Microalgae Culturing To Produce Biobased Diesel Fuels: An Overview

Article Cite This: Ind. Eng. Chem. Res. XXXX, XXX, XXX−XXX

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Microalgae Culturing To Produce Biobased Diesel Fuels: An Overview of the Basics, Challenges, and a Look toward a True Biorefinery Future Mark E. Zappi,*,†,∥ Rakesh Bajpai,†,∥ Rafael Hernandez,†,∥ Ashley Mikolajczyk,†,∥ Dhan Lord Fortela,†,∥ Wayne Sharp,‡,∥ William Chirdon,†,∥ Kyle Zappi,†,∥ Daniel Gang,‡,∥ Krishna D. P. Nigam,⊥ and Emmanuel D. Revellame§,∥ Downloaded via UNIV FRANKFURT on July 24, 2019 at 01:59:39 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

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Department of Chemical Engineering, ‡Department of Civil Engineering, §Department of Industrial Technology, ∥Energy Institute of Louisiana, University of Louisiana, Lafayette, Louisiana 70504, United States ⊥ Department of Chemical Engineering, I.I.T. Delhi, Hauz-khas, New Delhi 110016, India ABSTRACT: Microalgae is envisioned by many experts to be one of the key future feedstocks for producing transportation fuels and other chemical products. The concept has many positive aspects inclusive of being fully renewable, having minimal carbon footprint, and being able to be implemented in low value agricultural lands. There has been a tremendous amount of developmental work done to commercialize the concept since the mid-1900s; however, the reality is that the cost for a gallon of microalgae oil is still too expensive to be considered a viable option to produce biobased diesels at this time. Expanding the production of more than one or two products from a microalgae biorefinery is an economic must. Products derived from the algal cake must be developed and commercialized to offset the high cost of oil production. This paper will investigate the status of the concept and provide insight into directions needed to improve economic viability.

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INTRODUCTION The global community has long strived to move toward an energy and chemical industrial platform system based on renewable feedstocks. The US has been active for decades trying to develop viable (economically and technically) green, sustainable liquid fuels and chemical platforms that are not based on petroleum, but on biomass feedstocks. Some staggering statistics about the state of US energy needs from a global perspective are that (a) the US is estimated to contain only ∼3% of known petroleum reserves; (b) the US population only represents 4.5% of the total world population; and (c) the US utilizes approximately 20% of annual global energy usage.1 Within the US, transportation energy usage has increased by over 30% from 1950 to 2013 with petroleum usage almost tripling within this time period2 while the global energy use growth rate over the past decade hovers in the 1% to 2% range.3 Granted that recent developments in fracking technology has eased concerns over near-term energy shortages and greatly reduced US dependence on foreign sources of petroleum, the US still places a high priority on developing a realistic and stable method(s) to produce fuels and chemicals from fully renewable sources that, when combusted, do not add to greenhouse gas emissions which are postulated to represent a key cause of global warming.4 The annual carbon © XXXX American Chemical Society

dioxide emissions from the US are estimated to represent about 18% of the total annual global carbon dioxide released.5,6 It is a reality to recognize that US petroleum reserves are a finite resource that 1 day will play out thus requiring the US to have in place replacement feedstocks (and associated technologies) that are hopefully truly renewable. It is interesting to note that over 80% of the world’s energy use comes from fossil fuels (oil, natural gas, and coal) with more than 98% of global carbon emissions stemming from these three sources.7,8 Another consideration to factor into the need for developing viable sustainable fuels and chemical feedstocks is the rapid increase in energy consumption by traditionally low energy-using countries, such as China and India. Thus, vast sources of green energy that are completely renewable and their sourcing and processing both having minimal ecological impacts are badly needed as the global energy usage continues to increase over the years.3,5 Special Issue: Biorenewable Energy and Chemicals Received: Revised: Accepted: Published: A

March 25, 2019 June 4, 2019 June 18, 2019 June 18, 2019 DOI: 10.1021/acs.iecr.9b01555 Ind. Eng. Chem. Res. XXXX, XXX, XXX−XXX

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Industrial & Engineering Chemistry Research

paper will limit much of the discussion to open pond cultivation.

Even though political and policy drivers have initiated a significant development effort in the US toward establishing a viable biofuels market,9,10 progress appears to be stalling over issues such as food pricing and inventory threats along with the potential widespread ecological damage caused by expanded fertilizer usage as increased lands are brought into farming production.11−14 The recent low prices and large of stored inventories of petroleum products across the globe are also greatly contributing to the stalling of biofuels development and commercialization.3,15 Clearly, nonfoodstock based sources of biofuels need to be developed to provide a more stable biofuels industry. Among the available options for transportation fuels, the most promising appears to be biobased diesels, such as biodiesel and renewable diesel, that utilize fats and oils (aka. lipids) to produce these biofuels. Dufreche et al.16 have discussed the differences and production methods used to produce both biodiesel and renewable diesel which are chemically two distinctly different biofuels. However, they are similar in that they both use lipids as their respective feedstock into each of the two processes. Unfortunately, current lipid inventories are generally considered insufficient to meet the demands of displacing appreciable amounts of the today’s US diesel market.17,18 Additionally, lipid market prices have been for years hovering at levels that do not support their use for the cost competitive production of biofuels. Since the mid-2000s feedstock prices still represent over 70% of production costs.17−20 Microalgae-to-fuels concepts represent promising options to address the long-term energy issues detailed above.20−22 However, this potential industrial feedstock is still a developing process. Microalgae as a fuels feedstock does appear to offer many advantages over more traditional feedstocks such as oilseeds, although they still require considerable development to be more cost-effective.20,23−25 Benefits include the annual production of much more lipid volumes per acre, utilization of waste carbon dioxide in the production of microalgal biomass which serves as a biotic sink for anthropogenic carbon dioxide (a key greenhouse gas), use of solar irradiation as a light source with most culturing strategies, and the potential production of a truly sustainable fuel and chemical feedstock source. However, much more development is needed before the culturing of microalgae at large facilities becomes a commonplace industrial activity.20,24,26 This paper details the current state of the art for culturing microalgae along with an introduction to lipids and their markets, an updated overview of current culturing and processing methods, an assessment of the potential markets for microalgal-based lipids, and an assessment of potential markets that may utilize microalgal-based proteins (could be a key price offset for the lipids). The two key products from microalgae that are currently considered the two most promising marketable components of a microalgal cell grown from commercial microalgae to chemical product(s) facility are lipids and protein meal that is derived from delipified microalgal cells.20,27 This paper will focus primarily on the assessment of market opportunities for microalgae lipids, postlipid extraction meal, and whole cells. The culturing of the microalgae via open-ponds is the main growth technique evaluated within the paper, albeit the use of engineered photobioreactors is of commercial interest, the cost of producing microalgae in these systems is economically prohibitive as the lipids from photobioreactors are twice the cost of the lipids cultured in open ponds;20,28−30 therefore, this

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INTRODUCTION TO LIPIDS Lipids are a class of organic chemicals that are used by living organisms for storage of energy reserves. Plants contain oil, while animals contain fatsyet both are lipids. Lipids are often categorized as either saponifiable or nonsaponifiable.17,31 Saponifiable lipids include glycerides, waxes, phospholipids, sphingolipids, and glycolipids. Nonsaponifiable lipids include steroids, terpenes, prostaglandins, and fat-soluble vitamins. Among the lipids of greatest interest to industry are those classed as glycerides: monoglycerides, diglycerides, and triglycerides. Glycerides have glycerin backbones with fatty acids attached, respectively. Generally speaking, triglycerides are of the most industrial value because of their widespread presence in seed oils, such as soya, corn, and canola. Fatty acids provide critical chemical characteristics to the lipid. They are composed of long chains of carbons, linearly bonded via single or double bonds, and ending with the signature carboxylic grouping at the end of the chain. Fatty acids can be branched, but are most often found as straight chains in most industrial lipids of interest. Fatty acids that are composed exclusively of single C to C bonds are called saturated fatty acids. Those containing one or more double bonds are called unsaturated fatty acids. A commonly used notation for defining the chemical composition of fatty acids with regard to the number of carbons and degree of bond saturation is presented below for the fatty acid, palmitic acid as an example which has 16 carbons bonded with all single bonds (C−C): C16 The next example is oleic acid, which has 18 carbons and one double bond and is notated as follows: C18:1 Several example fatty acids of key industrial interest, including production of biobased transportation fuels, are listed below:17,31,32 Lauric acid: C12 Myristic acid: C14 Palmitic acid: C16 Palmitoleic acid: C16:1 Oleic acid: C18:1 Linoleic acid: C18:2 Example lipid sources of industrial value and their annual total gallons (lipid) per acre farming production are listed below:12,20,30,33−35 Soya: 55 gallons/acre (common US biodiesel feedstock) Sunflowers: 100 gallons/acre Rapeseed: 150 gallons/acre (common European biodiesel feedstock) Jatropha: 200 gallons/acre Palm: 650 gallons/acre Chinese Tallow: 850 gallons/acre Microalgae: approximately 1000 to 5000 gallons/acre The above-listed yield rates illustrate the growing push to move away from foodstocks, such as soybeans, toward nonfoodstock crops, such as jatropha and microalgae.20,36 Azad et al.36 list over 25 potential nontraditional lipid feedstocks that can be used to produce lipid-based biofuels. Yet, as the feasibility of turn-key crops to fuels systems is B

