Advancement of Abiotic Stresses for Microalgal Lipid Production: History
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Subjects: Biology
Contributor:
Rahul Prasad Singh
,
Priya Yadav
,
Indrajeet Kumar
,
Manoj Kumar Solanki
,
Rajib Roychowdhury
,
Ajay Kumar
,
Rajan Kumar Gupta

The world is currently facing global energy crises and escalating environmental pollution, which are caused by the extensive exploitation of conventional energy sources. The limited availability of conventional energy sources has opened the door to the search for alternative energy sources. In this regard, microalgae have emerged as a promising substitute for conventional energy sources due to their high photosynthetic rate, high carbohydrate and lipid content, efficient CO2 fixation capacity, and ability to thrive in adverse environments. The research and development of microalgal-based biofuel as a clean and sustainable alternative energy source has been ongoing for many years, but it has not yet been widely adopted commercially. However, it is currently gaining greater attention due to the integrated biorefinery concept. This study provides an in-depth review of recent advances in microalgae cultivation techniques and explores methods for increasing lipid production by manipulating environmental factors. Furthermore, our discussions have covered high lipid content microalgal species, harvesting methods, biorefinery concepts, process optimizing software tools, and the accumulation of triglycerides in lipid droplets. The study additionally explores the influence of abiotic stresses on the response of biosynthetic genes involved in lipid synthesis and metabolism. In conclusion, algae-based biofuels offer a viable alternative to traditional fuels for meeting the growing demand for energy.

  • microalgae
  • cultivation systems
  • biomass
  • environmental stresses
  • biorefinery
  • biofuels

1. Introduction

The increasing concerns about energy security and climate change caused by traditional energy sources are driving the world to explore renewable and sustainable energy resources. The reduction in non-renewable fossil fuel resources and the escalating impact of global warming have led many countries to prioritize these issues [1][2][3]. To mitigate the future crisis of traditional fuels and their adverse consequences on the environment, the research community is continuously working to explore an alternative to fossil fuels that may be economical, non-toxic, renewable, and eco-friendly [4][5][6]. Among the many solutions to the global energy crisis, the use of algal biofuels as an alternative energy source is a potential strategy to meet our energy needs. Algal biofuels are renewable and viable energy sources that can contribute to the future global energy infrastructure. They offer several benefits, such as reduced dependence on foreign oil and low CO2 emissions [2][3].
Initially, first-generation biofuels obtained from edible plant biomass, including barley, beet, corn, potato, sugarcane, vegetable oils, and wheat were used as a replacement for fossil fuels and showed effectiveness in reducing CO2 emissions in the atmosphere. However, the use of these first-generation biofuel sources raised concerns about potential food shortages and conflicts between food and fuel production. To address this issue, second-generation biofuels were developed using non-edible feedstocks, such as agricultural waste, wood residuals, and bioenergy crops. The carbon emissions associated with second-generation biofuels can be either neutral or negative. However, a drawback of these fuels is their dependence on the seasonal availability of raw materials. Algae have been categorized as third-generation biofuels, presenting a viable and advantageous alternative for biofuel production. They overcome the limitations of the previous generations and are also considered to be 10 times more efficient than second-generation biofuels [7][8]. Algal biomass cultivation can be achieved through three main methods: autotrophic, mixotrophic, and heterotrophic. Algae have a significantly higher growth rate than traditional fodder crops, and they contain approximately 30 times more oil content than conventional feedstocks. The lipid content of microalgae ranges between 20 and 60% of the total biomass, depending on the specific strain and the conditions under which they are cultivated [9][10][11]. The generation of algal biofuel involves the following steps: large-scale cultivation of algae, harvesting and biomass drying, lipid extraction, and the chemical conversion of extracted lipids into biofuel. 
Currently, various renewable energy sources are being utilized. Biofuels derived from microalgal biomass are considered to be economically viable and eco-friendly, making them a promising choice for the next generation of biofuels [12]. Recent research conducted by [13], examined the potential of microalgal biomass as a zero-emission fuel, considering its distinctive phytochemical characteristics. The rate and quantity of metabolite formation in microalgae are affected by cultivation systems and growth conditions. Microalgae are grown in unregulated ponds and tanks in an open-air pond system with natural lighting [14]. Unregulated growth conditions in microalgae cultivation provide economic advantages and cost-effectiveness, but they are susceptible to contamination and exhibit variable yields [15]. In contrast, closed culture systems and bioreactor-based cultivation provide a controlled growth environment, ensuring optimal output [16].
Microalgae synthesize a diverse range of chemicals in response to environmental stress, in order to adapt to harsh environmental conditions [17][18][19]. Furthermore, many factors including CO2 concentration, nitrogen and phosphorus starvation, light intensity, temperature, pH, heavy metals, and salinity could improve microalgal lipid content [20][21]. The physical characteristics of the medium, such as light, temperature, and nutrient supplementation, influence not only the strain’s metabolic machinery but also the composition and yield of microalgal lipids [22]. In contrast, choosing the right microalgal species, optimizing cultivation conditions, and factors affecting microalgal lipid content are the primary requirements for optimum biofuel production. The accumulation of lipids and lipid content can be changed by changing the growth conditions [23]. Therefore, researchers are focusing on abiotic factors to improve microalgal biomass and lipid content. However, there is still a need to develop new methodologies and techniques for the efficient production of biofuels from microalgal resources.
Microalgae store substantial amounts of neutral lipids, mainly triglycerides (TAGs), which are ideal for biodiesel production. Microalgal biorefineries not only have the potential to be a profitable approach for biofuel production, but they also have the ability to produce useful products of commercial value. In addition, microalgae-based biofuels address issues related to rising energy or fuel prices and contribute to CO2 mitigation [24][25]. Microalgae, such as Chlorella vulgaris, Scenedesmus sp., Monoraphidium sp., Isochrysis galbana, Tetraselmis suecica, Nanochloropsis occulata, Botryococcus braunii, Dunaliella tricolecta, and Neochloris are widely distributed in the environment and used as a source of food, medicine, and biofuels [26]. The production of biofuels using microalgae faces several challenges, including strain selection, mass cultivation, harvesting, drying, extraction, and transfer processes [27][28]。

