from point sources in ponds as bicarbonate. Cyanobacteria and eukaryotic algae transport and use bicarbonate as a source of carbon dioxide (Spalding 2008, Jansson and Northen 2010). At pHs between 6.4 and 10.3, the dominant (> 50%) chemical species of CO2 in water is bicarbonate, a nongaseous form of CO2. This transiently captured carbon is pumped into algal cells by bicarbonate transporters present in both the plasma membrane and in the chloroplast envelope of eukaryotic algae (reviewed in Spalding 2008). Inside the chloroplast, bicarbonate is converted into CO2 that can be fixed by rubisco (ribulose bisphosphate carboxylase oxygenase) to produce two molecules of 3-phosphoglycerate. Through a series of reactions these three carbon organic acids are reduced to the sugars that are substrates for starch and oil production. However, oxygen can compete with CO2 for fixation by rubisco. The products of the oxygenase reaction are 3-phosphoglycerate and 2-phosphoglycolate. The phosphoglycolate is subsequently metabolized to glycine, which, when condensed with another glycine molecule to produce serine, results in the loss of CO2. This carbon loss (one carbon per two molecules of glycine) diminishes the ability of the Calvin cycle to regenerate the five-carbon sugar substrate ribulose bisphosphate—required for CO2 fixation by rubisco—further reducing the efficiency of photosynthesis. This overall process is known as photorespiration because it occurs largely in the presence of light. The process of photorespiration reduces photosynthetic carbon fixation efficiency by 20% to 30% (Zhu et al. 2008). To reduce the competitive inhibition of oxygen on carbon fixation by rubisco, algae actively pump sufficient bicarbonate into cells to elevate internal CO2 concentrations to levels above those achievable by equilibrium with air, and competitively inhibit photorespiration (Badger and Price 1994). 724 BioScience • October 2010 / Vol. 60 No. 9

Carbon capture by algae One advantage of aquatic carbon capture and biomass production systems is the ability to capture CO2 in ponds in a nongaseous form as bicarbonate to fertilize algal growth. At moderate pHs (> pH 7) and temperatures (below 30 degrees Celsius), the dominant form of CO2 in water is bicarbonate. As previously discussed, algae have active bicarbonate pumps and can concentrate bicarbonate in the cell. The bicarbonate is subsequently dehydrated, either spontaneously or by carbonic anhydrase, and the resulting CO2 is captured through Calvin-cycle activity, ultimately in the form of algal biomass. Between 1.6 and 2 grams of CO2 is captured for every gram of algal biomass produced (Herzog and Golomb 2004). A variety of industrial sources of CO2 can be harvested using algal ponds. However, the various anthropogenic sources of CO2 will differ in their concentrations of CO2 and other contaminating molecules, and these attributes, as well as gas temperature and production volume, will influence the design of CO2-delivery systems for ponds. Flue gases from fossil-fuel power plants typically have high CO2 concentrations, ranging from 10% to 20%, but also contain biologically significant amounts of nitrous and sulfur oxides (NOx and SOx). The injection of power plant flue gases into algal ponds has been shown to elevate algal biomass yields by as much as threefold, but at a high energy cost (Jeong et al. 2003). Fortuitously, the benefits of flue gas injection on algal growth can be greater than the growth impacts solely attributed to inhibition of photorespiration by high CO2 concentrations (Douskova et al. 2009). Recent studies have shown that direct injection of flue gasses into ponds increases biomass productivity by 30% compared with direct injection of an equivalent concentration of pure CO2 Box 1. Constraints limiting algal biomass yield, biomass harvesting, and biofuel extraction. Algal production systems (50% to 60% costs) Identification of fastest-growing, highest-biomass-yielding strains Enhancing photosynthetic efficiency Ability to grow well across a wide range of temperature, light, and environments Available genomics; transformable, stable transgene expression Containment of genetically modified algae Increase oil accumulation with minimal biomass penalty Pond environmental control and biomass optimization Crop protection; control of competing algae, bacteria, viruses, grazers Removal of growth-inhibiting waste products Recycle growth media and nutrients to reduce environmental impact Harvesting and extraction systems (40% to 50% of costs) Low energy harvesting systems Efficient oil extraction or secretion processes Optimization of coproduct yields to offset oil production costs



