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Review

Cultivation and Biorefinery of Microalgae (Chlorella sp.) for Producing Biofuels and Other Byproducts: A Review

1
Bioresource Collection and Research Center, Food Industry Research and Development Institute, Hsinchu 30068, Taiwan
2
Aquatic Technology Laboratories, Agricultural Technology Research Institute, Hsinchu 30068, Taiwan
3
Department of Biological Science and Technology, National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan
4
Department of Pediatrics, Hsinchu Mackay Memorial Hospital, Hsinchu 30071, Taiwan
5
Department of BioAgricultural Sciences, College of Agriculture, National Chiayi University, Chiayi 60004, Taiwan
6
Department of Biological Science and Technology, National Chiao Tung University, Hsinchu 30068, Taiwan
7
Center for Intelligent Drug Systems and Smart Bio-devices (IDS2B), National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan
*
Author to whom correspondence should be addressed.
These authors contributed equally to the manuscript.
Sustainability 2021, 13(23), 13480; https://0-doi-org.brum.beds.ac.uk/10.3390/su132313480
Submission received: 6 November 2021 / Revised: 21 November 2021 / Accepted: 3 December 2021 / Published: 6 December 2021
(This article belongs to the Special Issue Microalgal Bioprocess and Sustainability)

Abstract

:
Microalgae-based carbon dioxide (CO2) biofixation and biorefinery are the most efficient methods of biological CO2 reduction and reutilization. The diversification and high-value byproducts of microalgal biomass, known as microalgae-based biorefinery, are considered the most promising platforms for the sustainable development of energy and the environment, in addition to the improvement and integration of microalgal cultivation, scale-up, harvest, and extraction technologies. In this review, the factors influencing CO2 biofixation by microalgae, including microalgal strains, flue gas, wastewater, light, pH, temperature, and microalgae cultivation systems are summarized. Moreover, the biorefinery of Chlorella biomass for producing biofuels and its byproducts, such as fine chemicals, feed additives, and high-value products, are also discussed. The technical and economic assessments (TEAs) and life cycle assessments (LCAs) are introduced to evaluate the sustainability of microalgae CO2 fixation technology. This review provides detailed insights on the adjusted factors of microalgal cultivation to establish sustainable biological CO2 fixation technology, and the diversified applications of microalgal biomass in biorefinery. The economic and environmental sustainability, and the limitations and needs of microalgal CO2 fixation, are discussed. Finally, future research directions are provided for CO2 reduction by microalgae.

Graphical Abstract

1. Introduction

Global population growth is increasing the demand for food, fiber, forage, and renewable biomass resources for energy, biofuels, and chemical products [1,2]. Policies must promote the long-term use of biomass and mitigation of climate change. Environmental pollution leads to global warming, i.e., via the emission of greenhouse gases (GHGs), which consist of approximately 72% carbon dioxide (CO2), 19% methane (CH4), 6% nitrous oxide and 3% fluorinated gases. CO2 is the principal GHG, and the emission of CO2 primarily results from the combustion of fossil fuels [3,4]. In 2015, the Paris Agreement claimed “net zero emissions of carbon” as a long-term global goal between 2050 and 2100. The United States (U.S.) National Oceanic and Atmospheric Administration (NOAA) reported that global average CO2 concentrations increased to approximately 417 ppm in 2020 and that the global CO2 rate is increasing annually. Rising GHG concentrations lead to global warming and climate change, which are believed to aggravate regional and global water scarcity [5,6]. Advanced strategies of CO2 mitigation have received increasing attention in the last decade [7,8,9], and many countries are actively immersed in processing/developing technologies to reduce GHGs [10,11].
Common carbon fixation or sequestration techniques include multidisciplinary physical [12,13], chemical [14], and biological [15,16] approaches. The biological approach of carbon fixation, i.e., CO2 biofixation, involves absorbing and utilizing CO2 by photosynthesis in autotrophic organisms or plants. Because solar energy is the main source required for CO2 biofixation, the operating costs are lower than those of chemical and physical methods. Additionally, fixed carbon can be converted into biomass for further applications, i.e., biomass can be recycled. Therefore, photosynthetic CO2 biofixation is a promising technology for carbon fixation [17,18]. As shown in Figure 1, microalgae are some of the most efficient photosynthetic organisms for CO2 biofixation as microalgae cultures have higher growth rates, higher conversion yields, lower demands for water, and smaller requirements for land area than terrestrial plants [16,19,20]. The factors of CO2 biofixation influence microalgal strains, CO2 from flue gas, nutrients from wastewater, light, pH, temperature, and cultivation system [7,9,15,16,17]. Microalgal biomass is generally composed of approximately 50% carbon by dry microalgal cells because of the estimated CO0.48H1.83N0.11P0.01 of the approximate molecular formula of microalgal biomass [21,22]. When microalgal biomass carbon is produced from CO2, approximately 1.83 g CO2 is consumed to produce 1 g microalgal biomass [23,24]. The produced microalgal biomass can be utilized to produce lipids (oil) and carbohydrates as a source of chemical precursors and biofuels [25,26,27,28]. Palm oil mill effluent (POME) in microalgal cultivation is utilization to not only obtain the wastewater treatment by chemical oxygen demand (COD) reduction, but also the resulting microalgal biomass, to be a good feedstock as biofuels, such as biodiesel and bioethanol [1]. The maximum biomass production and lipid yield of Chlorella sp. in POME as medium was obtained in the optimal condition of 10.9% CO2 and 9963.8 lux of light intensity through central composite designs [3]. The microalgal growth and lipid production were enhanced by the addition of phytohormone indole-3-butyric acid (IBA) [2], ferroferric oxide (Fe3O4) nanoparticles [29], sodium nitrate (NaNO3) [30], glycerol [31], etc. Additionally, the producing biomass microalgal CO2 fixation can be used to produce specific components that can be refined as high-value byproducts to realize the economic sustainability [32]. Based on the premise of complying with biosafety, the specific components of microalgae, such as lutein, β-carotene, zeaxanthin, fucoxanthin, and proteins can be further applied in food, animal feed, cosmetics, nutrient supplements, and pharmaceutical products [33,34,35,36]. Microalgae biological carbon fixation technology is beneficial at reducing carbon emissions, but how to achieve economic and environmental sustainability—at the same time—is a considerable challenge.

2. Factors Influencing CO2 Biofixation by Microalgae

The production of microalgal biomass is highly influenced by the suitability of microalgae strains, CO2, light, pH, culture system, temperature, and nutrients [37,38,39]. The sources of CO2 and nutrients for microalgal cultivation can be flue gas and wastewater, respectively. Therefore, many studies have investigated whether flue gas and wastewater can be integrated with microalgal cultivations, to achieve not only CO2 reduction, but also CO2 reuse for microalgal biomass conversion to produce biofuels. Flue gas and wastewater can also be treated by microalgal cultivations to obtain environmentally friendly and health-friendly effects [25,40,41,42,43]. In the process of microalgae cultivation, one single factor does not affect the growth of microalgae; it is often the interaction of multiple factors [44]. Therefore, keeping the performance of long-term and stable microalgal cultivation will determine the microalgal growth, especially outdoor cultivation.

2.1. Microalgal Strains

Many studies have indicated highly efficient ways to obtain CO2-tolerant, alkali-tolerant, and/or thermotolerant microalgae with high CO2 fixation efficiency. Microalgal strains could be obtained by screening the environment, by random mutagenesis or by genetic modification (Table 1). Improving the capacity of CO2-tolerant microalgae was good for application in flue gas containing high concentrations of CO2 to reduce the CO2 poisoning effect and increase CO2 fixation productivity [45]. The level of CO2-tolerant microalgae is usually referred to as high, very high, and extremely high, according to ranges of 2–5, 5–20, and 20–100% CO2-tolerant concentrations [46]. As shown in Table 1, these strains not only have the ability to withstand very high CO2 concentrations, but also have better growth performances, to obtain higher CO2 fixation efficiency. Flue gas from steel plants containing approximately 25% CO2, 70–80 ppm nitrogen oxides (NOx) and 80–90 ppm sulfur dioxide (SO2) resulted in up to 90% NOx and SO2, along with 50% CO2 removal efficiency by the cultivation of Chlorella sp. MTF-15 [47,48]. Because CO2 is the main component in boiler flue gas with trace amounts of sulfur oxides (SOx), the resulting biomass after CO2 fixation may be used as an animal additive or feed without the concern of posing biosafety risks [49]. To improve the CO2 fixation efficiency, the screening of alkali-tolerant microalgae has been investigated [50,51,52]. It is known that when the pH of water is above 6.3, dissolved CO2, bicarbonate (HCO3), and carbonate (CO32−) are the dominant species [53]. Therefore, elevated CO2 dissolution can be utilized in microalgae growth by increasing the pH of the culture medium. An alkali-tolerant Chlorella sp. AT1 was isolated and cultured in alkaline medium (pH = 11) with 10% CO2 aeration [50]. Chlorella sorokiniana SLA-04, which was isolated from alkaline Soap Lake, could adapt to growth in extremely high-pH media (pH > 10) [51,52]. The high biomass productivities of Chlorella sorokiniana SLA-04 were obtained by scavenging CO2 from only the atmosphere at high rates in pH > 10 medium during phototrophic cultivation. Excessive light intensity will cause the internal temperature of the cultivation system to rise, causing the growth of microalgae to be inhibited. Two effective thermotolerant mutants, M18, and M24 of Chlorella pyrenoidosa obtained by mutagen treatment, were capable of surviving at temperatures up to 47 °C, and showed optimal growth at 37 °C [54]. The research on screening specific algae strains in Table 1 is mainly in Taiwan, including the characteristics of CO2, alkali, and thermo-tolerance. However, in subtropical zones, the temperature of microalgal culture broth in PBRs can go up to about 40 °C by irradiation of sunlight [47], showing that the screening of thermotolerant strains is very important. The thermotolerance of Chlorella sp. M4, which was obtained by mutagenesis treatment from Chlorella sp. GD, was capable of overcoming high-temperature inhibition during outdoor culture due to high photosynthetic efficiency and biomass productivity at 40 °C with high-concentration CO2 aeration [55]. Thermotolerant microalgal strains can also be screened from high-temperature zones, such as the effluent of steel-making, power generation plants, and hot springs [56]. Thermotolerant microalgae are excellent candidates for large-scale outdoor cultivation, especially in subtropical and tropical countries [57]. Dual CO2 and thermotolerant Chlorella sp. strains 283 and 359 were isolated from their original strain of Chlorella vulgaris ESP-31 by N-methyl-N-nitro-N-nitrosoguanidine (NTG) mutagenesis [58]. The microalgal strain grew well at 40 °C and had high biomass productivity, 0.73–0.89 g L−1 d−1, for a 4-day culture.

