A review on lipid production from microalgae: Association between cultivation using waste streams and fatty acid profiles

Renewable and Sustainable Energy Reviews 109 (2019) 448–466

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Renewable and Sustainable Energy Reviews journal homepage: www.elsevier.com/locate/rser

A review on lipid production from microalgae: Association between cultivation using waste streams and fatty acid profiles

T

G.F. Ferreira, L.F. Ríos Pinto∗, R. Maciel Filho, L.V. Fregolente School of Chemical Engineering, University of Campinas, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Microalgae Wastewater Lipids Fatty acid profile CO2 Biorefineries

Microalgae are potential sources of high-value lipids, with essential fatty acids that provide health benefits, as the omega-3 polyunsaturated fatty acids. However, its cultivation and downstream processing is still not commercially viable for some applications due to high-water consumption and high costs mainly regarding energy demands and nutrients as nitrogen. Therefore, using waste streams in existing industries as carbon and nutrient sources, as well as evaluating the best methodologies for growth and lipid extraction are essential to viabilize this process. This review focused on the study of scenario the of using different microalgae species, integrating their cultivation into biorefineries using their wastewater and carbon dioxide combating water and air pollution, aiming lipid productivity and fatty acid profile with specific composition. It was found that culture medium conditions and cultivation systems are key elements in understanding the lipid production and can decisively affect the process performance. For example, closed photobioreactors with CO2 supply and light can provide higher photosynthetic efficiency and lipid accumulation, coupled with polyunsaturated fatty acid production. Wastewater use can reduce productivity and affect lipid composition, but CO2 injection can promote both higher biomass and lipid productivities; being Chlorella a potential candidate for implementation in industrial facilities once it showed high PUFA (around 1/3) and lipid content, up to 27%, grown in wastewater. Moreover, it is crucial to seek biomass fractioning to obtain different high-value products that will compensate for high capital and operating costs. Further evaluation of possible effects in the final product quality is required.

1. Introduction A wide range of bioproducts, including biofuels that are largely studied from different biomasses, represent alternatives to fossil sources due to the lower overall emission balance [1–3], possible mitigation of oil prices fluctuations in the international market and energy security. Within the possible biomass, microalgae are considered a promising option. They are a type of phytoplankton that exhibits a high growth rate, and some species can duplicate their cells several times a day, which consequently results in high yields of biomass [4]. Additionally, these bioproducts obtention can be combined with pollution control if wastewater and CO2 are used for growth, seeking a more sustainable process [5,6]. Photosynthetic conversion of solar energy, CO2, and even the conversion of wastewater into a variety of bioenergy products, food additives, pharmaceuticals, and cosmetics can be achieved by microalgae cultivation [7]. Therefore, its growth can be integrated with biorefineries, as is the case for bioethanol industrial sites, to produce microalgal biomass with minimal environmental impact. Among the

∗

primary metabolites produced from microalgae, lipids have been often designated to biodiesel production, but after evaluating mainly its fatty acids composition and carotenoids content, many researchers have turned their attention to possible higher-value products. Promising and widely studied species with high lipid content include; Botryococcus braunii, Chlorella vulgaris and Scenedesmus obliquus [8,9]. Other positive aspects of lipid production from microalgae are its semi-batch growth all-year-round and tolerance to adverse conditions. However, higher cultivation costs and energy requirement are observed in comparison to conventional crops production [10]. Despite microalgal biomass being vastly explored for biodiesel production in the past years, it is not currently cost competitive at large scale compared to conventional biofuel's feedstocks [11]. In China, although government support was present, microalgae biodiesel has failed to achieve the proposed goals, hardly being able to reach in the near future due to the lack of product benefits, among other reasons [12]. Therefore, there is a significant distance in making biodiesel from microalgae commercialized [13,14]. In this context, this review provides information on the main topics

Corresponding author. E-mail address: [email protected] (L.F. Ríos Pinto).

https://doi.org/10.1016/j.rser.2019.04.052 Received 16 July 2018; Received in revised form 9 April 2019; Accepted 16 April 2019 1364-0321/ © 2019 Elsevier Ltd. All rights reserved.

