# Microalgae as a Renewable Source of Energy: A Niche Opportunity

Authors: Simon Jegan Porphy Jegathese; Mohammed Farid
Journal: Journal of Renewable Energy
 (2014)

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## Abstract

Algae are believed to be a good source of renewable energy because of its rapid growth rate and its ability to be cultivated in waste water or waste land. Several companies and government agencies are making efforts to reduce capital cost and operating costs and make algae fuel production commercially viable. Algae are the fastest growing plant and theoretically have the potential to produce more oil or biomass per acre when compared to other crops and plants. However, the energy efficiency ratio and carbon and water footprint for algal based biofuels still need to be evaluated in order to fully understand the environmental impact of algal derived biofuels.


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## Body

## 1. Introduction

Even though algae have been studied for ~70 years, it is especially important now due to global warming, fluctuation in oil prices, and energy dependence on foreign nations. The first interest occurred during World War II, when these organisms were investigated as a potential source of a number of products such as antibiotics and a good source of protein [1]. In the late 1940s and early 1950s, the Carnegie Institution of Washington sponsored construction of a pilot plant and supplemental laboratory studies. This work is summarized in a report which serves as a valuable source of information even today for algae cultivation [1]. Commercial systems designed to produce algae for human consumption were developed in Japan in the 1960s [2].The algal lipids would be an ideal feedstock for high energy density transportation fuels such as biodiesel, green jet fuel and green gasoline. Since it does not complete with food price, agricultural land and that it has the ability to sequester large quantities of carbon dioxide [3]. Biofuels are expected to be one of the major sources of renewable energy which mainly comprises of biodiesel, bioethanol, and biogas [4, 5].Years of study indicate that various human activities such as deforestation and burning of fossil fuels have led to increase in the concentration of carbon dioxide in the atmosphere causing global warming. The burning of fossil derived transportation fuels significantly contributed towards greenhouse effect. The most rapidly growing sector is the transportation sector. Recent report from Environmental Protection Agency indicates [6] that 28% of worldwide greenhouse gas emissions comes from the transportation sector alone. Hence, the transportation sector has become an important target for the reduction of greenhouse gases.


### 1.1. The Concept of Production Biofuels from Microalgae

The notion of producing biofuels from microalgae was proposed as early as 1950s in the United States by Meier et al. [7]. Algae are a single cell microorganism which is composed of lipids, carbohydrates, and proteins. The algae biomass has potential to produce a variety of biofuels as follows:(i)
lipids from the algae biomass could be extracted and refined to fatty acids; the fatty acids can be further processed to produce biodiesel by transesterification;
(ii)
gasification of the algal biomass by anaerobic digestion or thermal cracking can produce biogas;
(iii)
carbohydrate fraction can be used for bioethanol production by direct fermentation;
(iv)
pyrolysis or thermal degradation of biomass produces solid, liquid, and gaseous products;
(v)
anaerobic fermentation of biomass to produce methane gas;
(vi)
direct combustion of biomass to generate power or syngas.The technique of mass cultivation of algae is well known and the process of production of biodiesel is also well understood, but the bottle neck today is the cost of producing it at an economical scale. During the 1970 oil crisis the United States Department of Energy initiated a project called “Aquatic Species Program: Biodiesel from microalgae.” The Aquatic Species Program efforts were intended to look at the use of microalgae as sources of energy [8]. The Aquatic Species Program worked for two decades on developing biodiesel from microalgae and they screened up to 3000 strains of microalgae. After carrying out many years of research they finally screened down to 300 strains out of which the green algae and the diatoms are considered to be the most potent classes of microalgae for biofuel production [8].TAG (triglycerides) are the anticipated starting material for high energy density fuels such as biodiesel, green diesel, green jet fuel, and green gasoline [9–11] (produced by a combination of hydroprocessing and catalytic cracking to yield alkanes of predetermined chain lengths). To produce algal biomass with high lipid content the algae needs to be cultivated under nutrient limited conditions (especially nitrogen, phosphorous, or silicon). Lipid content varies in both quantity and quality with varied growth conditions. While high lipid content can be obtained under nutrient limitation, this is generally at the expense of reduced biomass productivities [8].Currently, onlySpirulina andDunaliella (extremophiles) are capable of growing in mass scale in outdoor race way ponds because they can survive in high alkaline environment; this makes it easier for them to cultivate. Mass cultivation of algae on open ponds has not been scaled up beyond 25 acres [12, 13]. Another method of cultivation of microalgae is via closed photobioreactors. However, since the operation and maintenance cost is too high for closed photobioreactors, they are used primarily for high value products. Therefore, until large-scale systems are built and operated over a number of years, many uncertainties will still remain. Cultivation issues are there for both open and closed systems, such as reactor construction materials, mixing, optimal cultivation scale, heating/cooling, evaporation, O2 buildup, and CO2 administration, and have been considered and explored to some degree, but more definitive answers await detailed and expensive scaleup and energy evaluations [14–16].