2.2. CO2 from Flue Gas

Flue gas is the main source of CO2 emissions on Earth. CO2 in flue gas has been used as a carbon source for microalgae cultivation in most studies (Table 2). However, CO2 fixation by microalgae still has many problems that need to be overcome. For example, high-CO2 tolerance in microalgae is insufficient and directly discharges flue gas into microalgal culture ponds, which might lead to rapid changes in the pH of the culture broth [48,63,64]. When microalgae cannot adapt to extreme culture conditions, death of the microalgae will occur. Therefore, it is necessary to screen microalgae for pH tolerance. In general, the main component of flue gas is CO2, which presents a variety of CO2 concentrations, depending on the fuel source and the design of the plant. Chlorella sp. MTF-15 was cultured with flue gas aeration from a hot stove (26% CO2), coke oven (25% CO2), or power plant (24% CO2) at the China Steel Corporation, the largest steel plant in Taiwan. The biomass productivity of the microalgae cultured with flue gases from coke ovens, hot stoves, and power plants was 0.515, 0.314, and 0.342 g L−1 d−1, respectively [48]. Chlorella sp. was cultured in medium, with a controlled pH of 6, by aerating with synthetic flue gas (30% CO2) obtained from the African Oxygen Company in South Africa, and the maximum biomass concentration and biomass productivity were 3.42 g L−1 and 0.145 g L−1 d−1, respectively [40]. When Chlorella sorokiniana was aerated with flue gas (16% CO2) from the oil-producing industry of India, the maximum CO2 sequestration was 3.07 g L−1 [65]. The maximum biomass concentration and biomass productivity of Chlorella sp. KR-1 aerated with flue gas from a coal-burning power plant in Korea were 2.81 g L−1 and 0.561 g L−1 d−1, respectively, and the CO2 removal efficiency was approximately 13% [66]. The maximum specific growth rate and biomass concentration of Chlorella fusca LEB111 aerated flue gas (10% CO2) from coal power plants in Brazil were 0.181 d−1 and 1.24 g L−1, respectively [67]. The efficient biomitigation of CO2 (12–15%), NOx (0.01–0.08%), and SOx (0.006–0.06%) of flue gas from a power plant was obtained by the cultivation of Chlorella vulgaris [68,69]. The biomass concentration and amounts of CO2 sequestration of Chlorella sp. aerated with flue gas produced from the burning of coal were 1.92 g L−1 and 0.974 g L−1, respectively [70]. When integrated with sewage and flue gas in microalgal cultivation, the biomass concentration and CO2 removal efficiency of Chlorella vulgaris aerated with a coal-burning boiler (6% CO2) in India were 1.72 g L−1 and 90%, respectively [71]. A microalga Chlorella sp. Cv could tolerate the full-simulated flue gas, 10% CO2 + 200 ppm NOx + 100 ppm SOx. Under optimal conditions, the microalga could tolerate the simulated flue gas, and the maximum specific growth rate was 0.9824 d−1 [72]. It was proposed that the upregulation of several genes related to photosynthesis, oxidative phosphorylation, CO2 fixation, sulfur metabolism, and nitrogen metabolism was beneficial for the evolved microalga strain to tolerate the simulated flue gas [64]. Countries with high dependence on coal, such as China and India, are also actively engaged in CO2 carbon reduction research, using CO2 from the exhaust gas in microalgal cultivation to achieve carbon reduction, and use the produced microalgae biomass as a feedstock of biofuels. It has the opportunity to achieve economic and environmental sustainability by integrating the CO2 reutilization of exhaust gas and the effective development of biofuels.

2.3. Nutrients from Wastewater

In 2015, the United Nations World Water Development Report noted that the available freshwater resources globally will decrease by 40% by 2030. However, more than 80% of the world’s wastewater is discharged into the environment without treatment. The management model for wastewater should be changed from “treatment and disposal” to “reuse, recycle, and resource recovery”. Therefore, the use of wastewater for microalgae cultivation is a technological development trend [43,73,74]. The source of wastewater can be mainly divided into three categories: agricultural, municipal wastewater, and industrial wastewater. As illustrated in Table 3, the growth performance and biomass productivity of microalgae cultured in different types of wastewater were different because the contents of COD, total nitrogen (TN), total phosphorus (TP), and specific inorganic substances in wastewater were obviously different [25,44,49,75].

2.3.1. Agriculture Wastewater

The main source of agricultural wastewater was large livestock and poultry operations, and the main components in this wastewater were ammonium and organic nitrogen, which are good for microalgal growth. Piggery wastewater is commonly used in microalgal cultivation because this wastewater is rich in nutrient sources [76,77,78,79,80]. Additionally, aquaculture is a fast-growing industry because it has significantly increased the global demand for fish and seafood. Novel aquaculture systems incorporating wastewater treatment and effluent reuse have been rapidly developed for compliant wastewater discharge. Although the nutrient content of aquaculture wastewater is significantly lower than that of piggery wastewater, the content of pathogenic microorganisms and heavy metals contained in aquaculture wastewater is relatively low [81,82]. Therefore, aquaculture wastewater can be used as a large amount of water needed for microalgal cultivation, and the resulting microalgae biomass can be applied not only to a feedstock of biofuels, but also to animal additives or feed, which is a more minimal biosafety issue [49]. In Taiwan, most livestock wastewater is produced from pig farming. Therefore, it can be seen that the state has actively invested in research on the treatment of piggery wastewater. The raw piggery wastewater without pre-treatment could also be applied in microalgal cultivation. The produced microalgal biomass has about 20% lipids and is suitable for use as a feedstock of biodiesel [25,49,77,83].

2.3.2. Municipal Wastewater

At present, a large amount of municipal wastewater is being produced due to an increase in urban population growth. The composition of municipal wastewater varies greatly because of the substances from various families, businesses, and institutions. For example, the COD and TN in a municipal sludge digestate were 2175 mg L−1 and 840 mg L−1, and 164 mg L−1 and 43.2 mg L−1 [84], in municipalities with reserve osmosis concentrate [85], respectively. Generally, the COD, TN, and TP utilization efficiencies of municipal wastewater in microalgal Chlorella cultivation were approximately 85–100%, 80–100%, and 90–100%, respectively (Table 3). However, growth and biomass productivity are low because municipal wastewater lacks nutrients for microalgae utilization [86,87,88]. Research on the reutilization of municipal wastewater in microalgae cultivation is commonly seen in many countries, such as United Kingdom (GB), USA (US), Australia (AU), etc. Due to the difference in the compositions of wastewater, to apply the technology of microalgal cultivation to cities, the culture process needs to be modified depending on the region to achieve stable growth of microalgae, and further, to achieve the dual advantages of wastewater purification and CO2 reduction.