2. Microalgal Species and Biorefinery for Sustainable Biofuel Feedstock

Microalgae are photoautotrophs with the capability to survive in freshwater and marine ecosystems. Currently, it is estimated that approximately 200,000 to 800,000 microalgal species are present on the earth, of which only 50,000 have been identified and characterized [29]. The lipid content of microalgae is an important factor in the selection and screening of microalgae for biofuel production [30]. Microalgae consume CO2 and fix it into carbohydrates, proteins, and lipids under different environmental conditions, playing an essential role in the production of a variety of renewable fuels [31][32].
Previous research has indicated that numerous algal species, including Chlorella vulgaris, Chlorella emersonii, Chlamydomonas reinhardtii, Nannochloropsis salina, Skeletonema sp., and Parachlorella kessleri, have significant lipid content [33][34][35][36][37]. However, some species, such as Chlorella pyrenoidosa, Chlorella zofingiensis, Chaetoceros muelleri, Coelastrella sp., and Chlorococcum pamirum, have relatively modest lipid content [38][39][40][41][42]. When considering the lipid content in various algal groups, a general trend can be observed: green algae > yellow-green algae > red algae > blue-green algae. Similarly, when examining lipid productivity, the trend follows: green algae > red algae [43]. Figure 1 shows different microalgal species with high lipid content that hold promise for potential biofuel production.
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Figure 1. Some important microalgal species known for their high lipid content, which can be utilized for various types of biofuel production: (A) Chlorella sp., (B) Scenedesmus sp., (C) Chlorococcum sp., (D) Tetraselmis sp., (E) Botryococcus sp., (F) Desmodesmus sp., (G) Nannochloropsis sp., (H) Monoraphidium sp., and (I) Dunaliella sp.
Microalgae are a group of microscopic organisms that have the potential for CO2 sequestration and the ability to thrive in harsh environments [44][45]. However, due to their high photosynthetic nature, CO2 mitigation capabilities, and excessive biomass generation, microalgae can be exploited for various applications in environmental management and bioenergy [15][17][46][47]. Microalgae are rich in carbohydrates, proteins, fatty acids, and other bioactive compounds, which make them valuable feedstocks for various industrial applications, including cosmetics, nutraceuticals, livestock feed, fertilizers, and biofuels [4][48]. 