## 1.1. The Concept of Production Biofuels from Microalgae

The notion of producing biofuels from microalgae was proposed as early as 1950s in the United States by Meier et al. [7]. Algae are a single cell microorganism which is composed of lipids, carbohydrates, and proteins. The algae biomass has potential to produce a variety of biofuels as follows:(i)
lipids from the algae biomass could be extracted and refined to fatty acids; the fatty acids can be further processed to produce biodiesel by transesterification;
(ii)
gasification of the algal biomass by anaerobic digestion or thermal cracking can produce biogas;
(iii)
carbohydrate fraction can be used for bioethanol production by direct fermentation;
(iv)
pyrolysis or thermal degradation of biomass produces solid, liquid, and gaseous products;
(v)
anaerobic fermentation of biomass to produce methane gas;
(vi)
direct combustion of biomass to generate power or syngas.The technique of mass cultivation of algae is well known and the process of production of biodiesel is also well understood, but the bottle neck today is the cost of producing it at an economical scale. During the 1970 oil crisis the United States Department of Energy initiated a project called “Aquatic Species Program: Biodiesel from microalgae.” The Aquatic Species Program efforts were intended to look at the use of microalgae as sources of energy [8]. The Aquatic Species Program worked for two decades on developing biodiesel from microalgae and they screened up to 3000 strains of microalgae. After carrying out many years of research they finally screened down to 300 strains out of which the green algae and the diatoms are considered to be the most potent classes of microalgae for biofuel production [8].TAG (triglycerides) are the anticipated starting material for high energy density fuels such as biodiesel, green diesel, green jet fuel, and green gasoline [9–11] (produced by a combination of hydroprocessing and catalytic cracking to yield alkanes of predetermined chain lengths). To produce algal biomass with high lipid content the algae needs to be cultivated under nutrient limited conditions (especially nitrogen, phosphorous, or silicon). Lipid content varies in both quantity and quality with varied growth conditions. While high lipid content can be obtained under nutrient limitation, this is generally at the expense of reduced biomass productivities [8].Currently, onlySpirulina andDunaliella (extremophiles) are capable of growing in mass scale in outdoor race way ponds because they can survive in high alkaline environment; this makes it easier for them to cultivate. Mass cultivation of algae on open ponds has not been scaled up beyond 25 acres [12, 13]. Another method of cultivation of microalgae is via closed photobioreactors. However, since the operation and maintenance cost is too high for closed photobioreactors, they are used primarily for high value products. Therefore, until large-scale systems are built and operated over a number of years, many uncertainties will still remain. Cultivation issues are there for both open and closed systems, such as reactor construction materials, mixing, optimal cultivation scale, heating/cooling, evaporation, O2 buildup, and CO2 administration, and have been considered and explored to some degree, but more definitive answers await detailed and expensive scaleup and energy evaluations [14–16].


## 2. Bioethanol Production from Microalgae

Significant attention has been diverted to biodiesel production from microalgae since certain strains are capable of accumulating large quantities of lipid naturally inside their cells, through nitrogen-deficient cultivation. The lipid content inside the microalgae cells is boosted up significantly by blocking carbohydrate synthesis pathway.Biodiesel has a higher calorific value than bioethanol, 37.3 MJ/kg and 26.7 MJ/kg, respectively [17]. Nonetheless, microalgae are found to be a superior feedstock to produce bioethanol in comparison with other first and second generation bioethanol feedstock [17, 18]. First generation bioethanol is derived from food feedstock such as sugar cane and sugar beet. Over exploitation of this feedstock creates the “food versus fuel” issues and raised several ethical and environmental issues including deforestation and ineffective land utilization.Second generation bioethanol is produced from lignocellulosic biomass such as wood, rice straw, and corn stover. Initially, this lignocellulosic biomass must be subjected to pretreatment to break down the complex structure of lignin and to decrease the fraction of crystalline cellulose by converting to amorphous cellulose [19]. However, most of the pretreatment methods such as steam explosion and alkali or acid pretreatment are energy intensive and bring negative impact towards the energy balance [20]. In contrast, microalgae cells are buoyant and therefore do not require lignin and hemicelluloses for structural support [21]. Hence, it is expected that the overall bioethanol production process can be simplified due to the nonrequirement of chemical and enzymatic pretreatment step. Nevertheless, it should be noted that high concentrations of carbohydrates are actually entrapped within the microalgae cell wall. An economical physical pretreatment process such as extrusion and mechanical shear is still required to break down the cell wall so that the carbohydrates can be released and converted to fermentable sugars for bioethanol production [22].On the other hand, simultaneous biodiesel and bioethanol production from microalgae is also possible, in which microalgae lipid is extracted prior to fermentation process. This concept has been proven viable in a study by Harun et al. [22] in which lipid fromChlorococum sp. was extracted with supercritical CO2 at 60°C and subsequently subjected to fermentation by the yeastSaccharomyces bayanus. Microalgae biomass with preextracted lipid gave 60% higher ethanol concentration compared to the dried microalgae biomass without lipid extraction [23].In other words, both lipid extraction from microalgae biomass for biodiesel production and pretreatment step to release carbohydrates for bioethanol production can occur in just one single step. It could greatly enhance the viability of microalgae biofuels production in commercial scale. The bioethanol yields obtained are comparable to the yields from sugary and lignocellulosic feedstock, indicating that microalgae biomass is a feasible alternative substrate for commercial scale bioethanol production [23].


### 2.1. Methane Production from Microalgae

Relatively few studies have been published on the anaerobic digestion of microalgae. The earliest work compared digestion of domestic wastewater sludge and green microalgal biomass,ScenedesmusandChlorella, harvested from wastewater ponds. They found that these algae could yield as much as 0.25–0.50 L CH4/g input at an 11-day retention time (hydraulic) when incubated at 35–50°C [24] (methane yield is typically expressed as liters of methane produced per gram of volatile solids introduced into a digester). It is suggested that the relatively low digestibility was the result of cell walls resisting bacterial degradation, but the cell wall is readily digested by bacteria at higher temperature [25]. Inhibitory ammonia concentrations might also be a cause of low methane yields from algae digestion [26]. Algae biomass typically has a high protein content (40–50%; C : N ratio 6 : 1), which contributes to high total ammonia concentrations in the sludge. Codigestion with high-carbon, low-nitrogen substrates has potential for diminishing any ammonia toxicity and also increasing the biogas production per unit volume of digester tank [26].Methane yield and productivity were doubled when equal masses of wastewater sludge andSpirulina biomass were co-digested with waste paper (50% w/w) to adjust the C : N ratio to around 20–25 : 1 which, in turn, doubled the methane production rate from 0.6 L/L day to 1.2 L/L day at 35°C and with a retention time (hydraulic) of 10 days [26–28].