2.3.3. Industrial Wastewater

Some small- and medium-sized enterprises and informal industries often discharge wastewater into municipal pipelines or directly discharge it into the environment. Compared with the hazards caused by agricultural and municipal wastewater, industrial wastewater could be more harmful to water resources and the environment due to the contents of toxic heavy metal components. There are also studies on diluting the wastewater to reduce the sensitivity of the microalgal strain towards the toxicity of wastewater, and increase the wastewater utilization effectivity to obtain the microalgal growth [25,89]. However, wastewater from food processing is usually regarded as a safety resource and is suitable for the production of microalgal biomass for feed or food uses [90]. Because the sources of industrial wastewater were obviously different, the ranges of COD, TN, and TP utilization efficiencies of industrial wastewater in microalgal Chlorella cultivation were approximately 25–95%, 30–100%, and 50–100%, respectively [84,91,92,93] (Table 3). The COD, TN, and TP contents of the food industry wastewater is relatively rich, which is very suitable for use as nutrient sources for microalgae cultivation. Therefore, the better growth of microalgae can be obtained. However, the problem of bacterial contamination is more likely to occur because of the higher nutrient contents. This will affect the long-term stable performance of the microalgal cultivation technology.
Table 3. Biomass and lipid production and productivity of the microalgae Chlorella cultures using wastewater.
Table 3. Biomass and lipid production and productivity of the microalgae Chlorella cultures using wastewater.
Wastewater SourceMicroalgaeCOD 1 (mg L1)TN 1 (mg L1)TP 1 (mg L1)Biomass Productivity (g L1 d1)CO2 Fixation Efficiency 2 (g L1 d1)Lipid (%)Lipid Productivity 3 (g L1 d1)Country 4References
Agricultural wastewater
Raw dairyChlorella sp.25932831160.2610.478--CN[76]
Anaerobically treated piggeryChlorella vulgaris CY5377287280.2810.51419.60.055TW[77]
PiggeryChlorella sp. GD490550200.6811.24621.80.148TW[25]
Aquaculture121234151.2962.37221.30.276TW[49]
SwineChlorella vulgaris UTEX-26514813074.30.2470.45227.10.067KR[78]
PiggeryChlorella sorokiniana AK-11500–4500500–700150–2500.551.006--TW[83]
Livestock wasteChlorella sp.20002221030.2890.52936.30.105CN[79]
Municipal wastewater
CentrateChlorella sorokiniana UTEX1230-539.40.0830.1529.40.008GB[86]
DomesticChlorella vulgaris1425690.0540.09921.50.012US[94]
Chlorella minutissima0.0490.09022.90.011
MunicipalChlorella vulgaris SAG 211-11b2175840100.1440.264230.033FI[84]
SecondaryChlorella vulgaris UTEX 26131112350.0780.1438.70.021MX[87]
Chlorella vulgaris CICESE0.1050.19220.20.025
CentrateChlorella vulgaris513803320.0710.13029.60.021CN[88]
Municipal
(osmosis concentrate)
Chlorella vulgaris16443.213.10.320.585--AU[85]
Industrial wastewater
Meat processingChlorella sp. UM61512100212540.1710.31317.50.029US[90]
FoodChlorella vulgaris341--0.2070.379310.064CN[91]
Pulp and paperChlorella vulgaris SAG 211-11b905350280.2080.38121.70.045FI[84]
Alcohol and starch processingChlorella pyrenoidosa3599334390.3760.68819.70.074CN[92]
Tofu wheyChlorella pyrenoidosa FACHB-9-592490.2830.51817.50.049CN[93]
1 COD, TN, and TP: chemical oxygen demand, total nitrogen, and total phosphorus of wastewater. 2 CO2 fixation efficiency (g L−1 d−1) was calculated by 1.83-fold of biomass productivity. 3 Lipid productivity (g L−1 d−1) = (biomass productivity × lipid content)/100. 4 Country abbreviation: China (CN), Taiwan (TW), Korea (KR), United Kingdom (GB), USA (US), Finland (FI), Mexico (MX), Australia (AU). -: Data not shown.

2.4. Light

Because of photosynthesis for microalgal growth, light is the most important parameter in microalgal cultivation. Lighting in microalgal cultivation contains two main factors: light intensity and the wavelength of light. In general, the growth rate of microalgae can be greatly increased along with an increase in light intensity; however, when the light intensity exceeds the saturation light that can be tolerated by microalgae, the growth rate of microalgae will be significantly decreased [95]. Therefore, to achieve the maximum growth rate of microalgae, the light intensity is usually controlled to “light saturation”. Because microalgae itself will block light from passing, the light intensity decreases sharply with distance through the surface, causing a decrease in the growth rate of microalgae [96]. Under 400-μmol m−2 s−1 specific light intensity, the microalgal biomass productivity of a Chlorella sp. strain in photobioreactors (PBRs) was approximately 2-fold higher at 0.518 g L−1 d−1 than that grown in outdoor raceway open ponds [24]. The growth of microalgae Chlorella increased by continuous illumination using a light-emitting diode (LED) at the optimal light intensity without a shortage in light energy [97,98]. The incremental light intensity strategy was also an efficient way to improve microalgae growth because photoinhibition at the initial culture phase and insufficient light intensity at the latter culture phase could be avoided [99]. In terms of the wavelength of light, a wavelength range of 400 to 750 nm is absorbed during photosynthesis by most microalgae. The light source for the autotrophic cultivation of Chlorella vulgaris was investigated, and the results showed that red LED light (630–665 nm) resulted in small cells with active divisions, while blue light (430–465 nm) LED illumination led to a significant increase in cell size [100]. The mixed LED light wavelength with red and blue LED light (e.g., red:blue is 5:5) also affects and enhances microalgal growth, including Scenedesmus obliquus, Neochloris oleoabundans, and Chlorella vulgaris [101].

2.5. pH

The pH of culture broth affects the enzyme activity related to the metabolism of microalgae and the ion absorption efficiency of microalgae, which in turn affects the growth and carbon fixation efficiency of microalgae [50,102]. The optimal pH for growth varies among microalgal species, and in general, the optimum pH is neutral for most microalgae [103]. Flue gas usually contains high concentrations of CO2, NOx, and SO2 [48]. When microalgae were directly aerated with flue gas containing 10–30% CO2, the pH of the culture broth might be reduced to 5.5 [7]. When the microalgae were aerated with flue gas containing SO2 at 100 to 250 ppm, the pH of the culture broth decreased to pH 2.5 to 3.5 to generate bisulfite (HSO3), sulfite (SO32−), and sulfate (SO42−) [7]. If the flue gas is directly aerated into the culture broth of microalgae without dilution, the excess CO2 of flue gas will be discharged back to the atmosphere. To reduce the CO2 discharged back to the atmosphere, the CO2 captured from flue gas aerated into alkaline medium is easily converted into HCO3, which is dissolved in water and used for microalgal growth. The solubility of CO2 in water is low, but the CO2 content in the culture broth can be increased under alkaline conditions to further increase the CO2 utilization efficiency of microalgae [104]. In addition, gradually increasing the pH in a microalgal culture is desirable for reducing microbial diversity and is good for outdoor cultivation of microalgae [105].

2.6. Temperature

The optimal temperature range for microalgae growth is generally 15–26 °C [106]. Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity may be a primary site of damage by elevated temperature to cause a decrease in photosynthesis efficiency [107]. In contrast, there was not only a decrease in the metabolic rate of microalgae, but also a decrease in CO2 solubility in culture broth. Therefore, the optimal temperature for growth varies among microalgal species. The temperature of the flue gas will generally be as high as 120 °C or even higher [48]. Flue gas usually needs cooling to be aerated into the culture broth because the temperature of flue gas is too high. If the thermal-tolerant potential of microalgae is good, the cost of flue gas cooling can be reduced. In addition, when sunlight is used outdoors as a light source, the temperature of the culture broth easily changes with the surrounding environment. Béchet et al. [108] indicated that 18,000 GJ year−1 ha−1 of heat energy must be removed to maintain the broth temperature of column PBRs at or below 25 °C. Considering the cost of temperature control, thermotolerant microalgal strains are needed, especially in large-scale outdoor cultivation. When Chlorella sorokiniana was cultivated in outdoor 51-L column PBRs, the culture broth temperature reached 41 °C without growth inhibition [109], and similar results showed better growth performance under uncontrolled temperature in outdoor conditions [55,57].