DOI: 10.1021/acs.iecr.9b01555 Ind. Eng. Chem. Res. XXXX, XXX, XXX−XXX

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(w/w) for most microalgae of interest are 10−25%, 20−50%, and 10−40%, respectively.20,34,49,50 Algae also contain ash and pigments both generally found in 1%−10% w/w range for most species.51,52 Vitamins within microalgae are also reported to have commercial potential.52,53 However, it is the lipid fractions that have spurred the high level of interest that continues today. The potential of microalgae for lipid production is tremendous in that the difference in land use for producing 1 kg of biodiesel is about a 150× difference when comparing soybean to microalgae.30,54 The use of highlipid producing microalgae as a feedstock for a biodiesel production operation capable of meeting 50% of the current US transportation diesel fuels needs would require only 1 to 2.5% of existing US agricultural lands or an area roughly equivalent to the land area of Connecticut.55 This compares to soya, jatropha, and palm which are estimated to need the following acres to meet the same demand: 326%, 77%, and 24%, respectively.56 This comparative land requirement coupled with the promise for significant reduction of the pricing on produced microalgae oil and increasing seed oil costs have produced a lot of excitement over microalgae as potential feedstocks for biobased fuels over the past 15 years. Plus, the use of microalgal lipids instead of a human and/or animal foodstock eliminates the ethical concern of using food for fuels. This interest is not limited to small independent private investors or governmental laboratories; large energy companies, such as Chevron, BP, and Exxon-Mobil, have been developmental players to this technology indicating the evolution of this technology development from a grass roots movement into a viable industrial R&D mission. Quite often, industrial entities with considerable production experience and capacity also have joined the ranks of microalgae developers. Clearly, such efforts exemplify the promise felt toward this novel feedstock as a realistic industrial feedstock. But, the reality still exists that the cost of a gallon of algae lipid today is simply not cost competitive.20,57 Yet, a huge amount of funding and R&D activity remains in play based on the promise that this concept holds. The scenario envisioned by most microalgae to biofuels proponents involves large microalgae farms that will produce vast tonnages of algal cells at hopefully a reasonable cost. Two microalgae production modes are currently being debated as to which is the most efficient method for microalgae culturing: open ponds or photobioreactors.20,58,59 Efficient is defined as land use, cultivation/harvesting resource needs, lipid quality, and most importantly, process economics. To date, there are no long-term operating, full-scale microalgae to liquid fuels production facilities within the US. However, upon assessing the many promising aspects of microalgae in terms of their growth and chemical character of their lipids and proteins, significant effort needs to be expended to give this high potential option its full opportunity for maturation properly.20,60 On the other hand, culturing microalgae has been commercially successful for the production of other products. Converti et al.53 reported that over 1000 tons of microalgal biomass were produced in 1999 for use as an animal feed; of this tonnage, two-thirds was used for mollusk raising and onethird used for growing fish and shrimp. The production of polyunsaturated fatty acids (PUFAs) as health supplements to both human and animal diets is a fast-growing industry that often utilizes both phototrophic as well as heterotrophic microalgae species to produce Omega III and Omega VI fatty acids as nutraceuticals.61−65

studied, one clearly sees that the level of development and associated low-risk calculations of return on investments are much more solid with the developed foodstocks as opposed to high potential, yet relatively undeveloped crops such as Chinese Tallow and microalgae.17,20,37 The fatty acids attached to the glycerin background are very often critical in terms of a lipid’s value to an industry. Lipids that have been excessively heated repeatedly (during cooking) or stored for long periods of times will break down, thereby releasing fatty acids as free fatty acids or FFAs.38 The rancid process is a classic example of a lipid breaking down. Hence, the amount of free fatty acids (or FFAs) is a very important factor determining the lipid’s industrial value. The value is defined based on the ultimate intended use of the product being manufactured and how the lipid chemistry (FFA and/or glyceride present) supports that intended use. The issue of industrial uses and respective value of lipids will be further addressed later in this document in terms of their usage in biobased diesel production. Lipids of industrial value are most often extracted from oil seeds, such as soya, canola, and rapeseed. The lipid extraction or recovery process is actually referred to as “crushing” the beans and, in reality, is either typically physically compressed out of the solid matrix or chemically extracted via a solids (beans)/liquid extraction system.39 Commonly used liquid extractants are solvents such as a hexane (most commonly used), methanol, or acetone.40−42 Physical extraction methods usually employed involve a normally loaded press or a screwed device such as an extruder that uses screwed compression to force physically the lipid out of the solid matrix.42,43 The lipid market has traditionally been dominated by industries marketing lipids as cooking oils. However, the processing of lipids into the renewable/sustainable biofuels and sustainable materials is continuously evolving. Other than the traditional use of oilseed lipids used as a cooking medium, lipids are finding their way into many new industries. Some examples evolving industrial uses of note are listed below:44,45 Biodiesel Renewable diesel (aka. green diesel or biocrude) Nutraceuticals (lecithin, Omega III fatty acids, etc.) Polymers (paints, inks, insulation, plastics, etc.) Candle wax Adhesives Heating oils Cosmetics Lubricants Many of the above industrial uses will be further discussed later in this paper because of their potential for establishing markets for the potential lipids production from microalgae. Note that most of these are generally in the early stage of the maturation process of industries/markets and as such tend to be volatile in terms of both industrial demand and associated pricing structure. However, all appear to be fast growing industries that will require significant lipid feeds as they mature.

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INTRODUCTION TO MICROALGAE Microalgae have received significant attention by biofuels proponents over the past 10 to 15 years as a potential source of lipids for biodiesel production.20,46,47 Microalgae cells are primarily made up of three major components: lipids, protein, and carbohydrates.48,49 Typical ranges of these components C


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MICROALGAE CULTURING BASICS Algae are a very common group of aquatic organisms that are well-known for their ability to grow within highly differing ecological conditions.59,66 Their size can range from a larger form, macroalgae (seaweed), to the smaller form, microalgae. The bulk of algae (referred to herein as simply microalgae) of current industrial interest can be categorized into four groups:67,68 (1) diatoms (most often associated in industrial circles for their usage in diatomaceous earth, which is a filter medium); (2) green algae or chlorophytes (commonly found in many ponds including sewage treatment lagoons); (3) bluegreens or cyanobacteria (commonly found in the same locations as green algae, they often dominant over green algae in low-oxygen tensions); and (4) gold algae. There are many other algal groups not included in the above list that are viable for biofuels production given that numerous new species are identified every year. Of these, the US Department of Energy (US DOE) has identified diatoms and green microalgae of the greatest importance for large-scale microalgae culturing projects targeting the microalgae lipids as an industrial feedstock for biobased transportation fuels.20 The key criteria used by the US DOE20 to place such importance on these two groups were high lipid content and ease of culturing (for lipid content, essentially 15% to 50% oil [w/w]). Mobin and Alam48 reviewed the current state of microalgal species for biofuels production with little change in lipids production from the 2010 US DOE Summary Report,20 but they do note new research is showing coproduct development, via microalgae components, has progressed toward potentially reducing algae biorefinery operational costs due to potential new income streams. The diatoms are best characterized by their signature silicon skeletons. They are found in both saltwater and freshwater ecosystems. There are an estimated 10 000+ species of this type known with several hundred reported new species identified each year. Green microalgae are also considered a prime candidate for use as a lipid producer within cultured systems. These hardy species generally contain slightly less lipids than do diatoms, yet they do not require silicon as a culturing amendment. Most report that these microalgae are capable of achieving lipid contents generally within the 10% to 25% (w/w) range.20,34,48,69,70 Microalgae can also be categorized through their metabolic mechanisms used to store and utilize energy as well as building biomass.71 The four main categories of microalgae that show potential are (1) photoautotrophs, majority of microalgal type used for lipid production; (2) heterotrophs, nonphotosynthetic algae (no light needed) most often used for commercially producing higher-end chemicals such as Omega III oils (nutraceuticals); (3) mixotrophs, microalgae that can use either inorganic (photosynthetic) or organic carbon sources (heterotrophic); and (4) photoheterotrophs, microalgae that require light but can utilize organic carbon (there sometimes does exist confusion between the identity of a microalgae as a mixotroph or photoheterotroph). For most proposed microalgae to biofuels projects, photoautotrophs have been used or proposed to be used. As research progresses and as algae farms become more commonplace, the other systems may become more commonly considered/used. In particular, mixotrophs appear promising because of the ability to use the two carbon source options which reduces the dependency on light; the

need for a consistently available carbon dioxide amount; and the ability to potentially utilize waste organic carbon. It is amazing to consider that the vast potential of microalgae as an industrial feedstock for commercial fuels and other chemicals is only really in its infancy.20,59,69,72 This potential of microalgae is considered by many as a “gold mine” of industrial potential. However, there are some economic realities, and hence related technical developmental challenges, concerning the process economics of culturing microalgae for use in producing transportation fuels that will be discussed in this paper.

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MICROALGAE LIPIDS

As stated earlier, the most promising algal species typically have extractable lipid contents in excess of 15%.20,34,67,73 A review of published fatty acid profiles of various microalgae considered viable for biofuels production indicates that most generally have a degree of carbon to carbon bond saturation similar to that of soy oil.8 Hence, there are no envisioned shortcomings associated with replacing soy oil with microalgae oil in terms of cloud point (cold flow) performance of the produced biodiesel.74 Triglycerides represent over 50% of the microalgal mass, and of these, they are over 70% unsaturated (i.e., double C−C bonds) which is a highly desirable lipid form for fuel production.34,75 Note that the upper lipid cell constituent percentages reported are from optimized bench studies where highly controlled conditions to allow higher lipid composition. Field efforts will generally yield lesser amounts.20 Commonly found triglycerides reported in microalgae34 contain palmitic acid (C16:0), palmitoleic acid (C16:1), stearic acid C(18:0), oleic acid (C18:1), linoleic acid (C18:2), and linolenic acid (C18:3). The bulk of the remaining lipid fractions for most microalgae species are diglycerides and phospholipids. Three biobased diesels derived from microalgae are considered viable by most experts: biodiesel (fatty acid alkyl esters), renewable or green diesel (lipids cracked within a traditional petroleum refinery), and thermo-depolymerized algal cells into a hydrocarbon liquid (aka. Bio-oils) that can later be refined into diesel cuts. In terms of biodiesel, lipids containing over 70% unsaturated triglycerides are considered good sources for biodiesel due to concerns over a final product having poor cold-flow issues.17 With renewable diesel, only the phospholipids may pose problems during refinery processing because the phosphate in the phospholipids may potentially increase the extent of coking within the cat-cracking units.76 Thermal depolymerization appears to be the most forgiving of the three in terms of it uses the whole cells with no real interference noted for processing; however, this process is also the most under-developed of the three options. An interesting aspect of microalgae lipids when compared to most seed oils is the higher level of Omega III fatty acids present. This opens up a potential separation step with some microalgae culturing operations where if high levels of Omega III fatty acids are present, then separating these high value lipids for use in producing other high-end chemicals (coproducts) may be economically viable. In fact, if these coproducts are present at significant levels, their extraction and purification can be highly profitable as nutraceutical products.77−79 D