### 2.2. Biocrude Oil Production from Microalgae

Since microalgae slurry contains high water content after harvesting, therefore, extensive drying is essential before the biomass is subjected to extraction and transesterification. Drying of wet microalgae biomass consumed exceptional large amount of energy, that is, typically in temperate countries where sunlight is not available throughout the year. Furthermore, the energy for drying biomass is usually generated from nonrenewable sources (e.g., natural gas and coal), which could lead to high carbon footprint [29].In this regard, hydrothermal liquefaction could be an alternative way to produce bio-oil from microalgae through aqueous-conversion method, in which freshly harvested wet microalgae biomass are directly processed without drying. Microalgae are expected to be an excellent biomass feedstock for this technology because their small size cell will enhance rapid heat transfer to the required processing temperature [30].During hydrothermal liquefaction, water is heated to subcritical condition (200°C to 350°C) under pressurized condition in order to reduce its dielectric constant. Water at subcritical condition can serve as an effective solvent and significantly less corrosive than other solvents [31, 32]. Recently, several studies have investigated the potential of using hydrothermal liquefaction technology to convert wet microalgae biomass to biocrude oil and biochar [31, 33]. It was estimated that 43 wt.% of biocrude oil was successfully recovered fromNannochloropsis sp. (initial water content of 79 wt.%) through hydrothermal liquefaction at 350°C for 60 min and the biocrude oil obtained has a heating value of 39 MJ/kg [34]. However, the recovered bio-oil has a relatively higher composition of nitrogen and oxygen compare to petroleum crude oil. Hence, the bio-oil requires de-oxygenation and de-nitrogenation to upgrade it. More importantly, the process gave a positive energy of 45.3 KJ (assuming water enthalpies at 25°C and 350°C are 82 and 1672 KJ/kg, respectively, and the reactor is well insulated without any heat lost) indicating that hydrothermal liquefaction is a viable technology to convert wet microalgae biomass to bio-oil without requiring any drying process [32]. However, there are several issues that need to be addressed in hydrothermal liquefaction such as (1) chemical solvent such as dichloromethane (DCM) is required to extract bio-oil from thermal treated biochar which significantly reduces the process viability in industrial scale and (2) the aqueous phase may contain high concentration of organic matter that requires treatment before it can be discharged into water sources.


## 2.1. Methane Production from Microalgae

Relatively few studies have been published on the anaerobic digestion of microalgae. The earliest work compared digestion of domestic wastewater sludge and green microalgal biomass,ScenedesmusandChlorella, harvested from wastewater ponds. They found that these algae could yield as much as 0.25–0.50 L CH4/g input at an 11-day retention time (hydraulic) when incubated at 35–50°C [24] (methane yield is typically expressed as liters of methane produced per gram of volatile solids introduced into a digester). It is suggested that the relatively low digestibility was the result of cell walls resisting bacterial degradation, but the cell wall is readily digested by bacteria at higher temperature [25]. Inhibitory ammonia concentrations might also be a cause of low methane yields from algae digestion [26]. Algae biomass typically has a high protein content (40–50%; C : N ratio 6 : 1), which contributes to high total ammonia concentrations in the sludge. Codigestion with high-carbon, low-nitrogen substrates has potential for diminishing any ammonia toxicity and also increasing the biogas production per unit volume of digester tank [26].Methane yield and productivity were doubled when equal masses of wastewater sludge andSpirulina biomass were co-digested with waste paper (50% w/w) to adjust the C : N ratio to around 20–25 : 1 which, in turn, doubled the methane production rate from 0.6 L/L day to 1.2 L/L day at 35°C and with a retention time (hydraulic) of 10 days [26–28].


## 2.2. Biocrude Oil Production from Microalgae

Since microalgae slurry contains high water content after harvesting, therefore, extensive drying is essential before the biomass is subjected to extraction and transesterification. Drying of wet microalgae biomass consumed exceptional large amount of energy, that is, typically in temperate countries where sunlight is not available throughout the year. Furthermore, the energy for drying biomass is usually generated from nonrenewable sources (e.g., natural gas and coal), which could lead to high carbon footprint [29].In this regard, hydrothermal liquefaction could be an alternative way to produce bio-oil from microalgae through aqueous-conversion method, in which freshly harvested wet microalgae biomass are directly processed without drying. Microalgae are expected to be an excellent biomass feedstock for this technology because their small size cell will enhance rapid heat transfer to the required processing temperature [30].During hydrothermal liquefaction, water is heated to subcritical condition (200°C to 350°C) under pressurized condition in order to reduce its dielectric constant. Water at subcritical condition can serve as an effective solvent and significantly less corrosive than other solvents [31, 32]. Recently, several studies have investigated the potential of using hydrothermal liquefaction technology to convert wet microalgae biomass to biocrude oil and biochar [31, 33]. It was estimated that 43 wt.% of biocrude oil was successfully recovered fromNannochloropsis sp. (initial water content of 79 wt.%) through hydrothermal liquefaction at 350°C for 60 min and the biocrude oil obtained has a heating value of 39 MJ/kg [34]. However, the recovered bio-oil has a relatively higher composition of nitrogen and oxygen compare to petroleum crude oil. Hence, the bio-oil requires de-oxygenation and de-nitrogenation to upgrade it. More importantly, the process gave a positive energy of 45.3 KJ (assuming water enthalpies at 25°C and 350°C are 82 and 1672 KJ/kg, respectively, and the reactor is well insulated without any heat lost) indicating that hydrothermal liquefaction is a viable technology to convert wet microalgae biomass to bio-oil without requiring any drying process [32]. However, there are several issues that need to be addressed in hydrothermal liquefaction such as (1) chemical solvent such as dichloromethane (DCM) is required to extract bio-oil from thermal treated biochar which significantly reduces the process viability in industrial scale and (2) the aqueous phase may contain high concentration of organic matter that requires treatment before it can be discharged into water sources.