2.7. Microalgal Cultivation System

Open (raceway) ponds and PBRs of microalgal cultivation systems are usually—and primarily—adopted. Studies on CO2 fixation by microalgae used in open ponds and PBRs are outlined in Table 4. It has been reported that microalgal biomass production produced from open ponds is more efficient than 90% of worldwide biomass production [110]. The most prominent features of open ponds include simple construction, low cost and easy operation [111,112]. However, disadvantages of open ponds are also obvious, such as a large footprint, difficulties in operation control, unstable culture conditions, high evaporation loss, easy contamination, and the decay of light intensity with medium depth. Compared with open ponds, PBRs have many advantages, such as the most efficient mixing, the best growth conditions, high volumetric mass transfer rates, low risk of contamination, lowest losses of CO2, low shear stress and relatively low energy consumption [18,75,113]. However, the limitations of PBRs are construction cost and scale-up [114]. Overcoming the above shortcomings of cultivation systems is a future research direction for developing advanced cultivation systems. The two cultivation systems still have many challenges in practical operation [115]. Closed cultivation systems, e.g., PBRs, are still not widely applied in industry because the operation cost and construction costs of the systems are too high despite the high microalgal biomass productivity [116]. To solve the limitations of large-scale outdoor microalgae cultivation systems, from an engineering perspective, how to increase the efficiency of gas aeration and mixing should be considered. Low cost and energy consumption can both be achieved by the design of air mixing with flue gas CO2 aeration to improve microalgal growth by sufficient CO2 utilization. Therefore, outdoor large-scale microalgae cultivation systems can become closer to the industrialization process and commercial application by improving the efficiency of gas aeration and mixing. Suitable microalgal cultivation systems usually depend on factors such as cost, CO2 capture source, nutrient sources, and the type of target products. At present, most studies on CO2 fixation by microalgae are used in open ponds or PBRs, and few studies have integrated both microalgal cultivation systems to enhance biomass productivity [24,117]. In our previous study [24], an efficient PBRs/raceway circulating (PsRC) system integrated with the advantages of PBRs and paddlewheel-driven raceway ponds had great potential for the mass cultivation of microalgae. The total amount of CO2 fixation of the PsRC system was approximately 1.2 kg d−1 with 50% CO2 utilization efficiency, as simultaneous microalgal biomass production and CO2 fixation occurred by cultivating alkali-tolerant Chlorella sp. AT1 with alkaline-CO2 capturing operation in the PsRC system. Long-term cultivation for 40 days in a novel membrane photobioreactor, the steadily growth of Chlorella vulgaris were obtained and the maximum removal efficiency of CO2 was 80%. Because the self-forming dynamic membrane from microalgae was easy to harvest, the potential of achieving a sustainable CO2 fixation technology [118]. To investigate the carbon fixation effectivity of microalgae in outdoor cultivation, many studies have used the design of the cultivation system to scale up to pilot scale and industrial scale. The pilot scale is mainly used for research, because the expansion of the outdoor cultivation system may increase the cost of construction, the risk of microorganism pollution, and the release large amounts of CO2. In Table 4, the research in China and Taiwan has reached a ton scale, and it can be combined with waste gas for microalgae cultivation. The cultivation system combination the strategy of an increase of the CO2 content in the water for the microalgal growth and enhance the CO2 carbon fixation efficiency. One is to couple with spraying absorption tower to increase the CO2 content in the water [119], another is to use alkali-tolerant mutant strain combined with alkaline-CO2 capturing medium [24].

3. Biorefinery of Microalgal Biomass for Producing Biofuels and Byproducts

Microalgae cultivation is the most efficient method for biological carbon reduction and biofuel production [17,127]. Microalgal biomass cannot only be used as a feedstock for biofuels, but also be applied to the development of foods, nutrient supplements, cosmetics, and feed additives for animals and aquaculture (Figure 2). In recent decades, many global studies on microalgae have begun, and are actively engaged in the development and application of novel microalgae technologies with potential for commercialization [128]. Many international companies and countries throughout the world have also actively engaged in microalgae biorefinery research. For example, using microalgae as a feedstock, microalgal lipids can be treated with transesterification to produce biodiesel and jet fuel. Microalgal biomass polysaccharides can produce biofuels and various chemicals after chemical refinery processes and fermentation, and microalgal proteins can be used as feed additives [26]. Microalgal biomass also contains high-value compounds, such as carotenoids, lutein, and astaxanthin. Many biorefinery processes have been actively developed to convert microalgal biomass into biofuel, syngas, and even high-value chemical and biological byproducts. Microalgae are not a bioenergy source of commercialization in the short-term due to the low price of fossil fuels. Therefore, increasing the economic value of microalgae has become an important part of the development of microalgae technology. At present, the main uses of high-value microalgae are health foods, food additives and animal feed additives [19]. The biomass produced by the utilization of wastewater and waste gas in microalgae cultivation is mainly used as biofuel for biosafety considerations. However, from the perspective of economic value, it is recommended to further extract more functional compounds from the microalgal biomass, such as carotenoids, develop diversified high-value products. The final microalgae residue can also be used for biochar, so that the microalgae carbon fixation technology will have the opportunity to be truly applied to the industry.

3.1. Biodiesel

According to a 2017 report by Grand View Research, Inc., the global biodiesel market is expected to reach USD 54.8 billion by 2025. The market is expected to have a 7.3% compound annual growth rate (CAGR), owing to the increasing demand for biodiesel as a fuel in the automotive, marine, railway, and power generation industries. Biodiesel has become the mainstream biomass energy development and application in various countries worldwide due to its advantages of easy transportation, convenient storage, and direct application to current diesel engines [129]. At present, developed countries and developing countries are dedicated to an increase in biodiesel production. Therefore, countries around the world are still dedicated to the development of new feedstock for biodiesel production. Among various new feedstocks, microalgae have become feedstock for third-generation (3G) biodiesel because microalgae have a higher growth rate and utilization efficiency of solar energy than terrestrial oil-producing crops [130]. Microalgal oil production per unit of cultivated area is greater than that of other oil-producing crops [110]. The processing techniques of diesel from microalgal oil include pyrolysis and transesterification. However, when biodiesel is produced by pyrolysis, it is difficult to commercialize due to the consumption of a large amount of energy and the complexity of operation processes and produced products. Transesterification processing is the main processing for commercial biodiesel production because of its simple operation and low cost. In microalgae biorefineries, biodiesel development is the most frequently mentioned research topic due to fossil energy shortages. Therefore, several studies have investigated inexpensive and energy-efficient biodiesel obtained by integrating microalgae with flue gas aeration and wastewater reutilization [25,49,60,131].

3.2. Biobutanol

Carbohydrates of microalgae can be converted into fermentable sugars through hydrolysis to produce bioethanol and biobutanol [132,133]. Among the potential liquid biofuels, biobutanol is especially promising due to its higher energy density, lower hygroscopy, and superior physical and chemical properties as a gasoline additive to replace bioethanol. In addition to being a biofuel, biobutanol can also be used as a solvent for industrial purposes [134]. However, approximately 60% of the total biobutanol production cost comes from the feedstock cost. Therefore, carbohydrate-rich and fast-growing microalgae are considered potential feedstocks for biobutanol production [133,134]. Therefore, microalgal biomass, which is rich in carbohydrates, serves as a good and inexpensive feedstock for acetone-butanol-ethanol (ABE) fermentation to produce biobutanol [135]. The biobutanol production via ABE fermentation using carbohydrate-rich microalgae Chlorella vulgaris JSC-6 with 1% NaOH pretreatment and 3% H2SO4 hydrolysis was 13.1 g L−1 [136]. The highest biobutanol production by ABE fermentation using the resulting biomass of Chlorella sp. DEE006 was 6.23 g L−1 [137]. Wang et al. [133] used the carbohydrate-rich microalga Neochloris aquatica CL-M1 as a feedstock for butanol fermentation. Their results showed that the butanol concentration, yield, and productivity were 12.0 g L−1, 0.60 mol mol−1 sugar, and 0.89 g L−1 h−1, respectively.

3.3. Biogas

Microalgal biomass can be used as substrates for anaerobic digestion to produce biogas. Biogas mainly consists of 50–70% CH4, 30–50% CO2, and other trace amounts of nitrogen (N2), ammonia (NH3), and hydrogen sulfide (H2S) gases [138,139]. The distribution of macromolecule profiles, mainly including proteins, lipids, and carbohydrates, affects the efficacy of biogas production and changes because of microalgae species and culture conditions [140]. Moreover, the practical biogas production of microalgal biomass is lower than the theoretical production due to the rigid cell wall of microalgae, C:N ratio of microalgal biomass, and the conditions of anaerobic digestion [141]. When microalgae biomass was pretreated to break down the cell wall by pretreatment with heat, pressure, enzyme hydrolysis, microwave, and ultrasonication before anaerobic digestion, biogas production could be increased significantly [142,143]. Microalgal biomass could be used as a substrate and cosubstrate for biogas production [141]. A maximum production of approximately 240 mL CH4(g) volatile solids−1 was obtained by the co-digestion of chicken manure and microalgae Chlorella 1067 [144]. When CO2 was generated in the biogas, the calorific value of the biogas was reduced due to the lower amount of CH4 [145]. Therefore, CO2 in biogas can be used for microalgae culture for biogas upgrading, i.e., increasing the CH4 concentration of biogas. Kao et al. [61] established an outdoor microalgae-incorporating culture system with a gas cycle-switching operation that could be efficiently used as a CO2 capture model for biogas upgrading. The concentration of CH4 could be increased from the original 70% to 87% by utilizing CO2 in desulfurized biogas produced from the anaerobic digestion of swine wastewater by an outdoor cultivation of Chlorella sp. MM-2 [146]. The maximum CH4 content of the co-digested treatment of Napier grass and cow farm slurry group for 45 days was increased to 64.4%, which was 3.4-fold higher than that of the untreated group [147]. A new discovered process of direct interspecies electron transfer (DIET) can help to an increase of biogas production by promoting rapid electron donation and acceptance of microbes during the anaerobic digestion [148].

3.4. Aviation Fuels

Although microalgae biofuels are limited in the aviation industry [149], microalgae-based aviation fuels are considered a substitute to produce an efficient fuel. For example, United Airlines and Qantas have tried using blends of microalgal biofuel with up to 40% mixtures and have completed successful trials of the product. For some microalgae species, the free fatty acids in microalgae oil are nearly similar to those in crude petroleum. Aviation fuels are a complex mixture of a large number of hydrocarbons from C8 to C16 [150]. The conversion of microalgae oil into aviation fuel needs to reduce the number of carbon chains by catalytic processes because the carbon chains of microalgal oils are often C16 and C18 [151]. The catalytic process aims to modify the carbon molecules from microalgae oil to obtain the chemical structure or configuration known for aviation fuel [152].