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MICROALGAE CULTURING Microalgae need five key growth factors to reach optimized growth conditions. These factors, listed below, are critical to not only growth but also chemical composition and cultural integrity within culturing reactor systems:46,71 a Light: for supporting photosynthesis b Carbon dioxide (CO2): serves as the primary carbon source for metabolic functioning (note that most microalgae are photoautotrophs; however, some are heterotrophs) c Temperature d Nitrogen: building biochemical block component e Phosphate: building biochemical block component Microalgae growth occurs via cell division with this growth often quantified via the calculation of gross cell mass doubling time.66 Their growth within batch cultures undergoes a variety of rates and respective cell characteristics associated with the “maturity” of the batch population. Within a culturing system, controlling the growth stage or phase of the population can yield a microalgae of targeted chemical character and cell density.20,46 Often, one or more growth factors can be allowed to become limiting, which in turn can dictate the growth phase of the system and thus the microalgal cell composition (within limits). Controlling growth factors can impart a consistency to the reactor unit(s) and, as such, is a very common practice for most bacterial-based culturing systems.80 Microalgae growers have reported using very similar strategies. In fact, studies have focused on optimizing algal growth dynamics in terms of both cell numbers and within-cell lipid levels and fatty acid composition.20,67 Overall Climate. The location of an ideal land area requires a myriad of decisions often requiring a balancing of two opposing site considerations. Microalgae culturing operations require a lot of water and sunlight. Climate will also dictate temperature, which can have a significant impact on microalgae growth rate, cell composition, and even algal speciation. Hence, climate is a key decision involving the firstline evaluation of potential sites for housing full-scale microalgae to fuels farming operation. 81,82 Microalgae culturing operations can utilize a lot of water in which evaporation can be a leading cause of water loss, which is a key concern for open pond farming.20,83 The US DOE presents an excellent summary of site selection considerations when locating a new microalgae farming operation.82 Within the US, the dry, hot climate of Southwestern and semitropical Southern US regions appear to be the most competitive regions for the culturing microalgae. Wigmosta et al.84 also came to this conclusion in their evaluation of land areas within the US. The Southwestern US has tremendous solar irradiation to support microalgae culturing but faces significant challenges due to water shortages and distance to refineries (renewable diesel) and biodiesel plants. Open microalgae culturing requires a lot of water, and the dry, arid areas of the Southwestern US lose a lot of water due to evaporation and have very little water widely available for replenishing these losses.20,83 The Southeastern US has a lot of available water and high humidity, but marginal land surface solar irradiation. The relative humidity of this region is typically high compared to most areas of the US, which provides conditions with minimal evaporation and hence very limited makeup water required due to atmospheric water losses. A review of US

DOE’s Energy Information Agency (EIA) database on the locations of fuel refineries, storage, distribution pipeline networks, and power plants (CO2 sources) in the US indicates that the coastal Gulf of Mexico plains contain the highest concentration of fuels-related facilities in the US (https:// www.eia.gov). Hence, the Southern US Region appears to be particularly attractive for microalgae culturing operations. Light. Most microalgae need light photons for use in the photosynthetic metabolism of carbon dioxide.71,73 Light introduction can represent a very different challenge to any photoreaction-based system, such as microalgae culturing as compared to chemical additions (although as discussed below gaseous chemical input also can pose challenges or really limitations). The most efficient and effective light introduction that produces excellent algal biomass yields are found in engineered photobioreactors;85 however, the resulting final lipid production costs associated with these reactor systems are almost three times more expensive than those found with open ponds.20 Hence, sufficient sunlight is a must within an open pond: excessive solar irradiation can heat the pond liquids to temperature levels that can have an adverse impact on cell growth. Yet, not enough sunlight will hinder cell growth and potentially lower the water temperature to less than ideal growth temperatures. For example, the climate in South Louisiana does appear to provide more than sufficient sunlight, yet the humidity levels and summer temperatures are not so excessive to cause excessive water evaporation or overheating of the cultures, respectively. Gulf of Mexico coastal US states are located in the midlevel radiation bands based on review of solar radiation data.86 It is postulated that this solar flux is very likely to also provide near ideal conditions because this level of photonic flux coupled to a reasonable associated heating effect will give the microalgae sufficient photons for growth while not causing intense heating. Weyer et al.87 evaluated global microalgae cultivation lipid yields based on climatic conditions in five city regions around the world. They report that the theoretical limit for algal-based lipid production in these areas is 38 000 gal/acre/year; however, they predict realistic yields are in 4300 to 5700 gal/acre/year range (again, note that these high lipid yields represent estimated theoretical limits and are not likely to be hit in practice under field conditions). It should be noted that the US City of Honolulu, which was predicted to produce one of the highest lipid yields, is in a similar solar irradiation flux zone as the Gulf of Mexico. In fact, given the seasonal dry/rainy seasons within the tropics where the rainy tropical seasons are often characterized by long periods of cloudy skies, it is postulated that semitropical climates may offer a much steadier annual provision of photons over tropical areas with long periods of rainy seasons. A balance of winter temperatures and overall light irradiation needs to be balanced during site selection. Carbon Dioxide. The estimated biomass yield for microalgae with regard to carbon dioxide input is estimated to be approximately 100 tons of microalgae from an inputted 180 tons of carbon dioxide utilized by the cells.88 This microalgae biomass to carbon dioxide input dosing ratio is commonly reported in the 1.6 to 1.8:1 (w/w) range.34,88 Unfortunately, for achieving a targeted level of algal biomass in most systems, atmospheric sources of carbon dioxide alone will not meet the carbon needs for supporting the high densities of algal growth targeted for most systems (often in the 50 to 100 kg/l/day range); therefore, for most microalgae growth systems, carbon dioxide must be added (often via gas E


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increase from 20 to 25 °C cut cell lipid content in half. When temperature was slowly ramped from within the 20 to 30 °C range, the growth rates were constant until a temperature of 38 °C was hit, resulting in the halving of growth rate. Yet, the lipid content remained constant over this temperature ramping step (from 25 to 30 °C). Temperature impacts are species and culturing condition specific with many factors impacting both growth rate and lipid productivity (both bulk production and compositional fatty acid speciation); however, culturing of microalgae in the 20 to 30 °C range appears to be optimal.53,95,96 Hence, summer periods will generally yield more oil per acre than winter periods. During cold conditions, growers will need to expect a considerable drop-off in lipid production. This is why milder climates, such as the Coastal Gulf of Mexico Region in the US, tend to be ideal for culturing microalgae. It is noteworthy to mention that a key benefit of space concentrated culturing of microalgae within photobioreactors does hold the benefit of temperature control which can be used to optimize growth conditions from a temperature maintenance perspective. Macronutrients. Nutrients are key to the support of all living organisms. With microalgae, nitrogen (N) and phosphorus (P) are the key nutrients that are often referred to as “macronutrients”. Nitrogen in particular is a key nutrient in that studies have shown that “starving” algal cells of nitrogen can dramatically induce lipid production by as much as 4fold.97−99 Others report that starving both nitrogen and phosphorus will stimulate higher lipid fractions in microalgae.95,100,101 There is evidence indicating that sulfur is another nutrient that when microalgal cells are starved on this chemical, cell lipid content also increases.102 In fact, Cakmak and company102 reported that when nitrogen starving is used, the cells do exhibit an increase in lipid content, but recover to prestarved levels upon restoration of normal nitrogen dosing; however, they note that sulfur starved cells continue to produce higher lipid fraction much longer after returning sulfur dosing to prestarvation levels. When using nutrient starving, although the lipid levels may increase, the growth rates are likely to decrease. These two opposing effects must be balanced when attempting to optimize a microalgae culturing system.53,103 Therefore, for short-term enhancement of lipid content, nutrient starving is viable as long as the biomass concentration remains stable, but long periods of starving may reduce biomass levels. This is a balance in terms of nutrient dosing strategies that must be optimized for each unique bioreactor situation. Macronutrients are typically delivered as specified carbon to nitrogen to phosphorus weight ratios (often referred to as the C:N:P ratio), but with phototrophs, the lipid or biodiesel product aspects of the “C” or dry produced biomass are often used instead of input carbon (a gas in the case of a phototroph). Yang et al.83 report that for 1 kg of biodiesel, 0.33 kg of nitrogen and 0.71 kg of phosphate are needed to support a healthy microalgal biomass for this level of lipid production. Note that biodiesel yields to nutrient inputs ratios presented by Yang et al.83 are based on stoichiometric calculations that the authors utilized to estimate these ratios based on the work of others: the ratios as presented are dependent on the actual lipid yield achieved. Rogers et al.21 suggest that a good C:N:P (w/w), with the “C” in this case being dry cell mass, is a ratio of 525:92:13 (w/w) or when unitized with respect to the dry biomass, 1:0.18:0.021. Pate et al.104 report agreement with this ratio, suggesting a dry-algal

sparging). In fact, Putt et al.89 suggest that atmospheric carbon dioxide only provides 5% of the required carbon dioxide for high-rate open ponds. Ideally, the sources for the carbon dioxide should be waste gases such as those produced from power plants or localized processing equipment (generators or dryers). These sources offer the farm cheap sources of carbon dioxide (perhaps free) while offering these facilities a potential method for removing the carbon dioxide from their waste gases that will help them with their efforts to reduce greenhouse gases. The actual percentage of carbon dioxide needed within the feed gas streams can vary based on the available gas source. The upper limit for carbon dioxide concentrations (often reported in percentage of input gas [v/v]) that begins to cause algae inhibition was reviewed by Salih90 who determined these levels to be well beyond 30% and even as high as 80%. Almost all sources of combustion-based candidate carbon dioxide sources, such as power plants, driers, natural gas processors, ethanol plants, and internal combustion engines, produce waste gas streams that contain many more compounds (inorganic and organic) other than carbon dioxide.89,91 Numerous carbon dioxide bearing waste gases have been tested by various research groups with no groups reporting significant inhibition.92,93 A drop in pH was reported which does indicate the need to ensure that culture system solutions remain within an acceptable pH range which often is neutral (∼7.0) except for systems using elevated pH levels to maintain species purity.92 Note that since carbon dioxide is a gas, the mass transfer of the gas into solution−particularly in open ponds with shallow troughs−can be challenging (see the reactor design section of this paper for more discussions on this issue). There are new developmental works that are indicating the carbonates may be used as a liquid source for inorganic carbon in place of carbon dioxide (water solutions containing the carbonate species). The use of carbonates will eliminate issues with finding carbon dioxide sources close to the planned algae culturing site and mass transfer challenges of transferring the carbon dioxide gas into the culture water. Hanifzadeh et al.24 compared the culturing of Chlorella vulgaris (a green microalgae) within very small raceway ponds (450 L) using carbon dioxide versus sodium bicarbonate (NaHCO3). They concluded that the bicarbonate dosed systems can cultivate the microalgae at reduced cultivation and energy costs by ∼50% and ∼80%, respectively. However, much more work needs to be done in the area of using carbonates in place of carbon dioxide since the carbonates could impart issues relating to destabilizing the pH of the culturing system and scaling within the process equipment. Also, costs could increase using a real commercial scale assessment. Nevertheless, the use of carbonates is a promising option. Temperature. Most of the microalgae to fuels systems, particularly open pond systems, have temperatures controlled by seasonal conditions caused by solar radiation hitting the pond surfaces. Warm temperatures yield high growth rates with colder temperatures often slowing down cell metabolism resulting in lower growth rates and lipid production.94 Most research indicates that aqueous culturing media temperatures up to 40 °C do not significantly impact overall lipid production. But, higher temperatures are not always good for microalgae culturing. Converti et al.53 found that slight increases in temperature using a 20 to 25 °C step did result in reduced cell lipid content for a microalgae (Nannochloropsis oculata). They also report that with Chlorella vulgaris, an F