## 3. Challenges and Promises of Producing Biofuel from Microalgal Biomass

Annually 10,000 tonnes of algal biomass are currently being produced. Species likeChlorella,Spirulina,Haematococcus, andDunaliella are cultivated in open ponds or photobioreactors for high value products such as animal feed, antioxidants, and pigments [17]. It is known theoretically that algae have the potential of producing 6000 gallons of biofuel per hectare which is remarkable when compared to traditional crops such as soybean, rapeseeds, and coconut due to higher growth rates and less usage of land [17].However, to successfully cultivate microalgal biomass on a large scale we need to consider the following parameters:(i)
land (availability, suitability, and cost);
(ii)
type of microalgae (strain, cell size, lipid and carbohydrate content, harvesting, and processing);
(iii)
value of the algal product;
(iv)
cost of raw materials to generate high volume biomass;
(v)
amount of water needed for cultivation;
(vi)
climatic conditions;
(vii)
life cycle assessment (LCA) studies.Until today, there is no commercial plant producing and processing microalgae biomass into biofuels. This has led to the lack of understanding in the overall process and operation. Currently LCA is widely accepted as an effective tool to guide and give a clear idea to researchers and policy makers on revealing the real potential of a particular product that is being evaluated. It can also be used to indicate if production of a particular product can lead to negative environmental phenomena such as eutrophication, global warming, ozone depletion, human and marine toxicity, poor carbon footprint, land competition, and photochemical oxidation. Hence, LCA studies can be used to take precautionary steps to reduce these negative impacts on environment. In addition, energy balance can be calculated to determine and justify the energy hotspot (process involving significant amount of energy) of all stages within the system boundary of the LCA.There are only a few LCA studies performed on microalgae biofuels due to limited comprehensive data. Therefore, parameters related to microalgae biofuel production such as biomass productivity, lipid content, and downstream energy efficiency (harvesting, drying, and transesterification) are obtained based purely on lab scale experimental data. The data used in those assessments might be irrelevant when applied to large-scale production. However, LCA studies could have a predictive power. Most of the studies have concluded that producing biofuels especially biodiesel or biocrude oil from microalgae is an extremely energy intensive process [47]. The Energy Efficiency Ratio (EER), defined as the ratio of energy output to energy input, is generally used to indicate the sustainability energy index to produce a particular product in which a ratio higher than 1 designates to net positive energy generated and vice versa. All the EER values for biodiesel derived from oil bearing crops are more than 1 as shown in Table 1.Table 1
Energy Efficiency Ratio for biofuels produced from different feedstock.
Feedstock
Technology
Energy efficiency ratio (EER)
Reference
Jatropha
Biodiesel production by transesterification coupled with biogas production
3.34
[35]
Palm oil
Biodiesel production by transesterification coupled with biogas production
3.58
[36]
Marine Microalgae (Nannocholopris species)
Biodiesel production by transesterification coupled with biogas production. Cultivated through photobioreactor.
0.07
[37]
Fresh water microalgae (Chlorella Vulgaris)
Cultivating biomass through photobioreactor
0.35
[38]
Fresh water microalgae (Chlorella Vulgaris)
Cultivating biomass through raceway ponds
1.46
[38]The quantitative results shown in Table1 indicate that microalgae based biofuels do not necessarily propel a positive output but could pose a critical risk for unsustainable biofuels production. From the microalgae LCA studies, four of the key energy intensive hotspots were identified: (1) nutrients source [47], (2) microalgae cultivation technology [37, 38], (3) dewatering and biomass drying [48], and (4) lipid extraction [48, 49].


## 4. Key Energy Intensive Process in Microalgae Based Fuel Production

### 4.1. Nutrient Source for Cultivating Microalgae Biomass

In general algae require nitrogen (nitrate), phosphorus (orthophosphate), trace metals, and a sole source of carbon (carbon dioxide). These nutrients are normally from inorganic fertilizers that are used to achieve an acceptable growth rate and productivity of algal biomass. The use of chemical fertilizer has the advantage of reducing contamination in culturing medium. Hence, the water can be reutilized to reculture.A recent LCA study has pointed out that 50% of the overall energy used and GHG emission were associated with utilization of these inorganic fertilizers [50]. Inorganic fertilizer production has been categorized as an energy intensive industry, in which 37 to 40 GJ of low heating value (LHV) natural gas will be consumed to produce 1 tonne of ammonia (inorganic nitrogen sources, N-fertilizer). Furthermore, 1.2 kg of carbon dioxide (CO2) will be emitted for every 1 kg of ammonia produced [47, 51]. Thus, in the long run, using inorganic fertilizers to culture microalgae for biofuel production is definitely not sustainable. Apart from that, culturing of microalgae is found to consume more inorganic fertilizers than other oil bearing crops [50, 52]. Oil palm plantation required the least fertilization, around 83–87% lower than microalgae cultivation, whereas sunflower, rapeseed, and jatropha are 59–68%, 52–62%, and 17–35% lower, respectively [36, 53].In addition, it should be noted that the N-fertilizer consumption by microalgae was calculated based on optimist condition, in which high lipid content of 50 wt% was assumed. If the lipid content is assumed as 22% [54, 55], N-fertilizer consumption will increase to 0.67 kg/kg oil, an increment of 131% from the optimist scenario. Hence, recycling and reusing the excess nutrients in the culture medium should be encouraged to improve the life cycle energy balance of microalgae biofuels. Perhaps, the main concern of this approach is the ability of microalgae to reuse the nutrients and grow in an environment which is free contamination. Due to the severe impact of inorganic fertilizers towards the overall energy balance in microalgae cultivation [47], there is an urgent need to search for alternative and low cost nutrient sources to ensure long-term sustainability.In this case, using wastewater to culture microalgae appears to be an attractive and economical alternative. Normally, secondary and tertiary wastewaters contain significant amount of nitrate and orthophosphate which are not removed during primary treatment. If these nutrients are to be removed, an additional 60% to 80% of energy will be consumed in the wastewater treatment plant [56]. Instead, these nutrients can be used to culture microalgae and at the same time microalgae will play an important role as a reagent to purify the wastewater. Hence, culturing of microalgae in wastewater does not only offer an inexpensive alternative to conventional method of wastewater treatment but it can also substantially reduce the need of chemical fertilizers and their associated life cycle burden.