and are the subject of directed research investment from the public and private sectors (box 1). Various estimates indicate that potential oil and biomass yields from algae ponds range from 20,000 to 60,500 liters per hectare per year (2000 to 6000 gallons per acre per year) and 50,000 to 15,000 kilograms per hectare per year (140 to 420 tons per acre per year), respectively (Weyer et al. 2010). Optimization of light harvesting efficiency and enhanced metabolic flux leading to increased oil or biomass accumulation promise to boost the efficiency of biomass and oil production from algae at least two- to threefold (Wang et al. 2009, Stephens et al. 2010). These advancements— coupled with more energy-efficient algal harvesting and oil extraction technologies, coproduction of income-generating commodities including methane from the anaerobic digestion of delipidated biomass, and residual biomass for animal feeds—will collectively reduce the cost of microalgal oil production and potentially bring algal biofuel economics to parity with petroleum (Stephens et al. 2010).

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Carbon sequestration by algae To have the greatest impact on greenhouse gas accumulation, CO2 must not only be captured but also sequestered over very long (geologic) time intervals. Direct injection of CO2 into geological formations is one strategy under consideration for the mitigation of CO2 from point sources (Yang et al. 2008). However, it is difficult to ensure that CO2 stores in geologic formations will be secure over the long term. The escape of large amounts of CO2 to Earth’s surface could be catastrophic (Benson and Cook 2005). A potentially lowerrisk strategy for sequestering carbon dioxide is to chemically convert CO2 into stable liquids or solids. The production of carbonate salts is one approach being developed (Benson and Cook 2005); these salts could be buried or used as construction material. Another strategy for sequestering carbon is to bury it as biomass. This strategy is particularly attractive as solar energy is used to generate the biomass. One of the more controversial manifestations of biomass carbon sequestration has been the proposal to fertilize the open oceans to stimulate phytoplankton production (Stepan et al. 2002). Fertilizing oceans with the nutrients (e.g., iron) that usually limit algal growth can substantially enhance algal growth and carbon capture (Buesseler et al. 2004), but the ecological www.biosciencemag.org

impacts of fertilizing the oceans are largely unknown. An alternative strategy to open-ocean fertilization of phytoplankton is the controlled production of algal biomass in contained ponds or closed production systems optimized for biomass-accumulation and capture of carbon dioxide. Two possible algal carbon sequestration systems are considered here: (1) permanent burial of total algal biomass in deep geologic formations, and (2) burial of extracted or processed carbon-rich fractions from algal biomass (table 1). Burial of total algal biomass is the simplest technological approach. Direct burial of algal biomass is the most energyefficient way to sequester carbon, because no dewatering is required after processing. The downside is that considerable amounts of inorganic nutrients would also be buried with the algal biomass. As much as 7% of algal dry weight is inorganic elements or ash. Burying substantial amounts of nitrogen and phosphorous would not be sustainable. An alternative approach to burying biomass is to bury only the neutral lipid or hydrocarbon fraction of the algal biomass. As previously discussed, neutral lipids or TAGs account for as much as 60% of the total dry weight of algae. More than 75% of the mass of a typical TAG is carbon, and thus TAGs represent rich sources of captured carbon in cells. Selective extraction of TAGs under continuous-flow processes can be achieved using biocompatible organic solvents that selectively extract hydrophobic molecules without killing the algae, allowing the algae to more rapidly generate extractable biomass without the costs of regenerating cellular machinery (Sayre and Periera 2008). Triacylglycerols extracted using low-energy-harvesting and extraction processes could be injected into geologic formations to “lock” the carbon in place. Significantly, burying TAGs does not carry the risk associated with the potential escape of gaseous CO2 from geologic formations, and because TAGs do not contain elements other than carbon, hydrogen, and oxygen, inorganic nutrients (e.g., nitrogen, phosphorus, and sulfur) required for algal growth could be recycled and not buried with the carbon. Another strategy to sink carbon in a geologically stable form is to convert the biomass into biochar (Hielmann et al. 2010). Biochar is also a stable form of carbon that can persist in soils for millions of years (Amonette et al. 2007). Biochar is more than 90% carbon and is a by-product of pyrolysis at high temperatures in the presence of catalysts under anaerobic conditions (Hielmann et al. 2010). Pyrolysis also generates gaseous products including hydrogen, methane, and CO2, which may be combusted to drive the pyrolytic reaction. Biochar may contain inorganic elements but can be directly added to soil as a supplement instead of being buried, reducing energy costs and expanding the range of possible applications. A variation of pyrolysis that generates a liquid fuel by-product is hydrothermal liquefaction. Heat treatment of biomass (at temperatures greater than 400 degrees Celsius) in the presence of water leads to the production of bio-oils and other products, including biochar (Hielmann et al. 2010). As much as 55% of the carbon in algal biomass processed by hydrothermal liquefaction can October 2010 / Vol. 60 No. 9 • BioScience 725