3. Microalgae Cultivation Systems

For an efficient industrial process, microalgae cultivation technology needs to be economically viable, environmentally friendly, and have a high yield [24]. Although photoautotrophic and heterotrophic growth conditions are the most common, some algal groups can also grow under mixotrophic conditions [49]. Several techniques for microalgal cultivation have been reported, including open, closed, and advanced systems. The choice of cultivation method for microalgae depends on the type of species, the nutrient source, and the end application of the biomass [18]. Other parameters, such as photobioreactor design, volume mixing, temperature, lighting, and CO2 supplementation, also play a significant role in flue gas reduction from the environment and nutrient recovery from wastewater [17]. Microalgal cultivation systems can be categorized into four main groups, each with its own advantages and disadvantages (Table 1).
Table 1. Various modes of microalgae cultivation with their advantages and disadvantages.
Cultivation Mode Carbon Source Energy Supply Light Availability Advantages Disadvantages
Autotrophic Inorganic carbon Light Obligatory Low cost, low energy consumption, high pigments production. Low growth rate and biomass, specific photobioreactor required.
Heterotrophic Organic carbon Organic No requirement High biomass productivity and lipid accumulation due to high growth rate, process of scaling up is simplified, organic substrates can be used to alter biomass composition. Higher cost, easy to be contaminated by other
microorganisms, only a few microalgal species that can grow in a heterotrophic environment, inability to synthesize metabolites triggered by light.
Mixotrophic Inorganic
and
organic carbon		 Light
and
organic
carbon		 No obligatory Increased growth rate, biomass, density and lipid accumulation, extended phase of exponential growth, stopping the photoinhibition effect and reducing biomass loss due to respiration during the dark hours, switch between photoautotroph and heterotroph regimens at any time. High cost, contamination problems, limited microalgae species will grow.
Algal turf scrubber Organic and inorganic
carbon		 Light
and
organic
carbon		 Obligatory Improved nutrient status, pollutant removal, high biomass productivity rate, easy harvesting and low maintaince, decreased the overall production cost Requirement of sufficient space and infrastructure