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process water is not recycled. They further conclude that using a combination of seawater and wastewater effluents can reduce fresh makeup water use by 90%. They also suggest that the almost complete recycle of the process water can reduce water usage down to 581 kg water/kg of biodiesel produced. Harto et al.110 evaluated various alternative energy options in terms of water usage using a life cycle analysis. They conclude that switchgrass to ethanol systems that use irrigation had the highest water usage (∼10 gallons per vehicle miles traveled [VMT]) followed by corn to ethanol and algae culturing in an arid climate using open ponds being tied (∼3 gallons/VMT) as the next most water-intensive options. They also concluded that switchgrass raising with minimal irrigation over full irrigation reduced water usage by more than 1 order of magnitude. Additionally, they concluded that photobioreactor culturing of algae uses half the water volumes compared to open pond culturing. Without process water recycling at open pond system microalgae culturing operations, water losses are 84% discharge and 16% evaporation losses.83 Hence, even with recycling, approximately 15% of makeup water will be needed because of evaporative losses (the actual amount is dependent on the time of the year and climate conditions). Most open ponds are lined, so seepage losses are negligible. There likely may exist a limitation to the number of cycles used during process water recycling that can be used due to the buildup of growth inhibitors within the reused water. Limitations on the number of process recycles were reported by others for the culturing of microorganisms.111,112 This issue would have to be addressed for each unique culturing system, but it does represent an opportunity for water savings as well as potential disruption of targeted microbial activities if adverse impacts are not carefully checked. As mentioned earlier in this article, the use of wastewater effluents as a water source offers an interesting option to reduce the cost of nutrients and to reduce greatly the amount of water needed to be removed from the region.104−107 Lutzu and Dunford113 suggest that oilfield wastewaters are an option for consideration in that these oilfield operations produce huge volumes of these wastewaters per year needing disposal. Limiting the usage of regional water assets is particularly of great benefit in arid regions such as the Southwestern US where water resources are not plentiful and quite a valuable resource. Algal Species (Cultures). The actual algal culture to be used within a microalgae culturing system is a critical decision to be made. This decision should be based on climate, reactor type, and target cell constituent(s), such as lipids, proteins, or Omega III fatty acids. The discovery of the “perfect” microalgae has not been reported for universal use or even arguably one species even being “ideal” for a given system.48 A good microalgae strain will have a high lipid content (preferably mainly triglycerides), rapid growth rate, solid competitor within the bioreactor ecology, cheap to culture, and the delipified cake containing a large amount of marketable, value-added products.20 The selection of a microalgal strain for a particular large-scale culturing operation often requires finding a balance of these three factors: amount of lipids in the cells, reasonable growth rate, and species purity stability. Often times, a strain may have high levels of lipids, but a slow growth rate.49 When nutrient starving is used, then this deficit likely also causes a reduced cell (biomass) growth rate53 presenting the lipid level versus cell growth decision discussed earlier. Also, the reactor ecosystem needs to keep a high relative population of the targeted microalgae which means

biomass based C:N:P of 1:0.18:0.024 on a molecular weight basis (based on the C, N, and P mass composition of the source molecules). The titling of nitrogen and phosphorus as “macronutrients” provides the inference that there are micronutrients (S, Si, Co, Fe, Mo, etc.), which is indeed the case, but often the commercial fertilizers used have enough trace amounts of the micronutrients to support growth. Some micronutrients can also be introduced via some other introductory conduit such as the wind introduction of dust for open systems. One negative aspect of culturing microalgae for biofuels production using commercial fertilizers is that when a life cycle analysis around the algae-to-biofuel concept is compared to oilseed-to-biofuels concepts, the microalgae route uses significantly more nitrogen nutrient (and often from petroleum-derived commercial fertilizers via the natural gas used to produce the fertilizers) than does the oil seed-based systems.105 It was also noted by Lam and Lee105 that commercial fertilizer operations are one of the largest contributors to greenhouse gas emissions. Research teams are now evaluating the potential of using wastewater effluents as a source of nutrients and water for sustaining microalgae culturing operations.105−108 This option is promising, yet there are issues pertaining to introducing microorganisms, such as bacteria which are prevalent in wastewater effluents (unless disinfected which can cause other issues, particularly if chlorine is used which is the predominant disinfection agent within the US). By having bacteria and other microorganisms in the effluents coming from the wastewater treatment facility, there exists a good potential for establishing an invasive bacterial population within the microalgae culturing systems that may utilize valuable culturing resources (ex. nutrients). A significant population of invasive (nontargeted microbial species) could shut-down the targeted beneficial microalgae culturing operations due to the introduced invasive microorganisms out-competing the microalgae for supplied nutrients and other added growth factors. However, the option of using wastewater effluents as both nutrient costs and water usage can enhance the sustainability and ecological footprints of both the wastewater producer (cities and industries) and the microalgae cultivation farm while also reducing the cost of producing algal lipids due to reduced nutrient dosing costs.108,109 This option can also dramatically reduce water usage. Christenson and Sims109 listed the nitrogen and phosphorus typically found in a suite of wastewater sources with the wastewaters from confined animal raising facilities having a huge potential to provide significant amounts of macronutrients. Within their study, it appears almost all of the wastewaters they listed showed a high potential to meet the needs of culturing typical microalgae to fuels system. Process Water. Water represents the primary culturing media for microalgae. However, this is concerning given that the US is already experiencing significant water shortages or pending shortages. Wigmosta et al.84 report that microalgae to fuels is one of the highest water users in the developing biofuels arena. They show that an average ethanol-based biofuel needs 66 L water/km driven, while a soybean-based biodiesel needs only 19 L water/km and algae-based biofuels needs range from 20 to 118 L water/km driven. Pate et al.104 state that in 2005, the US used about 350 billion gallons of water (37% of this usage was attributed to crop irrigation). The culturing of microalgae is water-intensive. Yang et al.83 state that for every kg of biodiesel produced from a microalgae to fuels system (open pond), 3726 kg of water is needed if the G


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Figure 1. Simplified process flow diagram of a microalgae to fuels and other chemicals system.

Reactor types for microalgae culturing are often classified as either open pond or photobioreactor systems.20,21,28,30 In either case, the reactor employed must be able to supply effectively (cost-wise and operationally) the growth factors and ecological conditions detailed above at a sufficient rate within reasonable capital and operational cost regimes. The typical process flow diagram for microalgae to fuels and other chemicals in a production facility is shown in Figure 1. It is interesting to note that among the strong proponents of microalgae as a future feedstock for fuels there exists a sharp divide as to the appropriate type that must be used for culturing microalgae intended to serve as a fuel feedstock. No matter the reactor type used, other than the supplement of the growth factors, issues that also need attention include minimal mixing (to expose adequately the entire biomass to light and mix supplied nutrients), some protection strategy for maintaining cultural integrity (via ecological conditioning, highly dominant speciation exclusion, or physical isolation using some barrier), and ease of adaptability for the support of biomass harvesting. Of course, the key aspect of reactor performance of most importance is the amount of product produced per volume of reactor (typical units are weight/ volume unit or pounds per gallon) or in the case of most open systems, the amount of product from a per surface area metric (typically units are weight/area or pounds/ac), plus the most important result: the cost of the lipids and secondary products. With regard to biofuels, the products of most interest are lipids (oil) and the resulting high protein microalgae cake.20 To achieve this, reactors must provide optimized growth conditions and most often support a single target algal species (monoculture). Open Pond Designs. Open pond systems (aka. raceways or high-rate ponds) are typically designed using a shallow earthen basin that may or may not be lined. These open ponds are referred to individually as a raceway because of the usual elongated layout with semicircular ends.21,28,114,115 Sewage lagoons that are square or circular can be used for microalgae production, but these systems are not generally considered viable options for mass production of algae to fuels and chemicals because of their less than ideal designs and operations capabilities.116 A raceway configuration is a commonly used design which is essentially an oval open ditch system with a paddle wheel bridged over some portion of the track to facilitate mixing and/or carbon dioxide introduction.21,117 Lundquist et al.116 report that over 4000 tons per year of algal biomass is produced globally each year with most being cultured in raceway systems. Chisti35 reports that this design has been used since the 1950s with the largest facility being over 440 000 m2. Excellent drawings of raceways

that the culture or species integrity of the reactor must be maintained. A reactor system that has multiple microorganisms competing for reactor resources that do not all produce acceptable levels of lipids while also maintaining appreciable growth rates becomes a failed system. Most often, competing, nonbeneficial organisms are introduced through some biological contaminating vector. With open systems, maintaining the integrity of a single isolate is much more challenging than within closed systems. This is so because open systems are highly exposed to many contamination vectors (bacteria introduction via wind driven particles and/or bacterially active water input). However, there are several operational strategies that may be employed to maintain a reasonable level of cell integrity (defined from a call culture purity perspective). Examples include continual seeding, nutritional selection, pH, and/or temperature controlling. As stated earlier in this article, most microalgae to fuel efforts have rightfully focused on either diatoms or green microalgae. Yet, as more development takes place, there may be other microalgal species that may prove to be good options. It is correct to state that the bulk of microalgae species currently used in all operating and planned systems are green microalgae. However, it cannot be overstated that tremendous improvements are being researched that may yield the discovery and optimization of better-performing microalgal species for future commercial culturing systems. There have been and continue to be many solid research investigations into the discovery, optimization, and commercial utilization of reasonably performing microalgae species. Literally hundreds of microalgae species have been reported to offer possibilities for use in an algae to biofuels systems since the 1990s.20 Example algae cultures that have been reported to perform well for algae to biofuels systems include species from the following groups:20,32,48,68,71,96 Chlorophyta (green algae), Bacillariophyta (diatoms), and Cyanophyceae (cyanobacteria). Example algal species of note that have been commonly reported to produce solid lipid yields are (>20% dry weight as lipids) Botryococcus braunii, Chlorella emersonii, Dunaliella primollecta, Nannochloropsis oculata, Neochloris oleoabundans, Chaetoceros muelleri, Phaeodactylum tricornutun, Chlorella vulgaris, Chaetoceros calcitrans, Chlorella minutissima, Chlorella protothecoides, and Pavlova salina.