### 4.2. Microalgae Cultivation Technology

Biomass growth rates determined in laboratory studies are often expressed on per unit volume basis. However, the more appropriate reporting metric is growth per unit area, where area is that exposed to light. Therefore, in order to translate volumetric growth rates (typically from under artificial light conditions) into meaningful, real growth rates (typically under natural light), this requires knowledge of the area exposed to light and the hours per day that light was applied. There is a multitude of additional problems associated with making such translations. Most of the studies upon which volumetric growth rates are based are conducted indoors or at bench-scale and under tightly controlled steady-state conditions, none of which are likely to be applicable to mass production systems.An effective culture system should consist of the following criteria: (1) effective illumination area, (2) optimal gas-liquid transfer, (3) easy to operate, (4) low contamination level, (5) low capital and production cost, and (6) minimal land area requirement. The main advantage of growing microalgae in a closed photobioreactor is that it permits single strain culture in which optimum growth condition is always maintained to give high consistency in biomass and lipid productivity. Thus, closed photobioreactor has always attracted great interest from researches to further improve the operating conditions for implementation in commercial scale.LCA studies done on the energy needed for mass cultivation of microalgae on raceway ponds and photobioreactors indicated a rather unexpected result; raceway ponds emerged as a more sustainable and economic way to culture microalgae even though optimum culture conditions (microalgae with high lipid productivity) are achieved in air-lift tubular photobioreactor. The average energy input to operate air-lift photobioreactor is around 350% higher compared to raceway pond [37, 38]. Despite the advantages of lower level of contamination and optimal use of cultivation area, since CO2 is soluble in water relative to oxygen, the air-lift tubular photo-bioreactor consumed significant amount of power in order to obtain optimum mixing and gas-liquid mass transfer so that required mixing and optimum gas-liquid transfer rate are achieved. Based on currently available technology, air-lift photobioreactor is not up to commercialization stage unless proper modifications are performed to reduce the overall operating energy consumption. One of the plausible improvements that can be done is by designing an oscillatory flow reactor rather than a tubular type [37]. Oscillatory flow reactor consists of equally spaced orifice plate baffles in which the baffles behave like stirred tanks that can give excellent mixing effect by creating vortices between orifice baffles and superimposed oscillating fluid; then, energy consumption can be reduced because only minimal culture velocity is required to achieve intense mixing effect [57]. In addition, mass transfer of CO2 to culture medium can be further improved and enhances CO2 utilization by microalgae.


### 4.3. Dewatering and Drying of the Microalgae Biomass

Microalgae harvesting process posed a challenging task to engineer since microalgae are small size microorganism (generally, 1–20μm) and suspended in water. Currently, there are several methods to harvest microalgae: (1) bulk harvesting—to separate microalgae from suspension, such as natural gravity sedimentation, flocculation, and floatation and (2) thickening—to concentrate the microalgae slurry after bulk harvesting, such as centrifugation and filtration.Recent LCA studies [15, 48] revealed that microalgae grown in raceway ponds using wastewaters were harvested by two types of solid concentration methods, filter press and centrifugation. The filter press method contributed 88.6% (equivalent to 122 GJ/tonne biodiesel), whereas centrifugation contributed 92.7% (equivalent to 239 GJ/tonne biodiesel), respectively, to the entire LCA. Since the algae were grown in wastewaters (assuming ample nutrients were available), cultivation of algae contributed ~1% of the total LCA. The energy consumed in harvesting and drying of microalgae biomass should not be ignored as it may bring significant adverse effect towards the overall energy balance in producing microalgae biofuels [29]. Up to now, centrifugation and filtration are still not energy feasible methods to harvest microalgae in commercial scale [15, 48].In comparison to terrestrial crops microalgae biomass contain up to 80% moisture content. Hence, substantial amount of energy is required to dry algal biomass that is 11.22 MJ/Kg [29]. It is imperative to remove the moisture content from the biomass as it will interfere with downstream processing such as lipid extraction, transesterification, and pyrolysis. Solar drying is one of the best methods to dry the biomass. Nevertheless, solar drying methods can be employed only to temperate countries due to limited sunlight at certain time of the year. Otherwise, heat generated from fossil fuels is required to dry microalgae biomass continuously to ensure optimum biomass production for each cycle of culture. However, a LCA study by Sander and Murthy [48] has highlighted that using natural gas as a source fuel for drying microalgae biomass consumed nearly 69% of the overall energy input and led to a negative energy balance in producing microalgae biofuels. Thus, new technologies or approaches (e.g., development of efficient dryers) are urgently needed to ensure the sustainability of microalgae biofuels industry.


### 4.4. Lipid Extraction

The energy consumed in lipid extraction from dried microalgae biomass contributed only to small portion of the overall energy life cycle of microalgae biofuels (around 5–10%) [38, 48]. Effective lipid extraction is required particularly for microalgae with low lipid content as losing the lipid during extraction process may bring a significant impact towards the production cost of microalgae biofuels [58].Different from terrestrial energy crops, lipid extraction from microalgae biomass is relatively difficult due to the presence of thick cell wall that prevents the release of intracellular lipid. Hence, mechanical press which is effective to extract oil from terrestrial energy crops is generally not applicable to microalgae biomass. As discussed earlier in Section4.3 drying requires extensive energy. Therefore, it is important to develop wet biomass lipid extraction technologies such as supercritical CO2 technology.In fact, supercritical CO2 offers several advantages in comparison with chemical solvent extraction: (1) nontoxic and provides nonoxidizing environment to avoid degradation of extracts, (2) low critical temperature (around 31°C) which prevents thermal degradation of products, (3) high diffusivity and low surface tension which allow penetration in pores smaller than those accessible by chemical solvents, and (4) easy separation of CO2 at ambient temperature after extraction [39, 59, 60]. However, the main disadvantages of supercritical CO2 are the high cost of operation, skilled labour, high capital investment, and safety related issues.