Renewable and Sustainable Energy Reviews 109 (2019) 448–466

G.F. Ferreira, et al.

List of abbreviations ATP C COD DAG DHA ED EPA FA Fe FFA GHG H HC

K MAG MUFA N NPK P PBR PUFA Rubisco SFA TAG TN TOC TP

adenosine triphosphate carbon chemical oxygen demand diacylglycerol docosahexaenoic acid endoplasmic reticulum eicosapentaenoic acid fatty acid iron free fatty acid greenhouse gas hydrogen hydrocarbon

potassium monoacylglycerol monounsaturated fatty acid nitrogen nitrogen, phosphorus, and potassium phosphorus photobioreactor polyunsaturated fatty acid Ribulose bisphosphate carboxylase/oxygenase saturated fatty acid triacylglycerol total nitrogen total organic carbon total phosphorous

sustainable medium and biomass production improvements (Table 2). Compared to Table 1, slightly lower biomass productivity and lipid content are reported for most species. However, effluent treatment was verified, by the reduction of total nitrogen (TN), total phosphorous (TP), and chemical oxygen demand (COD), for example. Consequently, despite challenges as contamination and lower productivity still to be overcome, lipids from microalgal biomass could be integrated with bioremediation. Comparing Tables 1 and 2, for B. braunii, the highest biomass productivity was observed using wastewater (0.28 g L−1 d−1), and a lower value (0.22 g L−1 d−1) was the highest using synthetic medium. But up to 45% lipid content reduction using cheaper culture medium was obtained. C. vulgaris, on the other hand, showed a decrease in biomass productivity and increase on lipid content using wastewater, on average; and for Desmodesmus sp., these did not vary significantly. It is important to notice that the same cultivation conditions must be taken into account when evaluating if wastewater use influence negatively microalgae growth. As the studies reported on Tables 1 and 2 are from different authors, this comparison is an initial attempt to assess this question. There are different species of microalgae with high lipid productivity, as the ones from the Botryococcus genus that studies have already demonstrated the production of up to 70% of lipids under nitrogen stress conditions [56]. B. braunii is a colonial green microalga rich in hydrocarbons, which are produced and mostly secreted into the external environment, i.e., they are located in the outer cell wall. Consequently, Botryococcus species usually shows higher lipid content compared to other microalgae. Oleaginous microalgae produce neutral lipids and accumulate them in lipid droplets [57]. Lipid accumulation, in turn, is mostly dependent on nutrient stress. Nitrogen, phosphorus, pH, salinity, metals, light, CO2, amongst others, are parameters manipulated for increasing biomass productivity and lipid yield [58,59]. In the same microalgae strain, lipid composition may change depending on cultivation conditions. Palliwal et al. [60] compared literature results that showed increased triacylglycerol's (TAG's) concentration when abiotic stress factors are applied, such as high light intensity and nitrogen or phosphorus starvation. Nutrient deprivation has different responses in cell cycle cessation, once greater lipid accumulation due to N deprivation has been generally observed when compared to P deprivation [61–63]. Consequently, microalgae strain selection requires the evaluation of several aspects altogether. Besides the vital information contained in Tables 1 and 2, to enable microalgae cultivation in sustainable media, it is essential to understand nutrient tolerance. Nevertheless, promising microalgae species for lipid production and CO2 biofixation are B. braunii, as well as some Chlorella and Scenedesmus species. Additionally, genetically modified strains could further improve these aspects. Genetic improvement could be achieved using different methods such as