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ALGAE BIOREACTORS Bioreactors are constructed systems that provide reactor ecologies within the systems that are conducive toward supporting targeted biological activity. In the case of microalgae, it is the support of culturing activities toward a single algal species or group of species (aka. consortium). H


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Industrial & Engineering Chemistry Research are presented in the literature.21,117,118 Superficial or planar surface areas of the active area of individual ponds are often reported in the 0.1 to 0.5 ha range. The dimensions for length, width, and water depth of a raceway lane reported generally fall in the following ranges: 40 to 650 m, 1.5 to 30 m, and 10 to 60 cm, respectively.21,116−121 The depth of the channel should be not too deep as to allow sufficient sunlight penetration in support of photosynthesis while also facilitating effective mixing (deeper channels are harder to initiate mixing turnover). Lane length to width aspect ratios (L/W) are often in the ∼3:1 to 15:1 range.121 Note that Hadiyanto et al.121 suggest that the optimal L/W ratio is 10 in terms of reducing dead zones and saving power. The paddle wheel mixer is often used and is simply placed over the channel (as a bridged structure) and mechanically turned to achieve a desired superficial channel water velocity. The channel crosssectional velocities are kept high enough to ensure adequate mixing is provided via vertical and horizontal mixing eddies (caused by low-energy turbulent flow) of the microalgae, which should offer exposure of the total biomass to the sunlight. Yet, the flows are low enough to not expend too much energy.118,122 Channel cross-sectional velocities reported to be successfully used are in the 10 to 50 cm/s range.121,123 These velocities, selected based on biomass density and algal cell size, are used to keep the algal solids from settling and thus cause them to “roll-over” to maximize exposure of the total algal biomass to sunlight. Many of the suggested raceway designs included vanes within the two curved ends to facilitate a smoother turn to reduce energy costs. Recent work by Liffman et al.122 focused on energy savings through improved raceway end configurations using computational fluid dynamic modeling which indicated that the use of progressive bends resulted in mixing energy savings in excess of 80%. The microbial biomass solids concentration supported in these units are generally in the 200 to 1000 mg/L range with 200 to 500 mg/L representing the solids concentration most often reported.35,124−126 Superficial algal yields as high as 70 g/ m2/day have been reported with a range of 10−40 g/m2/day being most often reported and also being considered reasonable to sustain process feasibility.20,71,89,91,104 Cell yields based on reactor volume in the 0.02 to 0.2 g/L/day range are commonly reported.35,71,123,124 Carbon dioxide is the most used source of carbon for the photoautotrophs. The most common delivery method is gas spargers placed along the bottom of the channel floors.89,123 This somewhat goes against traditional gas sparging design rules of thumb where often bubble rises in excess of 10 feet are targeted;127 however, the “sinks” provided by high density microalgae blooms apparently do present enough concentration gradients to facilitate reasonably effective transfer since many successful microalgae culturing systems have employed bubbling as a means of introducing carbon dioxide. However, using this design does result in significant loss of carbon dioxide with numbers as high as 80−90% wasted being reported.89 Ketheesan and Nirmalakhandan123 proposed an airlift design that provides mixing within the channels while also introducing the carbon dioxide. They report an energy savings of 80% over paddlewheel mixing and an effective introduction of the carbon dioxide. Putt et al.89 discuss a variety of improved carbon dioxide methods for open ponds inclusive of gas-lifts, sparging pits, and bubble columns. Putt et al.89 suggested that a side bubble column is an excellent option. As mentioned above, if carbonates do become more commonly

used, then the mass transfer and sourcing issues associated with carbon dioxide will be eliminated. Yet, complications with pH control and scaling of process equipment may become issues with carbonate use. Positive aspects of raceway open ponds are low capital costs, relatively simple ease of operation, availability of fairly mature design protocols, utilization of off-the-shelf components, evaporation provides some cooling effects, and algae lipids are produced at almost half the cost for photobioreactorproduced lipids.118 The primary negative aspect of raceway open ponds is the difficulty associated with preventing algal species contamination due to the openness of the units (i.e., maintenance of a monoculture), maintaining optimal light exposure, being exposed to atmospheric conditions, introduction of solids via dusting, and evaporation water losses that can be significant in arid regions.118 Closed or Engineered Photobioreactors. The use of engineered photobioreactors to concentrate the culturing of microalgae into a less land intensive operation has been the topic of a tremendous amount of work over the past 20 years.128,129 These specially constructed, closed reactors have been proposed using a wide variety of configurations that all provide optimized reactor conditions for the support of much heavier biomass concentrations than are obtainable using open ponds. Reactors of this type are used to culture either photoautotrophs (needs light) or heterotrophic microalgae (does not need light). For sake of this discussion, only photobioreactors will be discussed in this paper. A variety of photobioreactor designs have been proposed and successfully tested.129,130 They all have been designed and operated to provide optimized conditions for culturing dense biomass concentrations containing high levels of lipids.130 Greenwell et al.131 argue that photobioreactors or combinations of photobioreactors integrated with open ponds represent the largest potential to mass produce microalgae for fuels production. Three primary volumetric-shape configurations are most commonly used: standing systems (flat plate and standing columns), tubular (horizontal, vertical stacked, and inclined), or pillow (horizontal rectangles and cylinders) designs.132,133 A review of the literature indicates that photobioreactors have been used for commercial purposes but often on a production scale much lower than associated with open pond systems.130 The process footprint of the photobioreactor systems is much smaller than open pond systems. Ugwu et al.130 listed size and performance data on a variety of commercial/research photobioreactors. They state that the largest system within the group was 25 000 L with several in the 200 to 400 L range reported. They also list that the microalgae biomass growth rates obtained in these reactors ranged from 0.05 to 2.7 g/L/day. Posten133 reports that the world’s largest photobioreactor is found in Germany at a scale of 600 m3 of active reactor volume. Most photobioreactor designs utilize light transparent construction components to allow maximum sunlight photon access into the biologically active part of the reactors for the sustaining of photosynthesis.129,134 Hence, glass, Plexiglas, polyvinyl chloride, and polyethylene (most common) all are good materials of construction.134 Some photobioreactors use immersed fiber optics or artificial light for the supply of the photons to support photosynthesis within the active reactor volume.135 Ono and Cuello136 evaluated the potential of a solar thermal concentration system as a means of increased photon production coupled to a fiber optics tube system that I


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such as lakes or seas.144,145 This floating design does not compete for land area and offers thermal-buffering assistance provided by the water. Often times, these systems are designed as long pillows or tubes.129 The positive aspects of photobioreactors are a high level of system controlling and access to maximize production, an appreciably smaller land process footprint, the opportunity to produce other products within the reactor (such as Omega III fatty acids), and a much easier system for controlling culture integrity (preventing invasive, nonbeneficial microbial cells from being established within the reactor). The key negative aspect is higher cost for the lipids due to the much higher need for manufactured components, increased operational complexity, and difficulty with producing a large-scale system given the small reactor diameters/widths required. Lam and Lee105 report that the power use costs associated with photobioreactors are approximately 1 order of magnitude more costly than the costs reported for open pond systems (∼30 vs ∼300 GJ per ton of biodiesel produced).

was immersed into a photobioreactor. Their evaluation indicated a positive aspect to this design, but more development was needed. A key design parameter for photobioreactors is the illuminated surface area versus total reactor volume or S/ V ratio.129 The higher the S/V ratio, the higher the biomass yields due to optimized photoefficiency toward algal cell exposures; however, there become limitations to S/V ratios when constructing photobioreactors at a large scale (commercial applications). Some photobioreactors are placed outdoors so that the sun can provide the light needed for the phototrophs while other photobioreactor systems are placed indoors where artificial light sources are used. These artificial light sources are often optimized for a photon emission range that is within a band that supports a high degree of cell photon absorbance. Studies have shown that blue light (450−470 nm) and/or red light (645−665 nm) emissions are the most optimal wavelengths for microalgae cultivation;137 therefore, some projects are focusing on the use of LED lamps that emit these two color emission bands as potential light sources. In fact, only 50% of the sun’s irradiation (400 to 700 nm) is usable for algae cultivation.134 Posten133 reports that the maximum conversion of light photons into chemicals via microalgae within a photobioreactor is estimated to be less than 10%. The orientation of the overall photobioreactors in terms of position to the horizontal ground is another design consideration. Often times, a horizontal system is used except for some sections of vertical or inclined orientation to facilitate improved gas transfer and/or light irradiation depending on geo-positional latitude with regard to solar irradiation. Tubular systems appear to be the reactors that are most commonly proposed/used for microalgae cultivation.129,133,138 Often times, these reactors use a serpentine tube run design to minimize process footprint, maximize light source exposure, and facilitate improved mixing. Common tube diameters are in the 5 to 60 cm range with lengths in excess of hundreds of meters reported.133,138−140 Tube systems can be designed as fully horizontal or vertical or somewhere in between. Fluid pumping rates used within the tubes reported are in the 20 to 50 cm/s range.139 Biomass concentrations as suspended solids are reported for these systems to be as high as 6000 mg/L.133 Mohamad138 claims that biomass concentrations could even reach levels as high as 30× those observed in open pond systems. Some research teams claim that the simplicity of the standing systems in the form of the flat plate design makes them the most robust system of the three designs.133 The suggested width of the two plates making a flat plate system is on the order of 10 cm to ensure effective light exposure. Biomass concentrations as high as 10 000 mg/L as dry solids are reported. Column systems are often configured using 40 to 50 cm diameters and heights in the 2 to 6 m range. Gases are introduced using sparged or gas-lifted introduction. The removal and management of the oxygen generated during photosynthesis is another design consideration unique to photobioreactors over open ponds. This produced oxygen volume has to be removed while keeping injected carbon dioxide within the reactor as long as possible. In some cases, dissolved oxygen can hinder microalgae growth.141 Pillow photobioreactors involve more compact volumes and process footprints due to the larger diameters used.129,142,143 Albeit not a commonly proposed design, there has been some work with these systems as floating photobioreactors have been used to allow for the culturing of microalgae within open water bodies

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HARVESTING AND DRYING OF ALGAL CELLS The harvesting of the microalgae crop is done via the transfer of reactor water into the separation and drying processing steps as a means of increasing the cell solids concentration to an acceptable solids level, which can be very costly.96,146 The processing steps for dewatering/drying start with fresh harvested microalgae suspensions collected from the culture reactor at a dry solids range 0.02% to 0.05%, which is often dried to over 85% as dry solids. This dewatering and drying step is one of the most energy intensive steps within the overall algae to fuels/chemicals process.147−149 Before dewatering, the microalgae suspension within the open pond or photobioreactor must be harvested.108,146 This is typically done by collecting reactor water and pumping or gravity feeding the water into the dewatering system. Biologically active pondwater removal is often performed on a per reactor basis using some preset harvesting frequency based on the algae cell growth rate. In some cases, a chemical flocculent is added to accelerate the dewatering process.108,109 For the actual dewatering of microalgae slurries from a culturing reactor, commonly used equipment include centrifuges, clarifiers, screens, filtration, and flotation.147,150 The operational experience tied to sewage sludge dewatering has provided a significant knowledge base now used for algae dewatering. Of the several options listed, centrifuges work well with microalgae separation, particularly those centrifuges used for sewage sludge densification. Centrifuges are the most often proposed options for algae dewatering.151,152 Albeit, this option tends to be the most energy intensive but oftentimes the least labor-intensive. Additionally, filter press systems that utilize flocculants and other dewatering enhancing agents (polymers) also have worked well with algae and have been successfully used.153,154 In either case, dewatering to levels between 15% to 30% solids is achieved using either of these systems.155,156 Other harvesting processes have been used or are being studied147,157,158 with none of these being proposed as often as centrifuges and filters.105 Hopefully with continued development, cheaper methods for dewatering will emerge that will reduce the overall cost of algae lipids (oil). Extraction and fuel processing methods used with microalgae often require a fairly dry algal cake (at least 85% solids); hence, drying is a major consideration within the overall process due to the large amount of heat needed to go from J