3.5. Biochar

Biochar from agricultural crop, wood, animal manure, and microalgal biomass can be produced by thermochemical processes, such as pyrolysis, torrefaction, and hydrothermal carbonization [153]. Compared with the lignocellulosic biomass, it has a better chance of achieving the sustainable carbon reduction technology by microalgal biomass due to the lipid-rich characteristic [154]. The short-chain fatty acids (SCFAs) production was increased in the anaerobic fermentation of microalgae by applying the algae-derived biochar [155]. The high surface area of biochar BC-450 was made from the residue of marine Chlorella sp. after lipid and pigment extraction through ultrasonic extraction and pyrolysis. The removal efficiency of heavy metal including Cr(VI), Zn(II), and Ni(II), was in 84–99% by adsorbent of biochar BC-450 due to the higher surface area [156]. As a green adsorption material, microalgal-based biochar also is used in wastewater remediation [157]. The nutrient-rich biochar after wastewater treatment further can be applied as biofertilizer and used for soil amendment [158,159]. Although the large-scale application technology of biochar in soil amendments or biofertilizers is still under development, microalgae-based biochar is indeed a promising material for wastewater treatment, soil remediation, and gas storage and separation [160].

3.6. Lactic Acid and Succinic Acid of Fine Chemicals

When microalgae are rich in carbohydrates, microalgal biomass can be used for the fermentative production of fine chemicals, such as succinic acid and lactic acid [161,162,163]. Because lactic acid has both carboxyl and hydroxyl groups, it can be converted into many useful chemicals, such as pyruvic acid, lactate esters, 1,2-propanediol, and acrylic acid [164]. The fermentative lactic acid yield of Lactobacillus plantarum 23 using the acid hydrolysis of Chlorella sp. M4 was 0.43 g−1 microalgal biomass under anaerobic conditions for 24 h [55]. Succinic acid is used as an intermediate chemical for a wide range of applications, such as industrial, food, cosmetics, and pharmaceutical uses. According to the report of Markets and Markets in 2018, the global succinic acid market was estimated to be USD 132 million in 2018 and is projected to reach USD 183 million by 2023, at a CAGR of 6.8%. The biobased succinic acid market is forecast to grow at a significant rate because petroleum-based succinic acid is limited by the volatility of its price and carbon footprints. The microalgal biomass of Scenedesmus acutus was acid pretreated, and the algal liquor of the resulting slurry was used in continuous fermentation for 756 h with Actinobacillus succinogenes 130Z to produce succinic acid. The maximum production and productivity of succinate were 30.5 g L−1 and 1.1 g L−1 h−1, respectively [165].

3.7. Feed Additives

Compared with general food, microalgae contain high amounts of protein and complete compositions of amino acids [166]. In addition, the nutritional value of microalgae is high because they contain biologically active compounds, such as pigments, lipids, vitamins, and trace elements [167]. Therefore, dry microalgal powder is good for the development of human nutrition supplements and animal feed, such as livestock, poultry, and aquatic feed additives [62]. Notably, specific microalgal strains contain high concentrations of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), lutein, astaxanthin, carotene, and other components, which are mainly used in companies worldwide to develop cosmetic and nutrient supplements. Currently, consumer interest in algae has increased significantly. Therefore, many companies have attempted to develop foods containing microalgae and their byproducts [168]. Some microalgae species or strains, such as Chlorella, which have great conceivable uses in the human diet [168,169], are already commercially used in foods [170]. However, the topic of this review is focused on the cultured microalgal biomass used as animal feed additives.

3.7.1. Aquatic Living Organisms

Microalgae are widely used in aquatic living organisms. Microalgae can be used as a food source for brine shrimp, copepods, and rotifers. In addition to serving as fish bait, microalgae can also be used as bait for shrimp shellfish. Microalgae contain omega-3 polyunsaturated fatty acids (EPA and DHA), which are good for the growth of fry and an increase in the survival rate of juvenile fish [171]. The vitamin C of microalgae can accumulate in fish through the food chain, and nerve conduction function in fish is improved [172]. Furthermore, microalgal pigments are often used for the color enhancement of aquatic products [167]. After feeding microalgae containing carotenoids (such as lutein, astaxanthin and/or β-carotene), the color of the fish’s flesh can be enhanced, and the economic value of aquatic products can be further improved [173].

3.7.2. Animal Feed Additives

Technavio’s report indicated that the global animal feed market size will grow more than USD 110 billion during 2021 and 2025, at a CAGR of nearly 4% and that 39% of market growth will originate from the Asia Pacific Accreditation Cooperation (APAC) during the forecast period. Microalgae-based animal feed is expected to become a major trend in the animal feed industry in the next decade [174]. Microalgae are rich in amino acids and can be the lysine source for feed additives. Lysine is the most important amino acid additive in animal feed, especially for pigs in the livestock industry. The addition of lysine in feed can help increase the daily weight gain of pigs and the lean meat percentage of pork [175]. Therefore, the microalgae containing abundant protein is suitable for feed additives application. The protein extraction was increased by freeze-drying and milling the dry microalgal biomass along with alkaline extraction [176]. Furthermore, with the addition of microalgae in feed, the specific pigments of microalgae can render the healthy color of muscle tissue of livestock and poultry in line with the preferences of consumers [177]. Polysaccharides in microalgae, such as glucan (β-1,3-glucan), can enhance immunity, reduce animal pathogenesis and increase animal survival [178]. EPA, DHA, and antioxidants in microalgae can reduce the total cholesterol of animals and the oxidation rate of meat during storage [179]. Feed containing microalgae could increase the amount of boar sperm, the secretion of sow’s milk and the survival rate of piglets [180]. A DHA-rich microalga as a dietary supplement would increase the carcass traits and meat fatty acid profile in growing-finishing pigs [181]. Microalgal feed additives were also applied to laying hens due to an increase in egg production and egg weight [182]. Astaxanthin-rich microalgae were used for the feed of laying hens; it is expected not only to increase the color of the yolks but also to produce functional eggs rich in astaxanthin, which will have great economic benefits in the egg industry. The supplementation of laying hen diets with microalgae on fatty acid content could enhance the health lipid indices and oxidative stability of hens [183]. However, the application of microalgae to feed is likely to face the problem of insufficient supply. If this problem of insufficient supply can be overcome, unlimited opportunities for feed by microalgae can be expected.

3.8. Carotenoids of High-Value Products

The global carotenoid market was estimated to be valued at USD 1127.5 million in 2019 by a report from Markets and Markets, and was projected to reach USD 1168.7 million by 2026. Carotenoids are considered powerful antioxidants and vitamin A sources and are widely applied in food, feed, nutrient supplements, skincare products, and pharmaceutical products. The limited supply of animal- or plant-derived carotenoids has increased the development of carotenoids that are produced by microbial fermentation and that are chemically synthesized. Additionally, the use of microorganisms, such as microalgae, yeast, filamentous fungi, and bacteria to produce carotenoids, is the most promising alternative because agricultural waste can be used as a source of nutrients for microbial cultivation or fermentation to further reduce production costs. At present, the main commercial pigments of carotenoids are lutein, astaxanthin, carotene, canthaxanthin, lycopene, and zeaxanthin [184]. The main reason is that microalgae are a natural resource of carotenoids that are inexpensive and that they have a high growth rate compared with plants [17]. The growth rate is 5- to 10-fold faster than that of land-based plants and they can be harvested throughout the year without seasonal harvest problems [185]. A novel two-stage heterotrophic-mixotrophic (TSHM) cultivation strategy was applied to increase lutein production in the Chlorella strain. Maximum lutein production (6.17 mg g−1) and production (33.64 mg L−1) were obtained with the TSHM strategy, which is considered the best production model for microalgal lutein [186]. Xie et al. [187] performed a pilot-scale cultivation of Chlorella sorokiniana FZU60 with a mixotrophy/photoautotrophy two-stage strategy to produce microalgal lutein. The lutein content, production, and productivity reached 9.51 mg g−1, 33.55 mg L−1, and 4.67 mg L−1 d−1, respectively, which were greater than those reported in other pilot studies. Therefore, most studies have investigated an increase in carotenoids, including lutein, production by the fast-growing microalgal Chlorella (Table 5). In Table 5, one can see that China is also actively developing research on microalgae carotenoids, to produce high-value products, to achieve economic sustainability. The focus of research is on astaxanthin and lutein of carotenoids produced from microalgae, which are the same as the current market trends for commercial applications [188].

4. Refining Analyses to Reduce the Costs of Microalgae CO2 Capture and Utilization

Microalgal production and biorefinery is a sustainable process by integrating with wastewater and flue gas to achieve CO2 reduction, carbon recycling, and wastewater treatment. For evaluating the potential of microalgae CO2 capture and utilization (CCU) strategies, robust analyses are needed to answer whether the microalgae culture system and microalgae-based biofuels production (i.e., biorefinery processes) can be constructed and/or scale-up. Besides the economic issues, the analyses are addressed, regarding the benefits on environmental health and sustainability. Reasonable assumptions for various analyses, mostly including techno-economic assessments (TEAs) and life-cycle assessments (LCAs), identified existing data, refinery processes, and information gaps must be filled to answer the questions on economics, environmental health, and/or sustainability.

