Algae biofuels: versatility for the future of bioenergy

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Algae biofuels: versatility for the future of bioenergy Carla S Jones1,2 and Stephen P Mayfield1,2 The world continues to increase its energy use, brought about by an expanding population and a desire for a greater standard of living. This energy use coupled with the realization of the impact of carbon dioxide on the climate, has led us to reanalyze the potential of plant-based biofuels. Of the potential sources of biofuels the most efficient producers of biomass are the photosynthetic microalgae and cyanobacteria. These versatile organisms can be used for the production of bioethanol, biodiesel, biohydrogen, and biogas. In fact, one of the most economic methods for algal biofuels production may be the combined biorefinery approach where multiple biofuels are produced from one biomass source. Addresses 1 The San Diego Center for Algae Biotechnology, University of California San Diego, 9500 Gilman Drive, MC0368, La Jolla, CA 92093, United States 2 Division of Biological Sciences, University of California San Diego, 9500 Gilman Drive, MC0368, La Jolla, CA 92093, United States Corresponding author: Mayfield, Stephen P ([email protected])

Current Opinion in Biotechnology 2011, 23:1–6 This review comes from a themed issue on Energy biotechnology Edited by Jim Liao and Joachim Messing

0958-1669/$ – see front matter # 2011 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2011.10.013

Introduction Over the past 50 years, the world’s population has more than doubled, coupled with an expectation of a higher standard of living and an ever-increasing economic output this has resulted in a large increase in primary energy consumption, particularly the use of fossil fuel-derived energy [1]. In 2010, world primary energy consumption grew by 5.6%, the largest percentage growth in almost 40 years. This growth included an increase in the consumption of all major fossil fuels including oil, natural gas, and coal [2]. This trend in increasing energy consumption is expected to continue as the world’s population is projected to increase by an additional 1.4 billion people by 2030, and have an increase of 100% of the world’s real income [1]. These increases will put enormous pressure on the finite supply of fossil fuel-based energy, exacerbating global concerns over energy security, fossil fuelbased environmental impacts such as climate change, and the rising cost of energy and food. All of these real www.sciencedirect.com

concerns support the need for the development of alternative and renewable sources of energy [3]. Currently, the world consumes about 15 terawatts of energy per year and only 7.8% of this is derived from renewable energy sources. Yet, the total power of sunlight hitting the surface of the Earth every year is about 85,000 terawatts [2,4]. However, replacing fossil fuelderived energy with renewable energy sources derived from sunlight, such as wind, solar, hydro, or biomass energy is a daunting task in large part because these energy sources have a lower energy density, cannot be controlled with an ‘on and off’ switch, and most are considerably more expensive than what fossil fuels are today [5]. In 2009, transportation represented 29% of the end-use shares of total energy consumption in the US with a significant portion of this consumption (approximately 80%) resulting from road transport using liquid petroleum fuels [6,7]. The high energy density and ease of transportation and storage of liquid petroleum transportation fuels make them difficult to replace with any current commercially available sources of renewable energy [7]. One potential answer to the replacement of the unique characteristics of liquid transportation fuels is to use the same resources that provided us with fossil petroleum fuels originally: photosynthetic microorganisms producing bio-oils.

Sustainable sources of bioenergy Photosynthetic organisms such as higher plants, algae, and cyanobacteria are capable of using sunlight and carbon dioxide to produce a variety of organic molecules, particularly carbohydrates and lipids. These biomolecules can be used to generate biomass or more directly through extraction as a source of fuel known as biofuels. The value of biofuels to meet energetic needs of the future, particularly transportation fuels, has continued to play a role in the formation of US policy for a number of years, including the recent establishment of the Renewable Fuels Standard in 2009 mandating the production of 36 billion gallons of biofuels by 2022 to displace petroleum in our transportation fuels mix [8,9]. Two of the most common biofuels currently produced are ethanol produced from corn or sugarcane and biodiesel produced from a variety of oil crops such as soybeans and oil palm [9]. Ethanol production has flourished in the US, rising 25% between 2000 and 2008 due to its use as a gasoline additive and due to federal mandates and tax incentives to fuel blenders. Today 30% of the corn currently grown is used for ethanol production [9,10]. If corn ethanol was the sole source used to achieve the Current Opinion in Biotechnology 2011, 23:1–6

Please cite this article in press as: Jones CS, Mayfield SP. Algae biofuels: versatility for the future of bioenergy, Curr Opin Biotechnol (2011), doi:10.1016/j.copbio.2011.10.013