## 4.1. Nutrient Source for Cultivating Microalgae Biomass

In general algae require nitrogen (nitrate), phosphorus (orthophosphate), trace metals, and a sole source of carbon (carbon dioxide). These nutrients are normally from inorganic fertilizers that are used to achieve an acceptable growth rate and productivity of algal biomass. The use of chemical fertilizer has the advantage of reducing contamination in culturing medium. Hence, the water can be reutilized to reculture.A recent LCA study has pointed out that 50% of the overall energy used and GHG emission were associated with utilization of these inorganic fertilizers [50]. Inorganic fertilizer production has been categorized as an energy intensive industry, in which 37 to 40 GJ of low heating value (LHV) natural gas will be consumed to produce 1 tonne of ammonia (inorganic nitrogen sources, N-fertilizer). Furthermore, 1.2 kg of carbon dioxide (CO2) will be emitted for every 1 kg of ammonia produced [47, 51]. Thus, in the long run, using inorganic fertilizers to culture microalgae for biofuel production is definitely not sustainable. Apart from that, culturing of microalgae is found to consume more inorganic fertilizers than other oil bearing crops [50, 52]. Oil palm plantation required the least fertilization, around 83–87% lower than microalgae cultivation, whereas sunflower, rapeseed, and jatropha are 59–68%, 52–62%, and 17–35% lower, respectively [36, 53].In addition, it should be noted that the N-fertilizer consumption by microalgae was calculated based on optimist condition, in which high lipid content of 50 wt% was assumed. If the lipid content is assumed as 22% [54, 55], N-fertilizer consumption will increase to 0.67 kg/kg oil, an increment of 131% from the optimist scenario. Hence, recycling and reusing the excess nutrients in the culture medium should be encouraged to improve the life cycle energy balance of microalgae biofuels. Perhaps, the main concern of this approach is the ability of microalgae to reuse the nutrients and grow in an environment which is free contamination. Due to the severe impact of inorganic fertilizers towards the overall energy balance in microalgae cultivation [47], there is an urgent need to search for alternative and low cost nutrient sources to ensure long-term sustainability.In this case, using wastewater to culture microalgae appears to be an attractive and economical alternative. Normally, secondary and tertiary wastewaters contain significant amount of nitrate and orthophosphate which are not removed during primary treatment. If these nutrients are to be removed, an additional 60% to 80% of energy will be consumed in the wastewater treatment plant [56]. Instead, these nutrients can be used to culture microalgae and at the same time microalgae will play an important role as a reagent to purify the wastewater. Hence, culturing of microalgae in wastewater does not only offer an inexpensive alternative to conventional method of wastewater treatment but it can also substantially reduce the need of chemical fertilizers and their associated life cycle burden.


## 4.2. Microalgae Cultivation Technology

Biomass growth rates determined in laboratory studies are often expressed on per unit volume basis. However, the more appropriate reporting metric is growth per unit area, where area is that exposed to light. Therefore, in order to translate volumetric growth rates (typically from under artificial light conditions) into meaningful, real growth rates (typically under natural light), this requires knowledge of the area exposed to light and the hours per day that light was applied. There is a multitude of additional problems associated with making such translations. Most of the studies upon which volumetric growth rates are based are conducted indoors or at bench-scale and under tightly controlled steady-state conditions, none of which are likely to be applicable to mass production systems.An effective culture system should consist of the following criteria: (1) effective illumination area, (2) optimal gas-liquid transfer, (3) easy to operate, (4) low contamination level, (5) low capital and production cost, and (6) minimal land area requirement. The main advantage of growing microalgae in a closed photobioreactor is that it permits single strain culture in which optimum growth condition is always maintained to give high consistency in biomass and lipid productivity. Thus, closed photobioreactor has always attracted great interest from researches to further improve the operating conditions for implementation in commercial scale.LCA studies done on the energy needed for mass cultivation of microalgae on raceway ponds and photobioreactors indicated a rather unexpected result; raceway ponds emerged as a more sustainable and economic way to culture microalgae even though optimum culture conditions (microalgae with high lipid productivity) are achieved in air-lift tubular photobioreactor. The average energy input to operate air-lift photobioreactor is around 350% higher compared to raceway pond [37, 38]. Despite the advantages of lower level of contamination and optimal use of cultivation area, since CO2 is soluble in water relative to oxygen, the air-lift tubular photo-bioreactor consumed significant amount of power in order to obtain optimum mixing and gas-liquid mass transfer so that required mixing and optimum gas-liquid transfer rate are achieved. Based on currently available technology, air-lift photobioreactor is not up to commercialization stage unless proper modifications are performed to reduce the overall operating energy consumption. One of the plausible improvements that can be done is by designing an oscillatory flow reactor rather than a tubular type [37]. Oscillatory flow reactor consists of equally spaced orifice plate baffles in which the baffles behave like stirred tanks that can give excellent mixing effect by creating vortices between orifice baffles and superimposed oscillating fluid; then, energy consumption can be reduced because only minimal culture velocity is required to achieve intense mixing effect [57]. In addition, mass transfer of CO2 to culture medium can be further improved and enhances CO2 utilization by microalgae.