4.1. Techno-Economic Assessments (TEAs)

TEAs calculate the capital (or investment) and operating costs of a system to arrive at the total system costs and the price of the final products. The majority of TEAs have assumed the use of a microalgae system of an open pond or closed PBR production [196]. Standardization of these models helps to assess performance against the state of technology and determine natural scalability price breakpoints. To standardize these analyses, agreement on boundary conditions is needed, including return on investment, land values, financing costs, biomass cost limitations, and resource cost curves. TEAs first require detail information on microalgae production. The information majorly includes (1) cultivation yield and microalgal composition (e.g., microalgae growth and productivity, oil content for biodiesel production, and carbohydrate content for fermented ethanol production); (2) engineering detail on CO2 capture efficiencies; (3) data on microalgae harvesting and dewatering technologies; and (4) water, as well as nutrient recycling [197].
Microalgae biofuel production has been extensively evaluated through TEAs. Chen et al. [19] reviewed many papers published between 2010 and 2013, reporting on the costs of biodiesel production from microalgae, ranging from USD 2.52–85.36 gal−1. This difference can be explained by various factors, including microalgal strains, culture system and scale, economic environment, and consideration of carbon credits. For instance, high-value byproducts could produce better financial evaluation results, and carbon credits or tax credits could lead to higher revenue. The PBR system for microalgae culture requires a large investment in the construction. Therefore, it was revealed that unit biodiesel costs of PBRs were 2–10-fold of that of open ponds with the same biodiesel production capacity [19]. Recently, the research showed a decreased average cost of microalgae-based biofuel by TEAs. Wu et al. [198] indicate that the break-even prices of diesel and ethanol are estimated about USD 0.49 kg−1 and USD 2.61 kg−1, respectively, the internal rate of return (IRR) is close to 29.21%. The cost of microalgae biodiesel production in China was estimated at USD 2.29 kg−1, but it is still higher than that of commercial diesel [199]. Increasing the capacity of microalgal productivity and lipid content could efficiently reduce the cost of microalgal diesel production [200,201]. By a design process of wastewater-based microalgal biofuel production through hydrothermal liquefaction and hydroprocessing, the cost of biofuels could be USD 4.3 gasoline gallon equivalent−1 [202]. From the result of TEAs, an economically viable microalgal Chlorella vulgaris based biorefinery for paper industrial effluent treatment and bioenergy production in the scenario of 3% photosynthetic efficiency, 75% lipids extraction efficiency, and 45% anaerobic digestion efficiency, a EUR 15.4 million net present value (NPV) and 12% IRR were obtained [203].

4.2. Life-Cycle Assessments (LCAs)

LCAs are carried out based on system model and energy balances, and should include evaluations of water consumption, nutrient use, as well as environmental impacts. Comprehensive LCA boundaries should include the GHGs produced by the energy demands for CO2 capture as well as transport, biorefinery process, and microalgae cultivation. In fact, LCAs and TEAs have always emerged as critical tools for assessing the impact and feasibility of the systems of microalgae-based biofuel production [204]. The boundary for LCAs of microalgae CCU systems should include the production of CO2 through to the end products and should account for “recycle” systems. Additionally, water, fertilizer consumption, and land-use of biomass product should be calculated within LCAs to refine environmental impacts of microalgae-based biofuel production.
In effort to understand and explore opportunities to harmonize the variability, several studies have reviewed the methodologies and results of the published LCA studies on microalgae biofuels [204,205]. Collectively, these previous reviews of LCAs of algae-derived fuels have shown that the significant result variations are due to the inconsistency in (1) scope definition (e.g., system boundary and functional unit); (2) assumptions (e.g., using constant values versus random values from empirical distributions); (3) technological choices (e.g., different process trains); and (4) data sources. In the past, harmonization efforts were exerted on reducing the inconsistency on the scope definition [206]. For example, Menten et al. [205] applied meta-regression analysis to 47 LCA studies (from 2002 to 2011) and showed that the GHG emissions associated with producing 3G biofuels varied by region, with ranges of 41.6 to 136.2 g CO2-eq MJ−1 (mean = 88.9 g CO2-eq MJ−1). Quinn and Davids [204] conducted a resource assessment collected from 25 LCA studies (from 1982 to 2014) for the scalability of microalgae biofuels and found a range of −75 to 534 g CO2-eq MJ−1 for biofuel production. Could researchers use data of LCAs to design an optimizing process for algal biofuel production with lower GHG emissions? Recently, a new microalgae-to-biofuels chains for producing diesel and ethanol was simultaneously reported by LCAs, the life-cycle GHG emissions for producing diesel and ethanol are 39 g CO2-eq MJ−1 fatty acid methyl esters and 112 g CO2-eq MJ−1 ethanol, respectively [198]. It is verified that the process integration of the heat recovery scheme, the entrainer recovery tower, and CO2 recycling can effectively reduce life cycle GHG emissions of this assay. LCAs have been also used to evaluate using microalgal oil and carbohydrate as feedstock to produce biofuel, butanol. The results revealed that the annual ReCiPe endpoint score of producing 1 kg biobutanol is lower than that of 1 kg biodiesel by 54.4%. It is indicated that microalgae-to-butanol chain is more ecofriendly than the microalgae-to-diesel chain due to lower LCA impacts [207]. Life cycle assessment of bioreactor for biodiesel production from microalgae revealed a fossil energy requirement variation between 3.6 and 5.7 MJ kg−1, a GHG emission of 0.85–1.46 kg CO2-eq kg−1 biodiesel, and a reduction in fossil energy requirement of approximately 87.3% in the pilot substrate-based microalgal bioreactor [208]. The net CO2 balance was −26 t d−1 in the scenario with highest photosynthetic efficiency and higher biomass productivity. That means that there is more consumption of CO2 by microalgae than that released in the biorefinery processes [203].

5. Current Carbon Fixation and Microalga-Based Biorefinery Research

The U.S. Department of Energy (DOE) established the Office of Energy Efficiency and Renewable Energy (EERE), which supports Research and Development (R&D) on alternative fuels in 1993. Within EERE, the Bioenergy Technologies Office (BETO) initiated a multi-year program plan (MYPP, 2016–2020) describing many specific challenges to overcome and goals to complete in order to increase the percentage of fuel in the U.S. coming from biological sources. One of the key components of the MYPP portfolio is “R&D on productive and competitive advanced algal systems”. BETO organized an Algae program dedicated to researching and improving the viability of microalgae as an energy source and byproducts. The aim of MYPP on algal R&D is to demonstrate at non-integrated process development unit-scale algae yield of 3700 gallons or equivalent biofuel intermediate per acre per year by 2020. For a longer-term goal—to demonstrate an unit-scale algal productivity of greater than 5000 gallons biofuel per acre per year by 2025, and to validate production of 5 billion gallons per year of reliable and sustainable algae-based biofuels at the cost of $3.00 gasoline gallon equivalent (GGE)−1 by 2030. In 2021, DOE announces USD 8 million for projects to develop algae-based co2 utilization technology that convert CO2 must show a net decrease in CO2 emissions through life cycle analysis, display a potential to generate a marketable product and show that the product displays beneficial aspects when compared to commercially available products produced with existing state-of-the-art technology.
Carbon fixation and microalga-based biorefinery research have also rapidly developed in Europe, and the European Union (EU) has supported many projects addressed on microalgal biofuels and its high value byproducts [209]. FUture European League 4 Microalgal Energy (FUEL4ME) was a four-year project funded by the EU, which aimed to develop a sustainable, scalable process for biofuels and byproducts from microalgae. The 4-year, EUR 15 million SCALE program, led by Microphyt, brings together 11 top-tier international partners on a mission to develop the world’s largest microalgae biorefinery. The flagship grant of SCALE is from the Bio-based Industries Joint Undertaking (BBIJU), a partnership of the European Commission and the Bio-based Industries Consortium. SCALE will further accelerate these environmental benefits by integrating renewable energy production, enhancing recycling capabilities, aiding the attainment of European climate targets, i.e., of cutting GHG emissions by 20%. Moreover, the production capacity will first fully integrated increase five-fold, allowing for the development and production of more than 15 new ingredients derived from microalgae for the fields of nutrition and cosmetics. The annual capacity of SCALE will be more than 100 tons of high-value ingredients.