2 Energy biotechnology

2020 federal mandates for renewable fuel, than 100% of the corn currently available in the US would be required. To meet these mandates and maintain today’s 30% corn crop utilization would require an increase in corn harvest by 423%, a number unlikely to be achievable in the next 10 years [8,9]. The dedication of significantly higher amounts of the US corn crop to fuel production could have devastating effects on food availability around the world where about 1.02 billion people are already undernourished [11]. This food versus fuel dilemma and the limited environmental savings associated with corn ethanol production led policymakers to specify that a significant portion of the biofuels (21 billion gallons) in the renewable fuels mandates be derived from noncorn starch products [8,9,12]. One source of these biofuels may be ethanol derived from sugarcane; however, although the domestic production cost of sugarcane ethanol is 24% lower than corn ethanol, the transportation cost and the coproduct credits associated with corn ethanol make sugarcane ethanol 17% more costly. Thus, sugarcane ethanol is also an unlikely candidate for the displacement of significant amounts of fossil fuels [10]. The high cost of sugarcane ethanol and the competition with food from corn ethanol leave a large gap between the current feasible production levels of ethanol and the fuel requirements for the RFS2 mandate. To overcome these limitations, lignocellulosic feedstocks are also being developed as sources for the production of ethanol [3]. Lignocellulosic feedstocks come in a wide range of different plants, including agricultural waste products such as corn stover, woody sources such as aspen and dedicated energy crops such as hybrid poplar and switchgrass [13]. Recent research has focused on understanding how the biochemical composition of these crops, mainly the ratios of cellulose, hemicellulose, and lignin, impact the efficiency of ethanol production, and on methods to lower the costs of the enzymes and pretreatments needed to release the fermentable sugar components [11,13]. Currently, no commercial scale cellulosic ethanol plants are in operation largely due to the high price of production, almost twice that of corn ethanol [13,14]. The displacement of transportation fuels by biofuels is not limited to ethanol. Oil-seed plants such as soybean, rapeseed, or palm oil, also offer the opportunity to produce biodiesel. However, once again these traditional oil crops are used as food, and hence using them as fuel has an impact on food availability [15]. Another source of biodiesel that has recently had a lot of media exposure is Jatropha curcas. J. curcas is a small tree that is considered drought-tolerant and produces seeds that contain 20–40% nonedible oil, therefore being noncompetitive with food sources and agricultural land [16]. Although there is not an agronomically developed strain of J. curcas for biodiesel Current Opinion in Biotechnology 2011, 23:1–6

production, research and breeding programs are focused on using many modern techniques such as transcriptomics and near-infrared spectroscopy to identify traits valuable in making this plant a dedicated oil-seed energy crop [17,18]. In recent years, algae have become a focus in both academic and commercial biofuels research. These photosynthetic organisms are known to produce high oil and biomass yields, can be cultivated within nonfreshwater sources including salt and wastewater, can be grown on nonarable land, do not compete with common food resources, and they very efficiently use water and fertilizers for growth [19]. However, the true hallmark of these microscopic organisms is in fact their versatility (Figure 1). Algae can tolerate and adapt to a variety of environmental conditions, and are also able to produce several different types of biofuels.

Algae bioenergy production options Bioethanol

Bioethanol from algae holds significant potential due to their low percentage of lignin and hemicellulose as compared to other lignocellulosic plants [20]. Algae can be classified as either microalgae or macroalgae based on morphology and size. Microalgae are microscopic organisms while macroalgae are typically composed of multicellular plant-like structure, like giant kelp. Although macroalgae can look similar to land plants, these organisms in fact do not have the same lignin crosslinking molecules in their cellulose structures because they grow in aquatic environments where buoyancy allows for upright growth in the absence of the lignin crosslinking [21]. While having a low lignin content, macroalgae contain significant amount of sugars (at least 50%) that could be used in fermentation for bioethanol production [22]. However, in certain marine algae such as red algae the carbohydrate content is influenced by the presence of agar, a polymer of galactose and galactopyranose. Current research seeks to develop methods of saccharification to unlock galactose from the agar and further release glucose from cellulose leading to higher ethanol yields during fermentation [22,23]. Microalgae are also being studied for bioethanol production. Green algae including Spirogyra species and Chlorococum sp. have been shown to accumulate high levels of polysaccharides both in their complex cell walls and as starch. This starch accumulation can be used in the production of bioethanol [20,24]. Harun et al. have shown that the green algae Chlorococum sp. produces 60% higher ethanol concentrations for samples that are pre-extracted for lipids versus those that remain as dried intact cells [20]. This indicates that microalgae can be used for the production of both lipid-based biofuels (see below) and for ethanol biofuels from the same biomass as a means to increase their overall economic value. www.sciencedirect.com