## 4.3. Dewatering and Drying of the Microalgae Biomass

Microalgae harvesting process posed a challenging task to engineer since microalgae are small size microorganism (generally, 1–20μm) and suspended in water. Currently, there are several methods to harvest microalgae: (1) bulk harvesting—to separate microalgae from suspension, such as natural gravity sedimentation, flocculation, and floatation and (2) thickening—to concentrate the microalgae slurry after bulk harvesting, such as centrifugation and filtration.Recent LCA studies [15, 48] revealed that microalgae grown in raceway ponds using wastewaters were harvested by two types of solid concentration methods, filter press and centrifugation. The filter press method contributed 88.6% (equivalent to 122 GJ/tonne biodiesel), whereas centrifugation contributed 92.7% (equivalent to 239 GJ/tonne biodiesel), respectively, to the entire LCA. Since the algae were grown in wastewaters (assuming ample nutrients were available), cultivation of algae contributed ~1% of the total LCA. The energy consumed in harvesting and drying of microalgae biomass should not be ignored as it may bring significant adverse effect towards the overall energy balance in producing microalgae biofuels [29]. Up to now, centrifugation and filtration are still not energy feasible methods to harvest microalgae in commercial scale [15, 48].In comparison to terrestrial crops microalgae biomass contain up to 80% moisture content. Hence, substantial amount of energy is required to dry algal biomass that is 11.22 MJ/Kg [29]. It is imperative to remove the moisture content from the biomass as it will interfere with downstream processing such as lipid extraction, transesterification, and pyrolysis. Solar drying is one of the best methods to dry the biomass. Nevertheless, solar drying methods can be employed only to temperate countries due to limited sunlight at certain time of the year. Otherwise, heat generated from fossil fuels is required to dry microalgae biomass continuously to ensure optimum biomass production for each cycle of culture. However, a LCA study by Sander and Murthy [48] has highlighted that using natural gas as a source fuel for drying microalgae biomass consumed nearly 69% of the overall energy input and led to a negative energy balance in producing microalgae biofuels. Thus, new technologies or approaches (e.g., development of efficient dryers) are urgently needed to ensure the sustainability of microalgae biofuels industry.


## 4.4. Lipid Extraction

The energy consumed in lipid extraction from dried microalgae biomass contributed only to small portion of the overall energy life cycle of microalgae biofuels (around 5–10%) [38, 48]. Effective lipid extraction is required particularly for microalgae with low lipid content as losing the lipid during extraction process may bring a significant impact towards the production cost of microalgae biofuels [58].Different from terrestrial energy crops, lipid extraction from microalgae biomass is relatively difficult due to the presence of thick cell wall that prevents the release of intracellular lipid. Hence, mechanical press which is effective to extract oil from terrestrial energy crops is generally not applicable to microalgae biomass. As discussed earlier in Section4.3 drying requires extensive energy. Therefore, it is important to develop wet biomass lipid extraction technologies such as supercritical CO2 technology.In fact, supercritical CO2 offers several advantages in comparison with chemical solvent extraction: (1) nontoxic and provides nonoxidizing environment to avoid degradation of extracts, (2) low critical temperature (around 31°C) which prevents thermal degradation of products, (3) high diffusivity and low surface tension which allow penetration in pores smaller than those accessible by chemical solvents, and (4) easy separation of CO2 at ambient temperature after extraction [39, 59, 60]. However, the main disadvantages of supercritical CO2 are the high cost of operation, skilled labour, high capital investment, and safety related issues.