6. Limitations and Needs of CO2 Fixation by Microalgal Cultivation

Overall, 3G microalgae-based biofuel is seen as a promising energy source. Despite the many advantages of developing renewable energy and high-value byproducts, it is still difficult to form an optimizing and profitable industry for microalgal carbon fixation and refineries. The greatest limitation of microalgae biofuel production is that it is still far too expensive for commercial viability. In addition to cost limitations, current restrictions in large-scale outdoor microalgal cultivation include (1) a high-efficiency microalgae culture system with a high cost of manufacturing, especially outdoor PBR systems; (2) the illumination area and photoperiod of the microalgae culture system; (3) tolerance to changes in the external environment, such as temperature and light; (4) the possibility of contamination from microorganisms and insects in a large-scale culture system; (5) the concentration, source, composition, feed rate, and transmission method of CO2; (6) an effective increase in microalgal biomass production and the contents of microalgal oil/high value products; (7) more energy consumption of the refinery procession of microalgal biomass; and (8) biosafety risk and governmental policy issues if microalgal biomass produced from wastewater and flue gas aeration is used to generate animal feed and food additives. Each of the above restrictions may be (or has been) resolved in individual studies, but establishing a process of microalgal carbon fixation that can overcome all problems comprehensively is still a difficult task. For example, wastewater utilization and flue gas aeration could help to significantly reduce the cultural costs of microalgal cultivation [42,210,211]. The production of microalgal biofuels integrated with other valuable byproducts from microalgal biomass could be a feasible way to reduce the biofuel cost from microalgae [19,212]. However, it is easy to limit the development of high-value byproducts for microalgal biomass due to biosafety considerations [49]. In addition, following microalgal cultivation, microalgae biomass recovery and dewatering processes not only increase costs, but also may increase carbon emissions by energy consumption [213,214]. Therefore, how to balance the conditions of CO2 fixation, renewable energy production, energy consumption, economic feasibility, and environmental health in microalgal cultivations and microalgal biomass refineries, to achieve net zero carbon emissions and economic profits, are global research goals.
Regarding cost limitations, it is necessary to establish a low-cost process for mass production from microalgae [44,209]. At this time, the industry is still experimenting on a variety of methods to culture microalgae, with the most popular models being open pond systems and/or closed-loop systems, i.e., PBRs [215]. Regardless, both systems are still unaccepted because of economic issues. PBRs provide the most effective systems for producing high-quality microalgae, but they are expensive in light of operations and maintenance. Therefore, PBRs are not economically accepted as a system of microalgae culture for commercial production. Moreover, more funding and research are necessary to approve the potential for microalgae biofuel in commercially viable products. Although many biorefinery technologies are moving out of the laboratory and into commercial-scale production, the production costs of microalgae-based biofuel is still high; in particular, the costs at the beginning to scale-up, need to be resolved, and novel technology is new and still developing [216,217]. Furthermore, the Conference of the Parties (COP) 26 was held in 2021, with the aim of making all countries committed to achieving net zero carbon emissions, and even more, expressing that there is no time to delay in the development of carbon reduction technologies. That is—microalgae-based biofuels are promising energy sources to be developed.

7. Future Direction of Research

As global warming is becoming more serious—how to effectively reduce CO2 is still an important issue. Therefore, research on the development of sustainable microalgae biological carbon fixation technology needs to continue. Future research directions should focus on the potential for long-term stable growth of microalgal strains and applicable large-scale microalgae cultivation systems under outdoor cultivation, which can use CO2 from exhaust gas or utilize the nutrients from wastewater. The potential microalgal strain will not cause damage to the surrounding environmental ecosystem. Coupled with global climate change challenges—researchers should focus on how to make the microalgal strains withstand changes in the surrounding environment during the cultivation process to continuously achieve CO2 carbon fixation. Under the premise of a low-cost harvesting process, the harvesting microalgae biomass will be fully utilized to develop biofuels, fine chemicals, and high-value products. The overall process involves “checking” the economic sustainability and environmental sustainability, to achieve a net positive energy balance and net zero carbon emissions (even to net negative carbon emissions).

8. Conclusions

Microalgae-based CO2 fixation technology is certainly promising. Compared with applying microalgae cultivation to CO2 fixation alone, which is unlikely to be economically attractive, there is an opportunity to reduce costs and simultaneously achieve CO2 reduction and wastewater treatment by integrating wastewater and flue gas in microalgae cultivation. The resulting microalgal biomass can also be a feedstock for biodiesel, biobutanol, biogas, aviation fuels, and biochar, lactic acid, and succinic acid of fine chemicals, feed additives, and carotenoids of high-value byproducts, to apply in cosmetics, food, and nutrient supplements. However, to balance the conditions of CO2 fixation, renewable energy production, energy consumption, economic feasibility, and environmental sustainability in microalgal cultivation and microalgal biomass refineries, to achieve net zero carbon emissions, and economic profit, are still global research goals. In summary, screening higher CO2 fixation efficiency of microalgal strains, establishing large-scale microalgal cultivation systems, and long-term stable processes for outdoor cultivation, harvesting the resulting microalgal biomass by low-cost harvesting processes, and developing biorefinery processes, evaluating the economic and environment assessment of microalgal CO2 fixation technology, need to be studied further. All countries should simultaneously pay attention to the environmental disasters caused by carbon emissions, and take action to improve it.

Author Contributions

Conceptualization, C.-M.K., Y.-L.S., H.-T.W. and C.-S.L.; writing—original draft preparation, C.-M.K., Y.-L.S., C.-H.L. (Cheng-Han Lin) and C.-H.L. (Chao-Hsu Lin); writing—review and editing, C.-M.K., Y.-L.S., H.-T.W. and C.-S.L.; supervision, C.-S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

All data in this study were obtained from published material in scientific journals, referenced in the paper, and can be obtained by any individual with access.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Acknowledgments

This work was supported by grants MOST 110-2313-B-A49-001-MY3 and MOST 107-2313-B-009-002-MY3 from the Ministry of Science and Technology (MOST), Taiwan. This work was also financially supported by the “Center for Intelligent Drug Systems and Smart Bio-devices (IDS2B)” from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project of the National Yang Ming Chiao Tung University and Ministry of Education (MOE), Taiwan.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

3Gthird-generation
ABEacetone-butanol-ethanol
APACAsia Pacific Accreditation Cooperation
AUAustralia
BBIJUBio-based Industries Joint Undertaking
BETOBioenergy Technologies Office
BRBrazil
CAGRcompound annual growth rate
CCUCO2 capture and utilization
CH4methane
CNChina
CO2carbon dioxide
CO32−carbonate
CODchemical oxygen demand
COPConference of the Parties
DHAdocosahexaenoic acid
DIETdirect interspecies electron transfer
DOEDepartment of Energy
EEREEnergy Efficiency and Renewable Energy
EPAeicosapentaenoic acid
ESSpain
EUEuropean Union
Fe3O4ferroferric oxide
FIFinland
FUEL4MEFUture European League 4 Microalgal Energy
GBUnited Kingdom
GGEgasoline gallon equivalent
GHGsgreenhouse gases
HCO3bicarbonate
HKHong Kong
H2Shydrogen sulfide
HSO3bisulfite
IBAindole-3-butyric acid
INIndia
IRRinternal rate of return
ITItaly
KRKorea
LCAslife cycle assessments
LEDlight-emitting diode
MXMexico
MYMalaysia
MYPPMulti-Year Program Plan
N2nitrogen
NaNO3sodium nitrate
NH3ammonia
NLNetherlands
NOxnitrogen oxides
NOAANational Oceanic and Atmospheric Administration
NPVnet present value
NTGN-methyl-N-nitro-N-nitrosoguanidine
PBRsphotobioreactors
PLPoland
POMEPalm oil mill effluent
PsRCPBRs/raceway circulating
R&DResearch and Development
RubiscoRibulose-1,5-bisphosphate carboxylase/oxygenase
SCFAsshort-chain fatty acids
SO2sulfur dioxide
SO32−sulfite
SO42−sulfate
SOxsulfur oxides
TEAstechnical and economic assessments
TNtotal nitrogen
TPtotal phosphorus
TSHMtwo-stage heterotrophic-mixotrophic
TWTaiwan
USUnited States
ZASouth Africa