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Industrial & Engineering Chemistry Research ∼20% dry solids to over 85% dry solids.105,155 A wide variety of commercial driers has been used or proposed for use in the drying of microalgae.153,159,160 Some smaller operations have used simple air-drying,161 but in most commercial-scale systems, this option is very land and processing time intensive. Depending on the lipid extraction system used, targeting of final solids levels for the final algae cakes at or above 90% is not uncommon.162,163 Example systems include rotary dryers,164 spray dryers,165 freeze-dryers,166 conveyor dryers,159 drum dryers,162 sun drying,59 or even solar-powered dryers.153 In essence, other than the capability to achieve targeted solids concentration (often being at or beyond 90% solids), costs are by far the most important parameter (of course, thermal breakdown of proteins is to be considered as well, but most economical systems do not heat to that level for economic reasons). In fact, drying costs can represent as much as 60% of total processing costs.153,167 Also, the drying of algal cells is the main contributor to the release of green-house gases from microalgae to fuel system operations.151

microwaves to facilitate hexane extraction. Their results indicated some promise; however, the extent of lipid extraction was not appreciably better than the extraction efficiencies reported by others using hexane alone. Their results did indicate the potential to reduce extraction contact time and potentially reduce hexane use. In reality, since there is very limited operational experience with a large pilot or full-scale algae to fuels operation, the actual cost and success of applying a lipid extraction method within a reasonable cost range are difficult to assess. With the other processes from cultivation through to drying, there is enough full-scale operational history with other similar living cells, such as sewage sludges and whole algal cake production, that the design and operational parameters for these processing steps prior to lipid extraction are generally well understood and can be extrapolated to the algae to fuels case. Lipid extraction is more challenging since there are only a few commercial experiences in the case of algae and these operations are not openly shared within the literature. Hence, lipid extraction via a cost-effective methodology will be a key challenge for those wanting to enter this industry. Estimates for extracting oil from microalgae are about 2 to 3 times the cost of extracting lipids from oilseeds. A developing process that may be used for lipid extraction is supercritical fluids, such as carbon dioxide or propane. Albeit supercritical extraction is very much a developing process for large-scale lipid extraction, it can be coupled with trans-esterification reactions under the supercritical conditions to produce simultaneously biodiesel during extraction. Finally, customizing solvent extraction via the formulating of the extraction fluid (i.e., using polar or nonpolar mixtures) can provide the exclusion of some unwanted lipids or conversely the capture of others (some be of high market value such as Omega III oils).

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LIPID EXTRACTION A wide variety of extraction methods have been proposed for extracting lipids from algae.20,163,168−171 The two most commonly used extraction techniques for lipid extraction of oilseeds are pressing and chemical extraction. The use of chemical extractants as stand-alone or combined extraction strategies offers the algae producer the ability to potentially extract multiple products other than nonpolar lipids such as pigments, polar lipids (lecithin), and proteins.163 Note that prior to most extraction efforts, some form of algal cell disruption is suggested and often used to improve lipid extraction efficiency.59,71,169 However, no one cell disruption method is widely agreed upon to be the best for algae extraction. Bead milling, chemical osmotic pressuring via NaOH solutions, microwaves, and sonication have all successfully been used (albeit, mainly in laboratory and pilot scale tests). For most algae applications, chemical extraction appears to have been the process of choice.42,59,155,168,169 The extraction systems used are generally similar to soybean crushing facilities (chemical extraction via hexane) except higher solids concentrations are used.155,172 For smaller fish feed oriented operations using microalgae as fish feed components, nonchemical facilitated pressing has also been used. These pressing systems are based on physical pressurization (actually an extruder) or normal pressurization (truly a press). As microalgae operations are expected to yield high volumes of lipids for bulk fuel production, chemical extraction is a likely choice for the lipid extraction step. Chemical extraction systems use solvents, such as hexane, simple aromatics, primary alcohols, or ketones, that all have high solubilities for lipids. The actual composition of the chemical extraction solution(s) will vary based on if only nonpolar lipids are targeted or if polar and nonpolars are of interest.42,156 However, in general, hexane appears to be the solvent most proposed and/or used. Xu et al.155 report hexane losses in the 2.4 g/kg of dry algal cake extracted with lipid extractions exceeding 95%. With these systems, intimate contact of the microalgae with the extracting agents is accomplished followed by the separation of the solid and liquid phases (often via a filter press). In some cases, ultrasonic and microwave processing are used to facilitate improved extraction via cell disruption and lipid disassociation.71 Balasubramanian et al.163 evaluated the use of

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OIL PURIFICATION

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THE REALITIES OF ALGAL LIPID COSTS

Since the lipid industry essentially is based on the cooking or food oil industry, over the years, the aesthetic value of an oil has been a key aspect of developing/maintaining a market. Albeit oil purification is often performed for improving visual aspects, in some cases, poor tasting and/or low quality components are also removed.173 In the biofuels industry, oil purification is performed to meet fuel standards, such as phosphate levels for example. In the case of fuels, often degumming (removing polar lipid fractions and free fatty acids) is the key processing step done.174 The extent of degumming or any other purification processing is almost a case-by-case issue for the more novel oils, such as microalgae.175 Depending on the fuel type targeted, the reduction of the extent or elimination of purification processing could yield minor costs savings if the final fuel product or its processing method are not adversely impacted by the presence of certain chemicals, phosphates, chlorophyll, etc.

Techno-economic analyses (TEA) of producing microalgal lipids have been done over the past few years. Most TEAs conclude the total production costs for the lipids to be in the $8 to $12/gallon and $15 to $20/gallon of lipid produced ranges for culturing in open ponds and engineered photobioreactors, respectively.20,28,116,176−180 The higher costs associated with the photobioreactors are associated with high capital and operational costs tied to these more complex and K


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cost investment to not develop strong markets for the delipified algal cake. Lipids. A great need in the biobased diesel industry clearly exists for chemically accepted lipids that are sold within a competitive price range against seed oil prices, such as soya oil.16 There is instability in the future of biobased diesel fuels due to low petroleum prices and competing first and second generation biobased diesels: biodiesel vs renewable diesel.16 Additionally, there are a number of potential markets for the microalgae lipids, other than as a feedstock for fuels. Example markets that may be developed for microalgae lipid fractions include serving as feedstocks to the production of polymers, nutraceuticals, and lubricating oils. The actual market potential of the lipids will be dependent on the actual chemical composition of the oils produced. However, there are a number of fully matured lipids that come from oilseeds and meat-based sources.17 Therefore, it is important to track the pricing of these other lipid sources. The current pricing of lipids currently available within the US that may compete with microalgae oil generally is hovering in the prices listed below:185−189 Soy: ∼$0.30/pound Rapeseed: ∼$0.80/pound Cottonseed: ∼$0.50/pound Peanut: ∼$0.55/pound Tallow: ∼$0.45/pound Corn: ∼$0.45/pound Sunflower: ∼$0.60/pound Canola: ∼$0.35/pound Tallow: ∼$0.30/pound The dramatic decrease in petroleum prices over the past couple of years cannot be overlooked as well. These prices will continue to increase pressure to reduce the per gallon costs of all biomass-based fuels. During the period ranging from 2008 to 2013, high oil and natural gas prices initiated a tremendous global push toward renewable fuels that can provide some level of energy independence for the US at a fairly competitive cost potential. However, current low prices are greatly hindering industry interest in algae-based fuels (and federal funding interests as well). Yet, as this paper has attempted to show, there is a vast potential to produce green vehicular fuels and other coproducts from algae-lipids. Also, it is becoming a widespread policy opinion that importing seed oils will no longer be as easily accepted for receipt of heavy government subsidies and hence federal and state government incentives may be reduced or even eliminated; this will only put more pressure to develop domestic sources of lipids. In summary, if a microalgae to oil facility can produce a reasonably priced lipid product with the expected lipid chemistry, then a very solid market for their product should be already in place, no matter if biodiesel or renewable diesel becomes the dominant biobased diesel product. Hence, this scenario should provide microalgae to product processors significant product sales flexibility as these markets mature. But, current per gallon pricing will maintain a drag on market developments with this impact directly tied to petroleum prices and government policy initiatives. Microalgal Cake. The development of a stable, high paying market(s) for delipified algal cakes is critical to making microalgae to fuels/chemicals an economically feasible industry because after all of the funds and labor are expended only 20% of these investments are the lipids. Hence, if the

engineered systems. Other TEAs, often using slightly more optimiztic process parameters, present evidence that lower microalgal-based lipids production costs are possible.108,181−183 These lower estimated costs are mostly tied to the parameters of increased lipid productivity, higher biomass yields, and/or reduced cap costs. A per gallon of lipid cost sub-$4/gallon is a US DOE target to place microalgae-based fuels as being economically feasible.184 Recent TEAs are indicating promise to reach competitive lipids, and in turn, biofuel prices. Hoffman et al.28 report projected final fuel costs in the $6.50 to $8.50 range using thermochemical conversion via hydrothermal liquefaction and biocrude refining via simulations on various estimated process parameters based on literature values and reasonable adjustments. Thus, this is why there appears to be so much excitement and promise felt toward the overall concept of producing biofuels from microalgae. It should be noted that the $4/gallon price represents the estimated processing cost for just the microalgae oil; however, most operations do plan to market their meal which should provide enough processing price offset to allow for the selling of the produced oil at a market price competitive with most seed oils. Hence, the proper marketing of the delipified meal components to provide an offset to oil production costs is a critical aspect of ensuring an economically viable microalgae to fuels production facility within today’s industrial environment.77 Or, utilize another form of whole algal cell processing to make fuels, such as thermochemical conversion, instead of a lipid-based system. However, nonlipid-based methods are far less mature than just-lipid processing methods. The drive to reach a per gallon lipid production cost less than $4 or $5/gallon has been a truly global effort supported by both government and private sector entities. Su et al.58 present an impressive list of microalgae lipid production R&D efforts since 2008 from numerous countries with the US and European investments alone totaling approximately 350 M US $ and 100 M EU$, respectively. Their paper concludes with the statement that more work needs to be done to yield a per gallon cost that is reasonable to support the algae to fuels market. However, as so often stated, they also conclude that the concept is very promising and worthy of these investments. The heart of any developmental effort to prove the moving of “the economic needle” of the microalgae to fuels process is the performance of consistent, holistic, and realistic TEAs using widely accepted rigorous TEA methods. Quinn and Davis57 support this statement as they found great reported pricing differences from cost assessments of producing biodiesels from algal lipids (almost all were simulated process costs from testbed and/or literature data). Quinn and Davis57 rightly suggest the need for the research community to use harmonized technology performance assessment methods.