4. Microalgae Harvesting Techniques

Microalgae harvesting is the process of collecting microalgae from the liquid medium in which they are grown. The choice of microalgae harvesting method depends on a number of factors, including the properties of the microalgae, the desired properties of the end product, and the feasibility of recycling the growth medium. Microalgae cells can be harvested using biological, chemical, mechanical, or electrical methods. Microalgae harvesting is a time-consuming and challenging process that often requires the use of advanced chemical or mechanical techniques. Flocculation, filtration, flotation, sonication, centrifugation, and precipitation are some of the methods that are used to harvest microalgal biomass (Table 2). When choosing a harvesting method, it is important to consider the downstream processing requirements, as microalgal biomass will need to be processed further. Therefore, these processes must be carefully operated to avoid damaging or contaminating the microalgal biomass. It is also ideal if the chosen harvesting method permits the culture medium to be recycled [50]. Often, a combination of two or more harvesting methods is used to achieve greater separation efficiency and minimize costs [51].
Table 2. A comparison of the principles, benefits, and drawbacks of various algal harvesting methods, adapted from [52].
Technique with Image Principle Advantages Disadvantages
Flocculation
Sustainability 15 13678 i001		 Aggregation of cells is achieved by enlarging their size through the addition of a flocculant, which can be in the form of chemicals (such as ferric chloride, ferric sulfate, and ammonium sulfate) or microbes (bacteria). Fast and easy technique, used for large scale, less cell damage, applied to a wide variety of species, less energy requirements. Chemicals may be expensive, high pH required, separating the coagulant from harvested biomass is difficult, limited culture medium recycling, increased microbial
contamination.
Filtration
Sustainability 15 13678 i002		 Large cells (size > 70 µm) can be filtered under pressure or suction whereas smaller cells (size < 30 µm require ultrafilters to be harvested. High recovery efficiency, cost effective, no chemical required, low energy consumption, low shear stress. Slow hence requires pressure or vacuum, not effective for small algae, membrane fouling/clogging and replacement increases
operational and maintenance costs.
Flotation
Sustainability 15 13678 i003		 Trapping algal cells by bubbling air. Well-suited for large-scale applications, economically efficient with minimal space demands, short operation time. Depends on bubble distribution into the suspension, needs surfactants.
Centrifugation
Sustainability 15 13678 i004		 Sedimentation based on the velocity, cell size and density. Fast and effective technique, high recovery efficiency (>90), applicable to all microalgae. Expensive technique with high energy requirement, high operation and maintenance costs, risk of cell destruction.
Precipitation
Sustainability 15 13678 i005		 Certain algae undergo self-precipitation, they settle at the bottom when circulation is halted. No energy or chemicals are needed, it occurs naturally. Species-specific, time periods vary depending on the species, not every species is self-precipitated.

5. Approaches to Stimulate Lipid Production through Abiotic Stresses

5.1. Effect of Carbon Dioxide

Microalgae can mitigate CO2 emissions by CO2 biofixing and can grow well in high CO2 concentrations [20]. The growth rate and lipid content of microalgae can be affected by the concentration of carbon dioxide. Many studies have investigated the effects of CO2 on the growth and fatty acid composition of microalgal strains. The mechanism involves the uptake of CO2 by algae and converting the captured carbon into lipids. The carbon from microalgae is then converted into biodiesel through transesterification, as shown in Figure 2.
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Figure 2. Mechanism of CO2 sequestration by algae and their conversion into triglycerides to biodiesel. Carbonic anhydrase (CA), ribulose 1,5–bisphosphate (RuBP), ribulose bisphosphate carboxylase/oxygenase (Rubisco), glyceraldehyde 3–phosphate (G–3–P), acetyl–CoA (A–CoA), endoplasmic reticulum (ER), phosphatidic acid (PA), and triglycerides (TAG).
Increasing the CO2 levels in the growth medium of microalgae leads to an increase in the production of cellular lipids and fatty acids [53]. A study found that increasing the CO2 levels from 0.5% to 1% increased lipid production in C. vulgaris, but higher levels of CO2 significantly decreased lipid content in other microalgae species [54]. Various organic carbon sources, such as glucose, fructose, sucrose, and glycerol can be used to cultivate Chlorella strains [55]. When the cellular growth requirements are met and excess organic carbon is present, it promotes lipid accumulation. In addition, the addition of CO2 can increase the growth and lipid production of Chlorella sp., making them a promising candidate for industrial applications, especially due to their high polyunsaturated fatty acids (PUFAs) content [56]. The lipid content of C. vulgaris, Botryococcus braunii, and B. terribilis ranges from 2.5 to 20.0% under varying CO2 concentrations. In C. vulgaris, CO2 addition enhances the palmitic acid, while for Botryococcus sp., no such type of change occurs [57].