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Figure 1. Microalgae-based carbon dioxide biofixation and biorefinery.
Figure 1. Microalgae-based carbon dioxide biofixation and biorefinery.
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Figure 2. Biorefinery application of microalgal biomass on biofuels and high-value byproducts production.
Figure 2. Biorefinery application of microalgal biomass on biofuels and high-value byproducts production.
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Table 1. Growth performance and CO2 fixation efficiency of microalgal Chlorella with different tolerant characteristics.
Table 1. Growth performance and CO2 fixation efficiency of microalgal Chlorella with different tolerant characteristics.
Tolerance CharacteristicsMicroalgaeGas AerationTemp. (°C)Maximum Biomass Conc. (g L−1)Biomass Productivity
(g L−1 d−1)
CO2 Fixation Efficiency 1 (g L−1 d−1)Country 2References
High-CO2 tolerantChlorella sp. MTF-15Flue gas 4262.520.5150.942TW[48]
Chlorella sp. AE2010% CO2283.220.2930.536CN[59]
20% CO23.130.2850.522
30% CO23.020.2750.503
Chlorella vulgaris NIOCCV5% CO2280.6740.1110.203IN[60]
10% CO21.580.2650.485
20% CO20.9760.1630.298
High-CO2 and CH4 tolerantChlorella sp. MB-920% CO2 and 80% CH4262.350.2430.445TW[61]
CO2 tolerantChlorella sp. GDBoiler flue gas 3266.540.8921.632TW[49]
High-CO2 tolerantChlorella sp. LAMB 3140% CO226~0.90.0790.144CN[15]
High-CO2 and thermotolerantChlorella vulgaris ESP-31, 283 and 359Simulated flue gas (25% CO2, 80–90 ppm SO2, 90–100 ppm NO)401.91 (283)/1.99 (359)0.73 (283)/0.89 (359)1.336 (283)/1.629 (359)TW[58]
Alkali-tolerant
(pH 6–10)
Chlorella sp. AT110% CO2265.081.0101.848TW[62]
Alkali-tolerant (pH > 10)Chlorella sorokiniana
SLA-04
Air200.90.0590.108US[51]
Air20–250.740.0460.078[52]
ThermotolerantChlorella pyrenoidosa M18Air374.650.9311.702IN[54]
Chlorella pyrenoidosa M244.110.8221.504
Chlorella sp. M46% CO2404.21.051.922TW[55]
Chlorella pyrenoidosa M18Air451.690.3380.619IN[57]
Chlorella sorokiniana10% CO2371.160.2320.425IN[56]
15% CO21.050.2110.384
5% CO2 and 80 ppm NO1.270.2540.465
1 CO2 fixation efficiency (g L−1 d−1) was calculated by 1.83-fold of biomass productivity. 2 Country abbreviation: Taiwan (TW), China (CN), and India (IN). 3,4 Concentration of CO2 in the flue gas and boiler gas was 25% and 8%, respectively.
Table 2. Growth, CO2 fixation efficiency, and lipid productivity of the microalgae Chlorella cultures using flue gas.
Table 2. Growth, CO2 fixation efficiency, and lipid productivity of the microalgae Chlorella cultures using flue gas.
MicroalgaeFlue Gas SourceCO2 (%)Biomass Productivity (g L−1 d−1)CO2 Fixation Efficiency 1 (g L−1 d−1)Lipid (%)Lipid Productivity 2 (g L−1 d−1)Country 3References
Chlorella sp. MTF-15Coke oven130.5280.96621.50.614TW[48]
250.5150.94226.40.666
Hot stove130.4490.82233.80.866
260.3140.57535.20.591
Power plant120.4230.77436.30.792
240.3420.62641.60.633
Chlorella sorokinianaIndustrial flue gas160.2310.42321.10.049IN[65]
Chlorella sp. KR-1Coal-fired flue gas130.5611.02729.90.168KR[66]
Chlorella sp.Coal burning50.2730.5008.690.024IN[70]
Chlorella fusca LEB 111Coal power plant100.1110.20315.50.017BR[67]
Chlorella vulgarisCoal burning boiler60.3120.57123.20.074IN[71]
Chlorella sp. GDBoiler flue gas81.2962.37221.70.214TW[49]
Chlorella sp.Flue gas300.1450.26524.70.036ZA[40]
Chlorella sp. CvSimulated flue gas150.530.969NDNDCN[64]
Chlorella vulgarisPower plant120.5020.91940.10.201ES[68]
Chlorella sp. C2Power plant30.3140.57531.50.099CN[41]
1 CO2 fixation efficiency (g L−1 d−1) was calculated by 1.83-fold of biomass productivity. 2 Lipid productivity (g L−1 d−1) = (biomass productivity × lipid content)/100. 3 Country abbreviation: Taiwan (TW), India (IN), Korea (KR), Brazil (BR), South Africa (ZA), China (CN), Spain (ES).
Table 4. Biomass productivity and CO2 fixation efficiency of microalgae Chlorella in different cultivation systems.
Table 4. Biomass productivity and CO2 fixation efficiency of microalgae Chlorella in different cultivation systems.
MicroalgaeCultivation SystemCultivation Scale (L)CO2 (%)Maximum Biomass Conc. (g L1)Biomass Productivity (g L1 d1)CO2 Fixation Efficiency 1 (g L1 d1)Country 2References
Chlorella sp. MTF-15Column-type PBR112.5 (1/2 flue gas)2.8550.5280.966TW[48]
12001.5550.1970.361
Chlorella vulgarisPorous air-lift PBR160.03 (air)0.0950.0040.174HK[120]
Loop air-lift PBR0.1260.0070.231
Bubbling PBR0.7830.0541.433
Chlorella sp. GDColumn-type PBR124.8130.8701.592TW[25]
8 (boiler flue gas)4.9211.2962.333[49]
Chlorella vulgarisPlastic bottle1543.1510.3780.711PL[121]
Chlorella vulgarisFlat-plate PBR1.652.3030.5511.008CN[95]
Chlorella vulgarisBubble column PBR560.03 (air)0.9620.0430.079MY[122]
Chlorella pyrenoidosaOpen raceway pond800099.50.9270.1140.214CN[119]
Chlorella vulgarisCoiled tubular tree PBR1.20.03 (air)0.5520.0840.153CA[123]
Chlorella sorokinianaFlat panel PBR9051.9130.0910.167US[124]
Chlorella vulgarisPilot-scale PBR150Without aeration2.2110.1980.362CN[125]
Chlorella sp. AT1Column-type PBR1107.3721.0111.851TW[62]
PBRs/Raceway circulating system28822.5610.3210.588TW[24]
5281.9630.2370.434
10081.0520.1070.195
36001.6860.1500.275
66001.2570.1090.199
Chlorella sp. HS2Flat panel PBR213.8110.5431.021KR[126]
Chlorella vulgaris UTEX 26Raceway11000.03 (air)0.2520–26 (g m2 d1 for 65 days culture)-MX[111]
Chlorella pyrenoidosa PY-ZU1Pond-tubular hybrid PBR<5 (a model system)152.30.7701.409CN[117]
Chlorella vulgarisRaceway with computational fluid dynamics2050 (mix with air and pure CO2 gas)5.211.89 (g m2 d1, 14 cm depth of raceway)-TW[112]
Chlorella vulgaris CCAP 211/11BMembrane photobioreactor40151.010.1660.704IT[118]
1 CO2 fixation efficiency (g L−1 d−1) was calculated by 1.83-fold of biomass productivity. 2 Country abbreviation: Taiwan (TW), Hong Kong (HK), Poland (PL), China (CN), Malaysia (MY), USA (US), Korea (KR), Mexico (MX), Italy (IT). -: Data not shown.
Table 5. Carotenoids production from microalgal Chlorella.
Table 5. Carotenoids production from microalgal Chlorella.
MicroalgaeOperating ConditionsBiomass Productivity (g L1 d1)CarotenoidsCarotenoid Content (mg g1 DAB 1)Country 2References
Chlorella zofingiensisNitrogen deficiency with diphenylamine addition0.363Astaxanthin0.778NL[187]
Canthaxanthin0.405
Chlorella saccharophilaOptimization extraction by ultrasonication-β-carotene4.982AU[189]
Zeaxanthin11.21
Chlorella zofingiensisSemi-continuous operation1.041Astaxanthin3.213CN[190]
Chlorella protothecoidesSalt and light stress0.161Astaxanthin0.131BR[191]
β-carotene0.094
Lutein/Zeaxanthin1.236
Chlorella zofingiensisHigh light irradiation and nitrogen deficiency with glucose-feeding7.031Astaxanthin0.745CN[192]
Chlorella zofingiensis CZ-bkt1High light irradiation and nitrogen deficiency0.301β-carotene5.022CN[193]
Lutein13.81
Zeaxanthin7.013
Chlorella zofingiensisNitrogen deficiency0.142Astaxanthin3.912CN[194]
Chlorella sorokiniana MB-1-M12Mixotrophic semi-continuous operation3.9Lutein5.19TW[33]
Chlorella sorokiniana MB-1-M12Two-stage alternative cultivation strategies1.42–3.54Lutein6.17TW[195]
Chlorella sorokiniana FZU60Mixotrophy/photoautotrophy two-stage strategy33.55Lutein9.51CN[186]
1 DAB indicates dry algal biomass. 2 Country abbreviation: Netherlands (NL), Australia (AU), China (CN), Brazil (BR), Taiwan (TW). -: Data not shown.
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Kuo, C.-M.; Sun, Y.-L.; Lin, C.-H.; Lin, C.-H.; Wu, H.-T.; Lin, C.-S. Cultivation and Biorefinery of Microalgae (Chlorella sp.) for Producing Biofuels and Other Byproducts: A Review. Sustainability 2021, 13, 13480. https://0-doi-org.brum.beds.ac.uk/10.3390/su132313480

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Kuo C-M, Sun Y-L, Lin C-H, Lin C-H, Wu H-T, Lin C-S. Cultivation and Biorefinery of Microalgae (Chlorella sp.) for Producing Biofuels and Other Byproducts: A Review. Sustainability. 2021; 13(23):13480. https://0-doi-org.brum.beds.ac.uk/10.3390/su132313480

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Kuo, Chiu-Mei, Yu-Ling Sun, Cheng-Han Lin, Chao-Hsu Lin, Hsi-Tien Wu, and Chih-Sheng Lin. 2021. "Cultivation and Biorefinery of Microalgae (Chlorella sp.) for Producing Biofuels and Other Byproducts: A Review" Sustainability 13, no. 23: 13480. https://0-doi-org.brum.beds.ac.uk/10.3390/su132313480

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