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MARKET FEASIBILITY The two primary products appearing viable for most microalgae farm to product systems are lipids (oil) and postextraction algae cake (aka. PEARS: postextraction algae residuals). The oil is extracted using commercially available processing to produce a resulting microalgae meal cake. While there are several products that can be derived from microalgae oil, as previously outlined, the oil is planned for sale as a biodiesel feedstock. Note with a 20% lipid content in whole microalgal cells, which means that the resulting cake is 80% of total production weight. That is simply too much of a time and L


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the protein. This can be done by shifting the pH, but careful kinetic control (through pH, temperature, and time) must be employed to allow for denaturation of the protein but not allow for significant hydrolysis, because the molecular weight degradation will negatively impact the mechanical performance of the glue. These glues can be combined with a wide variety of agricultural waste products (e.g., sugar cane bagasse, corn husks, or rice husks) and/or waste forest products (e.g., chips, sawdust, paper, etc.) to create a variety of composite materials. These composites have been shown to have flexural strength and modulus comparable to conventional particleboards.47 Valuation of microalgal delipified algal cake could approach $1,000/ton based on calculations depending if a high quality glue can be developed and commercially matured. Animal Feed Supplements. The selling of the microalgae meal as an animal feed supplement is considered an excellent avenue for utilizing the value of the resulting meal from the process. Valuation in this field will generally track the open protein markets, which hovered in the $200−$300/ton range as listed above. The animal feed industry has a global sales volume of approximately 1 billion tons per year. Experts do expect the animal raising industry to experience significant growth (estimated as high as an 80% growth) over the next 20 years, thereby indicating a potential growth market for feed supplements. This is particularly promising in light of the continued growth of traditional feed grains, such as corn and soya, as biofuels feedstocks. The animal feed market is a growth industry that is currently searching for alternatives to traditional feed components making the use of algal cake a good potential market that will add increased profitability to the overall concept. A sector of the animal feed market that appears to be primed for using microalgae meal is the compound feed industry. This market manufactures animal feeds that are customized to provide a particular nutritional benefit based on the formulations produced via the addition of a certain combination of supplements. Given the protein, carbohydrate, and residual oil content of microalgae cake, this particular sector is one that should provide a good potential market. Potential markets for the meal, other than the feed market, that may be considered include the use of the meal in the production of commercial fish baits, production of polymers, and the production of alcohols via the fermentation of the carbohydrate fraction. Feed quality is the most critical external factor influencing animal health and viability. Most of the raw materials currently used for animal feed products are plant-based such as corn, soybeans, oats, and barley. With the increasing human population, it is critical to find feed sources that do not compete with human consumption. The need for alternative food sources has brought attention to many products including microalgae. Since algae is a biomass material that allows production with a daily harvest year around, this shows promise for animal feed supplementation or replacement. Algae proteins can be extracted or algae biomass can be used right after the oil extraction process,199 thereby bringing the feed market more sustainability. It is also feasible to use whole cells (nondelipified) as an animal supplement.200 In this case, the lipids are not utilized to make fuels but used in the animal feeds as a nutritional supplement. Depending on the species, algae can be composed of 6% to 71% protein content.201 Also, the nutritional composition of algae shows favorable characteristics for supplements in animal

delipified cake (essentially mainly protein) is not appropriately valuated, then lipid prices must carry the economic load which is the state of the industry today and why the state of the industry is generally labeled as not economically feasible. The current pricing of protein cakes that may compete with delipified microalgae cake is listed below (from an Internet survey of ag-market price Internet listings, 2016): Soy meal: ∼$300/ton Cottonseed meal: ∼$220/ton Sunflower meal: ∼$210/ton Canola meal: ∼$275/ton Linseed meal: ∼$220/ton Peanut meal: ∼$220/ton However, there are numerous technology options to convert algae cakes into coproducts with varying prices yielded depending on the types and amount of product(s) produced. The following sections of this paper will summarize some of the most promising options for delipified microalgae cakes. Production of Polymeric Products. One of several ways in which algae can be used to produce useful polymers is to harvest the polymeric substances that algae secrete through their cell membrane either naturally or after biological engineering. Extracellular polymeric substances, or EPSs, from microalgae typically include polysaccharides, proteins, and nucleic acids. There has been a wide variety of biomedical applications proposed for these substances including antiviral, antitumor, anti-inflammatory, anticoagulant, antioxidant, antibacterial, and antifungal applications in addition to acting as a thickening agent, drag reducing agent, and sorbent for wastewater treatment for more industrial applications.190 While the use of EPSs for wastewater treatment shows a lot of potential, the metal adsorption is closely associated with the EPS properties, metal species, solution chemistry, and operating conditions.191 As with most bioprocessing products, the isolation of these products is an important and active area of research.155,192 Pilot-scale studies have shown EPS can be isolated on a large scale using a coupled system of microfiltration and ultrafiltration.193 Algae can also be used to create some conventional monomers that are commonly used in the polymers industry. One such monomer is butanediol (BD). For instance, Saccharomyces cerevisiae has been engineered to produce (2R,3R)-butanediol, which can be used in synthetic rubbers.194,195 It has also been shown that algal biomass can be used to synthesize both 1,2-propanediol and 2,5furandicarboxylic acid (FDCA), and that algal oils can be converted to dicarboxylic acids.196 These algal-polymer/ polyester blends have been shown to have a wide range of biomedical applications.196 Algal oils have also been used to make bioepoxy resins.197 Acrylate monomers, including methyl methacrylate (MMA) and cyclohexyl methacrylate (CHMA), have been shown to accumulate within Chlorella kessleri, and if the production can be scaled up, these monomers would be useful for creating acrylic polymers through conventional syntheses.198 One simple way to convert algal biomass to useful products is to convert it into adhesives (glues). This is a common practice with other natural protein-rich sources such as soybean and casein. Assuming the biomass has a high protein content and that these macromolecules have not been significantly degraded in previous bioprocessing steps, these biomasses can be converted into glues through denaturation of M


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Industrial & Engineering Chemistry Research feeds202 including micronutrients like antioxidants, vitamins, minerals, essential fatty acids, and amino acids. Among the nutritional characteristics, algae also shows ease of digestibility203 which is another important aspect of animal feed development. As of 2007, it was estimated that over 30% of the current world algal production was sold for animal feed application.204 Microalgae have valuable application in aquaculture, livestock feed, and poultry feed because of the nutritional composition,202 which also has the potential can be extended to pets and farm animals. In fact, Alltech Inc. in Winchester, KY is growing microalgae (nonphotosynthetic) and using the harvested whole cells as a nutritional supplement to animal feeds. The use of algae in aquaculture is not surprising, since algae is a natural feed source for these animals. The most pronounced alteration in aquaculture feed is the decrease in the level of fishmeal and fish oil and the simultaneous increase of microalgae.199 The most frequently used species in aquaculture are Chlorella, Tetraselmis, Isochyrsis, and Pavlova.205 The species Hypnea cervicornis and Cryptonemia crenulata were tested for applicability as a source of protein in shrimp diets. It was concluded that it may be used as an acceptable 39% (w/w) component in shrimp feed.206 It was also suggested adding Spirulina platensis meal as an additive for shrimp larvae can improve growth and feed efficiency.207 The incorporation of microalgae in fish feed formulations has been shown to be sufficient, and even beneficial.208−210 It is also concluded that algae grown for aquaculture are more ecologically sustainable than traditional fish feeds.211 The less obvious applications of microalgae in animal feed extends to livestock. Spirulina is frequently used in feed supplements but can also be used as protein replacements. Studies replaced corn with a delipified microalgal meal which was a combination of algae biomass (deoiled) (57%) and soybean hulls. A 45% algae meal feed was digestible and supported the growth of steers.212 This also suggests that algae meal is a feasible feed for other ruminant animals. In fact, studies demonstrated that the supplementation of Spirulina can increase the live weight in Australian sheep.213 The primary applications of microalgae in animal feed were associated with nutrition, but other applications exist. Adding algae to hen feed can increase egg nutritional value, which could provide health benefits to humans.214 Currently, in pet food applications, the species Arthrospira is used in animal feeding for cats, dogs, and birds. This algae provides excellent nutritional supplements that have been found to yield positive impacts on the overall health physiology of these animals as provided via the natural vitamins, minerals, and essential fatty acids present in the algal biomass.215 Anaerobic Digestion of Microalgal Cake. Anaerobic digestion is a waste treatment process that converts organic waste into methane and carbon dioxide as the primary endproducts of the anaerobic biodegradation of the input waste.216 Biogas is the final gas produced which typically contains 50− 80% methane and 20−50% carbon dioxide with a few trace gases also present.217−219 Most often, anaerobic digestion is performed within digesters which are often sealed tanks that may or may not be mixed. Various configurations of a digester can be found in the literature. Additionally, sometimes anaerobic digestion is implemented within a sealed earthen or concrete lagoon.220,221 With anaerobic digestion, both waste reduction and the production of a value-added coproduct (biogas) are achieved. The biogas is essentially a replacement

for natural gas (∼1,000 BTUs/ft3), except the energetic value is based on biogas methane content. For example, a 70% methane biogas has an approximate energetic value of ∼700 BTUs/ft3 while a 50% methane biogas contains ∼500 BTUs/ ft3. Hence, for anaerobic digestion to represent a value-added coproduct for a microalgae farm operation, it must replace or displace the use of natural gas or generate on-site electrical power. Jankowska et al.222 published an extensive review of state of the art technology for digesting algal biomass into biogas. Generally, they view this option as a technically viable option. Yet, the economic benefits of potentially using algal cake for other coproducts is in question when compared to using it only as an input to a digester. Several studies investigated digestion of whole algal cells; in other words, none of the lipids were removed prior to feeding the digesters.22,219,223−225 These studies primarily used algae produced at wastewater treatment works or cultured macro or microalgae with the results generally indicating that digestion of these algal biomass sources may be economically feasible. However, a thorough study by Lundquist et al.116 showed that the digestion of whole cells for just biogas production is not economically feasible. Albeit on whole cells, Adams224 studied thermal pretreatment of whole algal cake (Nannochloropsis salina) with the hypothesis being that the thermal treatment would disrupt the algal cell walls (an often claimed ratelimiting step) and thus increase the rate and extent of biogas production. Yet, their results indicate no real benefit to the pretreatment step which is likely going to hold true for delipified cells. This contradicts the work of Schwede et al.226 who reported that thermal treatment was a better pretreatment technique over microwave irradiation or pressurization. The use of thermal pretreatment increased methane production by over 58% compared to the microalgal samples that were not pretreated. Sialve et al.227 offer an interesting integration of microalgae farming and the use of anaerobic digestion by passing the produced biogas through a microalgal bed for the removing of the carbon dioxide thereby increasing the energetic value of the biogas perhaps to even pipeline quality (>90% CH4). They also report that a high quality biogas can be produced from microalgal digestion (69−75%). Polakovicová, et al.228 studied the digestion of cell disrupted, green microalgae and the same microalgae species without cell disruption. They concluded that cell disruption more than doubles methane production. The maximum methane yield observed for the disrupted, delipified cells was 248 mL CH4/g cells reported as volatile suspended solids (VSSs). This is well within the range of methane yield (100−800 mL/g VSS) reported by Ward et al.219 after review of numerous studies on whole microalgae digestion. Zhao et al.229 evaluated the impact of lipid extraction fluid type on methane production from the subsequent digestion of delipified microalgal cells. They concluded that only chloroform showed significant inhibition (they reported on methanogens) compared to a wide variety of other common lipid extractants (hexane, ketones, methanol, dichloroethane, and ethanol). They also showed the value with reusing the digestate as a recovered source of nutrients for microalgae culturing. Finally, the authors reported that delipification appeared to increase the rate and extent of organic fraction (as VSS) conversion into biogas which is consistent with the results of others who studied lipid-bearing wastes (meat packing, food residuals, etc.) where lipids tend to be slower to degrade than proteins and carbohydrates. N


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Figure 2. Lipid production using an integrated, dual-bioreactor system.