5.2. Effect of Nitrogen Starvation

Nitrogen is a crucial macronutrient that directly contributes to the synthesis of proteins, carbohydrates and lipids. Microalgae can acquire nitrogen from sources such as nitrates, nitrites, urea, and ammonium [58]. Nitrogen is an essential nutrient that plays a critical role in the growth of microalgae. When algae experience nitrogen limitation, they downregulate the synthesis of many proteins that are involved in various cellular functions. The downregulation of protein synthesis in nitrogen-limited algae conserves energy and allows the algae to allocate more resources to lipid synthesis. For example, a study found that Scenedesmus quadricauda has a 2.27-fold increase in lipid synthesis when exposed to nitrogen stress [59]. Under nitrogen-starved conditions, the carbon flux within the cells is redirected towards lipogenesis instead of proteins and other nitrogen-containing compounds [60]. This metabolic shift increases fatty acids and TAG production, which are the primary components of algal lipids.
Nitrogen starvation triggers the upregulation of genes and enzymes involved in lipid biosynthesis. Crucial enzymes involved in lipid biosynthesis, such as acetyl−CoA carboxylase (ACC), fatty acid synthase (FAS), and diacylglycerol acyltransferase (DGAT), are often overexpressed during nitrogen deprivation [61][62]. These enzymes catalyze the conversion of carbon sources into fatty acids, which are then transformed into TAGs. As lipids accumulate in the algae, they are preserved in specialized organelles termed lipid droplets. The number and size of lipid droplets in algal cells increase during nitrogen starvation, leading to higher lipid content [63].

5.3. Effect of Light Intensity and Wavelength

Light is one of the most important environmental factors for microalgal growth. Previous studies have shown that high light intensity can significantly increase lipid accumulation in microalgae. The TAG content increased and the polar phospholipid composition decreased as the light intensity was increased in Cladophora sp. [64]. Nannochloropsis sp. cultivated under low light intensity (35 µmol m−2 s−1) had a lipid composition of 26% TAG and 40% galactolipid. A unicellular alga, Scenedesmus sp., accumulates a significant amount of lipid content when cultivated under light conditions of 250–400 µmol m−2 s−1 [65]. The total lipid content of Dunaliella salina, Isochrysis galbana, and Nannochloropsis oculata increases when the light intensity is increased to 150 µmol m−2 s−1 [66]. Microalgae grown under red light showed higher lipid accumulation than those grown under yellow or white light. Microalgae cultivated under green light had lower lipid accumulation than those grown under red light. For example, exposing a unicellular microalga Chlorella sp. to red light resulted in increased growth and lipid content [67].
Another technique for improving microalgal growth and lipid accumulation is to use chemical dyes to change the light spectrum [68]. For example, organic dyes such as rhodamine 101 and 9,10-diphenylanthracene have been used to convert unused and/or harmful portions of incident sunlight into usable photons for microalgae cultivation, thereby increasing the productivity of biomass and lipids. The lipid yield of Chlorella vulgaris can be improved by cultivating it in a medium containing these chemical dyes [68]. Red paint produced the highest biomass output, while blue paint produced the maximum lipid content of 30% dry weight [69]. The lipid composition of microalgae is significantly affected by photoperiod. The effect of light intensity on the lipid composition of microalgae has been investigated in a variety of ways, and it has been found that PUFA levels decrease as light intensity increases [70]. Microalgae grown under high light intensity and long light periods had higher saturated fatty acids (SFAs) levels and lower MUFAs and PUFAs levels [71].

5.4. Effect of Temperature

Temperature changes influence not only lipid synthesis but also lipid content in the microalgae. In most microalgae, a decrease in temperature resulted in an increase in polar lipid content, while an increase in temperature resulted in an accumulation of non-polar lipids [72]. Exposing Acutodesmus dimorphus to temperature stress at 35 °C led to a 22.7% increase in lipid yield and a 59.9% increase in neutral lipid accumulation [73]. A decrease in temperature from 30 to 25 °C in Chlorella vulgaris has been shown to increase lipid content by 2.5-fold, without any change in growth rate [74]. Low temperatures simultaneously stimulate lipid content and reduce growth in Chlorella sorokiniana [75].
Although most studies focus on total lipid content, few have investigated the impact of temperature on specific lipid classes. Microalgae cultivated at low temperatures have a high content of PUFAs, which are important for survival in harsh conditions. When the temperature was decreased from 25 to 10 °C, Isochrysis galbana showed a significant increase in PUFA content [76]. Phaeodactylum tricornutum also showed a similar increase in PUFA content when the temperature was decreased from 25 to 10 °C [77]. 