Algae biofuels Jones and Mayfield 3

Figure 1

Current Biofuels Sources Oil Seed Plants

Corn & Sugarcane

Anaerobic Fermentation of Waste Materials

Lignocellulosic Plants

Biodiesel

Bioethanol

Biogas

Biohydrogen

Ref. 15, 25, 27

Ref. 15, 20

Ref. 29, 38

Ref. 32, 37

Algae Algal Versatility for Economic Viability Current Opinion in Biotechnology

The RFS2 mandates the production of 36 billion gallons of biofuels by 2022. Currently many plant resources can be used to produce these biofuels; however, many of them compete with food availability. Algae represent a single photosynthetic production system that is capable of extremely versatile biofuels applications that will undoubtedly supplement other less versatile systems. References shown highlight their versatility.

Biodiesel

Algae biodiesel is another algal-derived biofuel with future commercial feasibility. Many species of algae produce large amounts of lipids as storage products, as high as 50–60% of their dry weight. Upon transesterification, these lipids are chemically similar to other oilseed crop derived lipids making algae a very productive potential source of biodiesel [25]. Despite this productivity, algae biodiesel is still not yet economically competitive with petroleum diesel, with algal biodiesel at US $1.25/lb compared to petroleum-based diesel at US $0.43/lb [26].

for lipid extraction, the complex cell walls of algae prevent this pressure extraction process [28]. Optimization of direct transesterification by chemically extracting and transesterifying lipids in the same step will circumvent the need for a two-step process and can still yield a quality biodiesel [26,28]. Although there are still many processes that need to be optimized, the high biomass and lipid productivity of algae warrants continued investment in research and development and makes algae a strong candidate as a source of commercially viable biodiesel. Biohydrogen

The cost of algae-derived biodiesel is proportional to the species-specific efficiency of algae to sequester carbon dioxide as lipids. Thus, microalgal bioprospecting has the potential to greatly impact the future efficiencies, and hence reduce cost, of algae biodiesel production [25]. In particular, bioprospectors look to find strains that are not only high lipid producers but also have superior growth and harvesting characteristics [15]. For instance, Aravjo et al. found that some algal species including Chaetoceros gracilis and Tetraselmis tetrathele can grow in saline water, produce high levels of lipids, and respond to sodium hydroxide inducing flocculation allowing for easier harvesting [27]. Optimization of the transesterification process would also greatly benefit the cost of algae biodiesel production. Unlike oil-seed crops that can be compressed www.sciencedirect.com

In the past few years most algae biofuel research has focused on liquid fuels, particularly those that can replace transportation fuels such as biodiesel and bioethanol; however, algae are also a potential source of commercial biohydrogen and biogas (biomethane) used as a gas fuel or for electricity generation [29]. Macroalgae are a potential source of biomass for the production of these gases due to their fast growth rates, ability to grow in oceanic environments and their lack of the structural lignin which is typically difficult to digest [30]. Many species of macroalgae are known for having high levels of carbohydrate, although in many cases these carbohydrates consist of nonglucose monosaccharides such as galactose [30]. Recent research has shown that the red algae Gelidium amansii and the brown algae Laminaria japonica are both potential biomass sources for biohydrogen production through Current Opinion in Biotechnology 2011, 23:1–6




anaerobic fermentation, but in the case of G. amansii, an inhibitory by-product of acid hydrolysis (5-hydroxymethylfurfural) decreases the hydrogen production rate by 50% due to noncompetitive inhibition [30,31]. Thus, as bioprospecting of macroalgae for their fermentative future continues, it will be necessary to optimize pretreatment methods for maximum biohydrogen production. Photosynthetic microalgae and cyanobacteria are also able to directly produce biohydrogen through photofermentation in an anaerobic process involving oxidation of ferredoxin by the hydrogenase enzyme [32]. However, hydrogenases directly compete with many other metabolic processes for the partitioning of electrons, and not all activities of hydrogenases function equally. Thus, a significant amount of recent research on microalgae photobiohydrogen production has focused on identifying robust hydrogenase activities, understanding their interaction with ferredoxin and other metabolic processes, and genetically modify these interactions to increase the efficiency of biohydrogen production [32,33,34]. Although hydrogen production from algae still seems years away from commercial viability, continued progress in this area shows its ultimate potential. Biogas