2013, the market price of β-carotene was $300−$700/kg while that of astaxanthin was $2,000−$7,000/kg.235 Several studies evaluated various conditions that influence the enhancement of pigment content of microalgae. The main factors that affect pigment production in microalgae are nutrient availability, salinity, pH, temperature, light wavelength, and light intensity.237 The limitation of key nutrients such as nitrogen to induce lipid accumulation in algae also induces the enhancement of pigment content.238,239 Microalgal pigments, like other algal metabolites, require delicate downstream processing to achieve high recovery and to meet regulatory standards. Extraction and purification stages are significant fractions of the capital and production costs for microalgae pigments.235 The biomass processing for metabolite recovery is typically dehydration of biomass, cell disruption, solvent extraction, filtration, and chromatographic purification. The total cost for a chromatographic systems can be up to 50% of major equipment cost (MEC) followed by evaporators at 25% of MEC.240 The type of pigment recovered is dictated by the extraction system used.235 An important consideration after the extraction stage is the storage stability of pigments. Some microalgal pigments such as astaxanthin are very sensitive to storage conditions.241 Liquefaction/Thermal Depolymerization of Algae/Algae Cake. Microalgae are promising biofuel feedstocks due to their higher photosynthetic efficiency, faster growth rate, and higher area-specific yield as compared to terrestrial biomass.27,242 However, microalgae, along with any microbial feedstock, suffer from their very high water content which needs to be removed prior to conventional biofuel conversion technologies. For example, lipid-producing microalgae need to have low moisture content before solvent or mechanical extraction.42 Similarly, traditional methods for thermochemical biofuel conversion (i.e., gasification, pyrolysis) require dry feedstock for an energy efficient process.242 For feedstocks with high moisture contents, aqueous phase processes might be the more suitable option for their conversion into biofuels. One such process is hydrothermal liquefaction (HTL) wherein biomasses can be simultaneously dissolved and hydrolyzed in hot, compressed water.27,243 HTL, also called hydrous pyrolysis, converts biomass into an oily or tarry fluid through reactions with water at elevated temperatures and pressures. This process mainly utilizes water as a solvent, catalyst, and reactant by exploiting the increases in H+ and OH− concentrations from dissociation of water at these elevated conditions. These ions accelerate acid- and base-

The use of digestion appears to be viable and worthy of consideration for use of delipified microalgal cakes. A biogas of almost equal energetic content to natural gas can be produced and used to either dry the algal cells or produce on-site power. Producing power on-site is economically more attractive because the site operators would be replacing electric power at the ∼ $0.12/kW-hr versus natural gas at $2.90/thousand ft3 (aka. MMBTU). Plus, the nutrients could be reused thus further reducing operational costs. The digestion process can also be redirected to produce volatile organic acids (VOAs), such as acetic, propionic, butyric, and lactic acids, which are byproducts of incomplete digestion. The VOAs can later be biologically converted into more microbial lipids, via a subsequent aerobic treatment step, then sold as commodity chemicals, precursors to liquid fuel production (petroleum diesel replacement) through various options such as esterification or refining which yield a biobased diesel, or as a direct cofuel fed into a biogas driven genset (will add beneficial lubricity to the fuel mixture). The energetic aspect of producing VOAs from digestion for later lipid conversion is based on a novel dual-bioreactor system under development by our research team which takes the VOAs produced from the anaerobic digestion then transfers the partially treated influent into an aerobic bioreactor (activated sludge) where the VOAs are aerobically converted into lipids.230 The lipids extracted from the bacteria as described by Dufreche et al.231 can be used as a commercial feedstock for biodiesel and/or green diesel production.16,232,233 A summary diagram of the envisioned process capable of converting wastewater influents into microbially bound lipids using an anaerobic/aerobic, dual bioreactor system is presented as Figure 2. This lipid production scheme aligns well with the microalgal lipids being produced within the algae; hence, this strategy offers a two path sourcing of lipids. Recovery of Pigments from Microalgae. Pigments for food, feed, pharmaceuticals, and cosmetics are among the high-value coproducts from microalgae. Amid the economic advantages of synthetic pigments, the market for natural pigments (NPs) has been increasing due to concerns of the potential harmful effects of the former to human health.234 This demand for NPs offers a motivation for fuel-targeted microalgae commercialization to increase revenue by integrating the recovery and sale of high-value pigments.52,235,236 Several microalgae can accumulate pigments up to 13% w/w.237 Pigment production can occur at the same time as lipid production.238 The dominant NPs in microalgae are chlorophyll a, b, c, β-carotene, astaxanthin, xanthophylls, and phycobiliproteins.234,237 In O


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estimates is in the $140/ton range (assuming a $1.80/gallon ethanol price).

catalyzed hydrolysis and depolymerization of biomass.242,244,245 Among the species of microalgae that have been subjected to HTL are Botryococcus braunii, Dunaliella tertiolecta, Spirulina, Microcystis viridis, and Nannochloropsis sp.246−250 HTL is generally carried out at temperatures in the range of 523−623 K, pressures between 5 and 20 MPa, and reaction times between 5 and 60 min.246,251 Commonly, HTL of algal biomass results to about 10−73 wt % of bio-oil, 8−20 wt % gaseous mixture, and 0.2−0.5 wt % ash with bio oil yields up to 64 wt % and solids conversion up to 93%. The calorific value of the bio-oil is in the range of 30−50 MJ/kg while the gaseous mixture mainly contains CO2, H2, and CH4.246,251,252 Studies also indicated that a heterogeneous catalyst (e.g., Pd/C, Pt/C, Ru/C, Ni/SiO2-Al2O3, CoMo/γ-Al2O3, and zeolite) can be directly added during HTL of algae for in situ upgrading of products.242 In addition, studies conducted at NREL and PNNL indicated that HTL of microalgal biomass could be combined with catalytic hydrogasification (HTL wastewater to CH4 and CO2) and off-gas combustion for power and process heat integration.253 Valuation of PEARS or whole microalgal cake based on information presented in Petrick et al.254 and assuming a per gallon oil value of $4/gallon appears to hover around $400 to $500/ton. Ethanol Production from Microalgae. A viable alternative conversion path for microalgae to fuel is carbohydrates fermentation to ethanol.70,255 Microalgae-to-ethanol conversion is classified as a third-generation biomass process for fuels.256 A premise in the concept of ethanol from microalgae is the capability of microalgae species to accumulate high amounts of carbohydrates, preferably those that are easily assimilated into the cells, such as starch. Thus, researchers evaluated the effect of nutrient limitation such as nitrogen on the carbohydrate/lipid fractions of some microalgae species.257 This objective was motivated by the inquiry on the consequences of enhancing the lipid content via limitation of key nutrients (e.g., nitrogen). There is no common pattern across various microalgal species. That is, some species can accumulate high fractions of lipid and carbohydrates at the same time while other species accumulate high fractions of lipid at the expense of low fractions of carbohydrates.257,258 C. vulgaris can be cultivated to high fractions of carbohydrates (∼50% w/w) in addition to high fractions of lipids (∼40% w/ w).258 Microalgal carbohydrates are mainly cellulose in the cell wall and starch in the plastids.259 Even though microalgal species contain very low amounts of lignin,259 ethanol fermentation still requires steps similar to other biomass-to-ethanol biological conversions: (1) biomass disintegration, (2) polysaccharides hydrolysis, (3) fermentation, and (4) distillation.260 The main difference between lignocellulosic biomass and microalgae biomass disintegrations is that the latter generally results in higher monosaccharides yields after saccharification as compared to the former.259,260 The utilization of microalgae cake for ethanol fermentation after lipid extraction inherently implements a chemical pretreatment of the biomass aiding to liberate the carbohydrates into their monosaccharide constituents. In a comprehensive experimental and simulation studies on C. vulgaris by Moncada et al.,261 the economics of ethanol microalgae was shown favorable (0.55 g reducing sugars/g cake; 0.17 g ethanol/g cake). The possibility of direct ethanol production from CO2 by select microalgae species was also explored through genetic engineering.262,263 Thus, the valuation of cake

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SUMMARY AND CLOSING STATEMENTS The concept of cultivating microalgae to provide the feedstock into a viable biorefinery is clearly one of potential and within the realm of economic feasibility. Many reductions in the prices from lipids sourced from microalgae must occur through continued research and development. Much of the needed research and development likely should occur at the laboratory scale since the limitations are more in the nature of reactions, extraction, and cell development and not large-scale design innovation. This statement should be reviewed by government funding agencies which are more recently focused on demonstration scale efforts when so much development is still needed at the laboratory or pilot scales. More process integration into wastewater treatment plant operations and/or heterotrophic bacteria/yeast culturing in concert with microalgae could reduce lipid costs. Additionally, a dire need exists to develop higher paying markets for the delipified microalgal cakes which is critical to the overall economic feasibility of an algae to fuels industry. The promise is there, yet development must be well focused and directed at technology gaps and not overaccelerating into large demonstrations.

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AUTHOR INFORMATION

Corresponding Author

*Dr. Mark E. Zappi, PE. E-mail: [email protected]. ORCID

Mark E. Zappi: 0000-0002-7608-076X Daniel Gang: 0000-0002-2565-0830 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This paper represents years of experience performing research and project due-diligence studies within the challenging world of commercializing microalgae as a biorefinery feedstock. Numerous students and staff from our laboratories have greatly contributed to the knowledge collected and summarized in this paper. Funds from the NASA ESPCoR program and Louisiana Board of Regents via the Louisiana LaSPACE program supported this comprehensive review.

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