5.5. Effect of Salinity

In response to salt stress, microalgae typically undergo biochemical changes that regulate lipid production. However, the salinity tolerance of different microalgae strains varies. Dunaliella sp. is an example of a microalga that can withstand high salt concentrations. Dunaliella salina is a well-studied microalga because it can use salt stress to increase both biomass productivity and lipid yield. Dunaliella tertiolecta exhibited an increase in both total lipid content and a notable percentage of TAGs when the amount of NaCl was increased [78]. Scenedesmus sp., when subjected to salinity stress of 400 mM during a biphasic cultivation process, resulted in a lipid content of 34.77% [79]. The lipid content of various microalgae, including Scenedesmus sp., Chlorella vulgaris, and Chlamydomonas mexicana, increases under salt stress conditions [19][79][80]. In most microalgae, the lipid content peaks at a certain salt concentration, and then declines significantly beyond this concentration. In Chlorella minutissima, salt stress affects both biomass production and lipid content [81].

5.6. Effect of pH

The pH affects the photosynthetic process, the solubility of inorganic nutrients, the rate of lipid accumulation, and the activity of enzymes in the cell. For microalgal growth, a certain pH range is required, which is limited and strain-specific. Microalgae are able to accumulate higher lipid content within a pH range of 7 to 9.5. Chlorella sp. showed an increase in lipid content up to 23% at pH 8, and Tetraselmis suecica showed a similar trend at pH 7.5. A study of the impact of various pH values (6, 7, 8, 9, and 10) on the biomass and lipid content of Nannochloropsis salina found that N. salina exhibited optimal growth rates and lipid content at pH 8 and 9 [82].
The relationship between CO2 and pH for microalgal cultivation is intricately linked through a process known as carbon dioxide dissolution or carbonic acid equilibrium. pH is important for microalgal growth because it affects the solubility of CO2 in the culture medium. As the pH increases, the solubility of CO2 decreases. This means that there is less CO2 available for microalgae to use. The optimal pH range for microalgal growth varies depending on the species of microalgae. However, most microalgae grow best in a pH range of 6.5 to 8.5 [24]. At pH levels below 6.5, the solubility of CO2 is too low, and at pH levels above 8.5, the toxicity of CO2 increases. When CO2 dissolves in water, it forms carbonic acid (H2CO3). 
The relationship between CO2 and pH is complex. As microalgae grow, they take up CO2 from the medium, which causes the pH to increase. This can be counteracted by injecting CO2 into the culture, or by adding a buffer to the medium. The amount of CO2 that needs to be added or the amount of buffer that needs to be added depends on the pH of the medium, the species of microalgae, and the growth rate of the culture. As CO2 dissolves in the culture medium where microalgae are cultivated, it decreases the pH of the medium. This means that as more CO2 is added to the culture, the pH of the medium becomes more acidic due to the formation of carbonic acid. Conversely, when CO2 is removed from the medium (for instance, through microalgal photosynthesis), the pH tends to increase, becoming more alkaline. This pH fluctuation is essential to monitor and control in microalgal cultivation systems because microalgae have specific pH preferences for optimal growth. 

5.7. Effect of Metal

The lipid content of microalgae is affected by the presence of trace metals, and the amount of lipids produced depends on the concentration of these metals in the growth medium. Heavy metals, including copper, zinc, and cadmium has been shown to increase lipid yield in some microalgae. Iron stands out as particularly effective in enhancing photosynthetic enzyme activities. For example, the overall lipid content of Chlorella vulgaris increases by approximately 3 to 7 times when it is exposed to FeCl3 [83].