(Douskova et al. 2009). The flue gas fertilizer effect may be due to the presence of supplemental nutrients (sulfur and nitrate) present in flue gasses. The efficiency of CO2 capture by algae can vary according to the state of the algal physiology, pond chemistry, and temperature. Carbon-dioxide capture efficiencies as high as 80% to 99% are achievable under optimal conditions and with gas residence times as short as two seconds (Keffer and Kleinheinz 2002). For a typical 200-megawatt-hour (MWh) natural gas–fired power plant, it has been estimated that an algal pond of 3600 acres would be sufficient to capture 80% of the plant’s CO2 emissions during daylight hours, assuming an algal areal biomass productivity rate of 20 grams dry weight per square meter per day (Herzog and Golomb 2004). Because of the greater CO2 emission levels per MWh of coalburning power plants, a pond approximately 7000 acres in size would be required to capture 80% of the CO2 emissions from a 200-MWh coal-burning power plant during the day. Locating ponds near CO2 point sources provides several potential cost- and energy-saving advantages. Integrated power plant–algal pond facilities would reduce the costs of CO2 transportation, produce limited waste heat from the power plant for warming ponds in the winter, and could give carbon credits to the utility. Locating ponds near CO2 sources can be problematic, however, depending on land availability and the climatic suitability of the site. Furthermore, CO2 capture by biomass production is not feasible in the dark. Thus, methods to capture, concentrate, store, and transport CO2 from source to sink (pond) during the day will need to be developed as part of the integrated solution for capturing as much of the CO2 emission as possible (Kadam 1997).

Articles Table 1. Features of various microalgal-based carbon sequestration systems. Algal carbon capture and sequestration systems

Advantages

Liabilities

Permanent burial of total fresh biomass

Captures the most carbon No biomass processing

Burial of inorganic nutrients and water in biomass

Permanent burial of algal lipids

No loss of inorganic nutrients Long-term energy reserve Easily handled as liquid

Sequesters < 50% of carbon present in biomass Energy costs associated with biomass processing

Soil amendment with algal biochar

Potential soil supplement Permanent carbon sequestration without burial

Sequesters less than 55% of carbon present in biomass Energy costs associated with biomass processing Potential dispersal of some fraction of inorganic nutrients

Summary At present, there are few examples of continuous long-term biomass production or carbon-capture systems using algae (Jeong et al. 2003, Doucha et al. 2005). However, laboratory and pilot plant studies suggest that capturing CO2 by algae is a potentially viable strategy for mitigating CO2 emissions from anthropogenic sources. The long-term prognosis for large-scale carbon capture using algae will depend on the passage of legislation promoting carbon-capture technologies and the economics of algal pond systems. Significantly, life-cycle analyses suggest the costs for capturing carbon and producing liquid biofuels from algae may approach the costs of producing petroleum-based fuels in the next 5 to 10 years (Schenk et al. 2008, Lardon et al. 2009, Stephens et al. 2010). Acknowledgments Funding was provided for this review by the US Air Force Office of Scientific Research and the Department of Energy’s Energy Frontier Research Center program to Richard Sayre. Additional thanks to Kevin Berner at Phycal LLC for information on algal biofuels life-cycle analyses. The Danforth Center is a nonprofit research center. Sayre is also chief technology officer of Phycal LLC in Cleveland, Ohio. Phycal is a for-profit algal biofuels company. References cited Amonette J, Lehmann J, Joseph S. 2007. Terrestrial carbon sequestration with biochar: A preliminary assessment of its global potential. American Geophysical Union; Fall Meeting 2007, abstract #U42A-06. Badger MR, Price GD. 1994. The role of carbonic anhydrase in photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 45: 369–392. Battisti DS, Naylor RL. 2008. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323: 240–244. Benson S, Cook P. 2005. Underground geological storage. Pages 197–278 in Metz B, Davidson O, de Coninck, Loos HM, Meyer L, eds. Carbon Dioxide Capture and Storage 12. Intergovernmental Panel on Climate Change. Buesseler KO, Andrews JE, Pike SM, Charette MA. 2004. The effects of iron fertilization on carbon sequestration in the Southern Ocean. Science 304: 414–417.

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