## 5. Waste to Energy

As discussed in the earlier Section4 several LCA studies [37, 47, 61] have indicated that the energy conversion efficiency ratio (EER) obtained for microalgae based biofuels is relatively lower than that of oil bearing crops. Several energy hotspots were identified in the overall algal based biofuels production process such as the use of inorganic source of nitrogen, operation, and maintenance of photobioreactor and harvesting/dewatering of microalgae biomass. Hence, it is recommended that culturing microalgae for biofuels production should be coupled with wastewater treatment with the aim to minimize heavy dependency on inorganic nutrients, reduce carbon and water footprints, and at the same time treat wastewaters.As shown in Figure1 high rate algal ponds (HRAP) are shallow and they have been widely used for the treatment of municipal, industrial, and agricultural wastewaters. In 1957 Golueke et al. [24] first proposed the use of HRAP for large scale production of algal based biofuels using wastewaters.Figure 1
High rate algal ponds in Arizona, US (Renewable Fuel and Energy B.V.) [62].HRAP have a depth of 0.2 to 1.0 meter and mixing is provided by paddle wheel. The paddlewheel provides a horizontal water velocity 0.15 m/s to 0.3 m/s. The CO2 can be added into a countercurrent gas sparging pump (~1.5 m depth) creating turbulent flow within the pond [63]. As shown in Figure 2 raceway ponds can be configured as multiple loops around central dividing walls. These raceway ponds can be baffled as shown on Figure 2 to enhance mixing.Figure 2
Raceway ponds with multiple loops and baffles [64].Algal biomass production from wastewater HRAP offers an attractive proposition with regard to the carbon footprint. The HRAP construction and operation are needed for providing wastewater treatment. Thus, the algal biomass is a byproduct which represents the biofuels feedstock which is free from environmental burden. For example, Shilton et al. [66] gave an example for a town of 25,000 people in the English countryside; they were using a pond for treating their wastewater instead of electrochemical treatment system resulting in saving 35 million kWh over a 30-year design life. It was noted that for UK an average of 0.43 Kg of CO2 was emitted per kWh of electricity produced and this amounts to 500 tonnes of CO2and that would require a land of 200 hectares of pine forest for CO2 mitigation.Although pond systems are common forms of wastewater treatment technology and used in smaller communities around the world, to date HRAP has not been widely utilized. However, with increasing regulatory pressure to improve wastewater treatment and with increasing recognition of the renewable energy production and improve greenhouse gas mitigation that HRAP offer, it is likely that they will be utilized in the future. Table2 compares commercial production of HRAP and wastewater treatment HRAP for biofuels production.Table 2
Comparison of commercial and wastewater treatment HRAP.
Factors
Commercial production HRAP
Wastewater treatment HRAP
Reference
Capital, operation, and maintenance cost
Requires heavy investment
Covered by wastewater treatment
[39, 40]
Land use
High
Covered by wastewater treatment
[40, 41]
Commercial availability
Already established for high bioactive compounds
Already established at a small scale for wastewater treatment.
[40, 42]
Most costly parameters
Water, fertilizer, harvesting, and mixing
Covered by wastewater treatment
[41, 43]
Limiting factors for algal growth
Light, temperature, nutrients, CO2 (externally provided)
Light, temperature, nutrients (internally provided by wastewater treatment), CO2 (partially provided by bacteria by the oxidation of organic compounds and by the exhaust gas available in wastewater treatment facilities).
[40, 41, 43]
Algal productivity
High productivity, as high as 30 gm/m2/d
High productivity is not the main driver, the emphasis is more on waste treatment and the algal biomass is the byproduct
[43–45]
Harvesting
Due to small sized cells <20 µm
Bioflocculation of algal cells achieved by aggregation of algal cells with wastewater bacteria.
[43, 45]
Water footprint
Requires significant amount of water and net water loss via evaporation
Not applicable
[44]
Risk of contamination
Comparatively lower
High
[46]
Algal species
Possible to cultivate single species microalgal cells. However, so far only extremophiles which can survive under extreme conditions are used for raceway algal cultivation
Maybe possible by selective biomass recirculation
[42, 46]Another method to cultivate low cost microalgal biomass is by growing them in enclosed semipermeable membranes filled with wastewaters and allow them to float in the oceans, for example, the OMEGA (offshore membrane enclosure for growing microalgae) project carried out at NASA Ames Research Center [67, 68]. Figure 3 shows the prototype of the OMEGA project. This method has an advantage over land based microalgae cultivation for fuel production. The OMEGA project does not require land; the fresh water algae can be grown in the enclosed semipermeable membranes filled with wastewaters and the waves of the ocean will provide mixing. The algae will feed on the nutrients available in wastewaters that are contained in the enclosures, while the cleansed freshwater is released into the surrounding ocean through the membrane by forward osmosis [69]. The forward osmosis membranes use relatively small amounts of external energy compared to the conventional methods of harvesting algae, which is an energy intensive dewatering process. Forward osmosis enables the membrane to absorb carbon dioxide from the air, release oxygen, and at the same time release fresh water through the membrane into the ocean [67]. The temperature will be controlled by the heat capacity of the ocean. Even if the membrane leaks, it will not contaminate the local environment in the ocean. The enclosed fresh water algae will die in the ocean. Nevertheless, further LCA and economic evaluation are needed to commercialize OMEGA at a feasible scale. This is a win-win strategy in reutilizing the waste to produce another source of energy which greatly amplifies the sustainability of microalgae biofuels.Figure 3
NASA OMEGA prototype [65].


## 6. Water Management Issues When Cultivating Microalgae

A recent study done by National Academy of Science, a nonprofit organization in the United States, pointed out several high-level concerns for large-scale development of algal biofuel, including the relatively large quantity of water required for algae cultivation. In fact, to produce the amount of algal biofuel equivalent to 1 liter of gasoline, between 3.15 liters and 3.65 liters of freshwater is required, depending on the production pathway [65, 70].Water not only provides a physical environment in which the algae live and reproduce but it also delivers nutrients, removes waste products, and acts as a thermal regulator. Unlike natural environments, mass cultivation systems require that the water be acquired, contained, circulated, and pumped to and between desired locations. All of these activities entail inputs of energy, both direct and indirect, and the amount of energy expended is tightly coupled to the volume of water involved. The volume of water involved depends on system geometries, losses from the system, and, most importantly, the ability to reclaim and reuse water.Algae require considerable amounts of water in order to grow and thrive. The organisms themselves are typically 80–85% water and the photosynthetic process results in the dissociation of roughly one mole of water per mole of CO2 [70, 71]. This means that approximately 5–10 kg of water is consumed per kg dry biomass.Hence, saline systems are, in general, considered preferable to freshwater systems because they minimize diversion of freshwater from other critical applications such as human consumption and conventional irrigation. Therefore, in an algal cultivation system for an effective water management we need to estimate the amount of water needed to support the culture at a target biomass productivity level at any given time and also the amount required to replace water that is removed from the cultivation ponds, either as a function of system design or due to evaporation.


## 7. Conclusion

There is a golden opportunity for researchers in this field to explore other potential utilization of microalgae biomass and to further diversify more value added products that can generate revenues from microalgae. Also, based on several LCA studies the EER for microalgae is still relatively low compared to high energy crops such as rapeseed, palm, and jatropha. It is recommended that culturing microalgae for biofuels production should be coupled with wastewater treatment with the aim to minimize heavy dependency on inorganic nutrients to reduce carbon footprint and water footprint and improve the economics of algal biomass production for biofuels and for treating wastewaters. However, the real potential of using wastewater to culture microalgae is still uncertain and yet to be explored since wastewater.Extraction of lipid from microalgae presents a complicated task. Physical extraction method which is suitable to extract oil from oil bearing crops is not efficient in extracting lipid from microalgae since the lipid is embedded within a layer of cell wall. Cell disruption method followed by chemical solvent extraction is necessary to recover the lipid effectively. However, care should be taken as some of the cell disruption methods require large quantity of energy input that could lead to negative energy balance. Several breakthrough technologies such as supercritical extraction/transesterification, in situ transesterification, supercritical water reactor, and hydrothermal recovery are yet to economically be scaled up to enhance microalgae biodiesel, biogas, or biocrude oil production.For long-term sustainability and environmental benefits, all the processing stages of microalgae biofuels should be simplified without involvement of extensive energy input especially drying. In addition, the processes should be easily adopted in the existing biofuels industry that can be implemented immediately especially in third world countries. This is because culturing microalgae for biofuels production is not only meant for profit making and benefiting the environment but also to help people from the bottom billions in terms of food and energy security.



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