5.8. Effect of Sulfur Starvation

Algae require sulfur in the form of sulfate as an essential nutrient for their growth. Sulfur limitation in the growth medium can induce lipid accumulation in algae. In response to sulfur limitation, algae may alter their metabolic pathways to prioritize lipid synthesis as a way to cope with the stress. For example, under sulfur starvation, Chromochloris zofngiensis and Scenedesmus acuminatus exhibit high lipid accumulation [84][85]. Sulfur stress can also change the fatty acid profile of algal lipids. This could lead to changes in the proportion of saturated to unsaturated fatty acids and the length of fatty acid chains [85]. Sulfur stress can alter the regulation of key enzymes involved in lipid biosynthesis pathways.

5.9. Effect of Phytohormones

To stimulate lipid accumulation in microalgae, it is important to use both traditional abiotic stress conditions and innovative techniques. This is necessary because there is a reciprocal relationship between biomass and lipid accumulation under abiotic stress [86]. The effects of phytohormones on microalgal metabolism, especially in relation to lipid production, are still not fully clear. However, it has been noted that auxins, a type of phytohormone, can promote the growth of Scenedesmus sp. This growth regulator has been found to increase the content of TAGs and MUFAs, while simultaneously reducing the content of PUFAs [87]. The combination of indole-3-butyric acid (IBA) at a level of 10 mg/L and 6-benzylaminopurine (BAP) at a level of 5 mg/L exhibited a synergistic effect. The synergistic effect led to a 2.34 g/L increase in biomass production and a 42.43% increase in lipid content [88]. Similar findings were reported in Chlorella sp., where the application of IBA promoted maximum growth and lipid yield [89].
Fluvic acid, an additional phytohormone, has been used to enhance lipid yield in microalgae. This effect was achieved by modulating gene expression and the actions of principal enzymes such as phosphoenolpyruvate carboxylase and acetyl-CoA carboxylase [90]. The application of salicylic acid (SA) at a concentration of 10 ppm resulted in a substantial increase in lipid, reaching 475 mg/L in the early stationary growth phase. The application of salicylic acid (SA) was found to be crucial for the formation of omega-3 fatty acids, specifically eicosapentaenoic acid (EPA, C20:5) [91]. Higher concentrations of methyl jasmonate (MeJA) were found to promote the formation of MUFAs, especially oleic acid (C18:1). Most phytohormones have demonstrated the ability to enhance biomass production, and some have also shown promise in improving lipid yield and modifying lipid composition.