Recently, microalgae have also become a topic of interest in the production of biogas through anaerobic

fermentation. The efficiency of biogas production has been shown to be species-dependent based on relative efficiency of cell degradation and on the presence or absence of molecules that may inhibit methanogenic archaea [29]. The production of biogas from algae may also play an important role in bioremediation as harmful algal blooms in lakes, ponds, or oceans can result in the production of toxic secondary metabolites that can have drastic effects on these ecosystems, and removing these algae for biogas production can reduce these impacts [35]. Currently, the production of biogas from algae is still limited due to the need to heat the digesters and the requirement for more land area and infrastructure to produce the same amount of energy as can be obtained for algae biodiesel [36]. Versatility of microalgae for economic success

The versatility of biofuel production from algae may provide answers to both the economic hurdles and the lifecycle challenges faced in renewable energy production. By extracting more than one type of biofuel from algal biomass or an additional coproduct, the value of the biomass increases while also offering additional offsets to the environmental impacts. As mentioned above, the combined biorefinery concept can be used to increase ethanol content from algae following extraction of lipids [20]. This concept can also be used in combination with biogas and biohydrogen production, either by producing a valuable product before fermentation or by using the gaseous

Figure 2

Bioprospecting Genetics Breeding

Water Nutrients

Pond Design Water Management Crop Protection

Strain Development

Inputs

Production

Harvest

Dewatering - recycled to inputs

Direct H2 production Co-Production Extraction

Gasoline Refining Diesel jet

Value added Co-products

Fuel Extraction

Residual Biomass

Anaerobic Digestion - Biogas Nutrient recycling to inputs Current Opinion in Biotechnology

General schematic of the algal biofuels production chain. The biggest challenges currently being investigated concerning this production chain are shown in bold. Current Opinion in Biotechnology 2011, 23:1–6

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Algae biofuels Jones and Mayfield 5

products of fermentation to power the process of producing that high value product. In the first scenario, the high value product can include biohydrogen produced anaerobically just before anaerobic digestion for biogas production [29,37,38]. In the second case, electricity generated from biogas can be used to offset the energy requirements for anaerobic digestion of microalgae during biogas production, agriculturally derived biogas can be used to provide a CO2 stream for algae growth and coproduct production, and biogas can be used to power the cultivation and lipid extraction process for algae biodiesel [36,39,40]. Regardless of the combined biorefinery concept chosen, the economic viability and environmental sustainability of the production of algae biofuels will depend on creating a completely optimized and efficient overall utilization that leaves little waste and uses every component of the algal biomass.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.

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Algae biofuels are not without limitations, largely due to the high cost of the infrastructure and the energy required for growth and harvesting due mainly to the high water content of growing algae (Figure 2) [41]. Research designed to unlock valuable biochemical molecules using enzymatic hydrolysis from the complex algal cell wall without the need to dewater the culture could have a significant impact on the energetic requirements for algae biofuels processing, as the drying of the algal biomass consumes about 69% of the input energy [42,43]. Metabolic engineering will likely play a critical role in strain development to optimize the biofuel producing strains, including improved methods for carbon partitioning, creating designer triacylglycerides through lipid chain length manipulation, and improvements in biohydrogen production through recombinant engineering [44–46]. Finally, the availability of water and nutrients to promote algal growth are important to the success of this biofuel platform both in terms of economic competitiveness and environmental impact. Recent research has shown that algae are quite successful when grown using wastewater and recycled nutrients from agricultural sources [47,48,49]. Despite the hurdles to the economically viable production of biofuels from algae, these organisms still represent one of the best options available as a source of bioenergy. Their success will largely depend on the interdisciplinary research and collaboration between engineers, chemists, and biologists that will be required to optimize the growth, harvest, and processing of these organisms to create an extremely versatile and efficient production platform for bioenergy.

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Acknowledgments SPM is a founder of and has a financial interest in Sapphire Energy an algal biofuel company, but this work should not be considered to reflect the views of Sapphire Energy. This report was supported by a grant from the US Air Force #FA9550-09-1-0336 to SPM. CSJ is a San Diego IRACDA Postdoctoral Fellow supported by NIH Grant GM06852. www.sciencedirect.com

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