6. Microalgal Biorefinery for Biofuels Production

A microalgal biorefinery is a specialized facility designed to harness the full potential of microalgae for the production of biofuels and various other valuable products. Microalgal biomass can be processed into an extensive array of products, including proteins, carbohydrates, lipids, pigments, polyunsaturated fatty acids, antioxidants, nutraceuticals, vitamins, biofertilizers, animal feed, biosurfactants, and bioenergy products (Figure 3). A microalgal biorefinery, in combination with other processes, has the potential to solve the current bioeconomic problem by producing multiple high-value products [92]. Microalgae are an efficient feedstock for generating various types of biofuels, depending on the chosen generation route (Figure 3). Microbial biomass conversion to biofuels is an alternative approach to the increasing demand for fossil fuels. Microalgal biorefineries hold promise as a sustainable and versatile solution for biofuel production, offering the potential to address energy needs while promoting environmental sustainability and economic diversification [93][94].
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Figure 3. Various types of biofuels and value-added products produced by microalgae biomass depending on the specific methods.
The zero-waste principle represents a fundamental shift in the paradigm of microalgal biorefinery, emphasizing the efficient utilization of all components within microalgal biomass to minimize waste generation [95][96]. In traditional microalgal cultivation and processing, there is often a focus on extracting a single high-value product, such as lipids for biodiesel production, while the remaining biomass and by-products are discarded. However, the zero-waste approach recognizes the intrinsic value of every constituent within microalgae and seeks to extract and utilize multiple valuable products from a single biomass source. The zero-waste principle endeavors to achieve the highest degree of resource efficiency by extracting, separating, and valorizing all components of microalgae. This entails not only the extraction of lipids but also proteins, carbohydrates, pigments, and other bioactive compounds [97]. For instance, after lipid extraction, the residual biomass can be processed to recover proteins suitable for food and feed applications, pigments for cosmetics, or carbohydrates for bioethanol production [98][99]. This comprehensive utilization optimizes resource efficiency, minimizes waste, and reduces the environmental footprint of microalgal biorefineries. Moreover, it helps diversify revenue streams by generating multiple valuable products from the same starting biomass, thereby enhancing economic viability.
Industry examples showcase the practical implementation of the zero-waste principle in microalgal biorefineries. One such instance is the production of omega-3 fatty acids and astaxanthin from microalgae [100][101]. Omega-3 fatty acids are highly valued for their health benefits and are used in dietary supplements and functional foods. Meanwhile, astaxanthin, a potent antioxidant and pigment, finds applications in nutraceuticals, cosmetics, and aquaculture feeds [102]. By cultivating microalgae for these high-value compounds, the zero-waste approach ensures that the residual biomass, which still contains valuable proteins, carbohydrates, and pigments, is put to use, reducing waste and enhancing the economic feasibility of the entire process.
Embracing the zero-waste principle in microalgal biorefinery aligns with broader sustainability objectives and the transition towards a circular bioeconomy. It reduces the environmental impact associated with waste disposal and provides an environmentally responsible alternative to resource-intensive practices. Furthermore, by efficiently utilizing microalgal biomass, the zero-waste approach contributes to the development of a sustainable and circular bioeconomy, where resources are conserved, reused, and repurposed [101]. This not only helps mitigate environmental pressures but also fosters economic resilience and innovation in the microalgal industry.
Further, microalgae biorefinery has emerged as a promising approach for sustainable and diversified bioproduct production, driven by the concept of multi-product valorization. Traditionally, the focus in microalgal cultivation has primarily been on a single high-value product, such as biofuels or nutraceuticals. However, the realization of the full potential of microalgae lies in their ability to yield multiple valuable products simultaneously. One compelling example of multi-product production in the microalgal industry is the cultivation of Haematococcus pluvialis. This microalga is renowned for its ability to accumulate astaxanthin, a potent antioxidant and red pigment used in nutraceuticals and cosmetics [103]. While astaxanthin is a high-value product, the residual biomass still contains valuable components, including proteins and carbohydrates. In response, some companies have developed integrated biorefinery processes to simultaneously extract astaxanthin, proteins, and carbohydrates from H. pluvialis, thus diversifying their product portfolios and reducing waste.
Another compelling instance involves the production of value-added nutraceuticals from microalgae. Companies have successfully cultivated microalgae such as Chlorella sp. and Spirulina sp. to produce not only lipids for biofuels but also high-protein biomass suitable for dietary supplements [104][105]. The versatility of microalgae enables the simultaneous production of lipids for biofuel and proteins for nutraceuticals, underscoring the potential for multi-product production in microalgal biorefineries. This approach enhances economic viability by tapping into multiple markets and revenue streams.
Additionally, some microalgal species, such as Nannochloropsis and Schizochytrium, offer the unique advantage of co-producing biodiesel and omega-3 fatty acids. While Nannochloropsis is known for its lipid-rich biomass suitable for biodiesel production, it also produces valuable long-chain omega-3 fatty acids such as eicosapentaenoic acid (EPA) [106]. Similarly, Schizochytrium produces docosahexaenoic acid (DHA), another omega-3 fatty acid, alongside lipids [107]. The co-production of biodiesel and omega-3 fatty acids exemplifies the potential for microalgae to serve multiple industries, including biofuels and nutraceuticals. Embracing the concept of multi-product production in microalgae biorefineries not only enhance economic feasibility but also aligns with the broader goals of sustainability, resource efficiency, and circular bioeconomy development. Here are some of the biofuels that are commonly produced using biorefineries.

This entry is adapted from the peer-reviewed paper 10.3390/su151813678

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