involved in microalgae cultivation that can influence biomass and lipid productivity, such as strain selection, growth regimes, cultivation systems, and lipid extraction process. Emphasis was given to the production of lipids with high added value in a sustainable culture, highlighting the possibility of using flue gases as CO2 source and wastewater effluents as a nutrient source. Furthermore, as studies indicate that by using waste streams, biomass production is usually reduced, it is still necessary to overcome some barriers to achieve a bio-based refinery. Many review papers have assessed the possibility of using microalgae for wastewater treatment [15–20] that can provide simultaneously nutrient and other pollutant's removal, and high biomass production. Main findings to implement this idea were to adapt cultivation systems to avoid internal shading and high suspended solid contents by using turbulent flow [16], but mechanisms involved in pollutant removal and bio-conversion are still unclear [17]. Challenges as highcosts could be minimized by coupling wastewater treatment with biomass production for biofuels [21,22] and CO2 sequestration [23–26]. Others as contamination are still to be overcome [18]. Moreover, the effects of producing lipids from microalgae cultivated using wastewater and CO2 regarding its productivity and composition still require more information. Therefore, the consequences of recycling nutrients in a sustainable and integrated process that could affect product quality, were discussed in the work. This review highlights key points in the field, consicely describing the advances on key processes involved in microalgae cultivation, and apart from several studies that focus on biofuel's production, attention was given to polyunsaturated fatty acids, comparing different applications and economic studies. 2. Microalgae cultivation 2.1. Microalgae strain selection The first step towards microalgae application in industry is selecting a specific species according to its performance as bioremediator, CO2 sequester, as well as its biomass composition. Table 1 shows studies reported in the literature for comparison of different microalgae, with or without CO2 supplementation during cultivation. The results will help the selection between the most promising and widely studied species; Botryococcus, Chlorella, and Scenedesmus family. Also, Nannochloropsis was inserted to compare experimental results with a marine microalga, usually explored as an omega-3 source. The most used autotrophic culture media are BG-11 and Chu-13 with CO2 supplementation, but there can also be found studies using gaseous effluents [27–29] as an additional nutrient source, associating growth with effluent treatment. Among mixotrophic culture studies, synthetic medium with an organic carbon source is used [30,31]. On the other hand, many studies found in literature used existing aqueous effluents and solid wastes for microalgae cultivation, aiming at 449

450

a

CO2 only as respiration product.

Scenedesmus obtusiusculus

Scenedesmus obliquus

Nannochloropsis sp.

Desmodesmus sp.

Desmodesmus brasiliensis

Chlorella vulgaris

Chlorella sp.

Chlorella kessleri Chlorella sorokiniana

Mixotrophic Autotrophic

Zarrouk BG-11

Autotrophic Mixotrophic Autotrophic Autotrophic Autotrophic Autotrophic

N11 Varied (2+) Modified Detmer BG-11 Modified Detmer BG-11

Autotrophic Autotrophic Autotrophic

Mixotrophic Autotrophic

BBH 27 BG-11

BG-11 Bold N3 Modified F/2

Autotrophic Autotrophic Autotrophic

Autotrophic

Modified Walne Basal Modified Chu-13 BG-11

Autotrophic

Autotrophic Autotrophic Autotrophic Autotrophic Mixotrophic Autotrophic Autotrophic Mixotrophic Autotrophic

Culture type

Varied (2+)

Modified Chu-13 Varied (2+) Modified Chu Modified Chu-13 Zarrouk Modified Chu Modified Chu-13 Bristol BG-11

Conical flask 250 mL Tubular photobioreactor 2 L Erlenmeyer 1 L Erlenmeyer 1 L Fermenter 11 L Erlenmeyer 1 L Erlenmeyer 1 L Erlenmeyer 2 L Photobioreactor “air-lift” 2.4 L Erlenmeyer 250 mL Bubble column photobioreactor 2.5 L Erlenmeyer 1 L Erlenmeyer 1 L Erlenmeyer 250 mL Photobioreactor 5 L Erlenmeyer 250 mL Fermenter 11 L Erlenmeyer 250 mL Erlenmeyer 3 L Photobioreactor 1 L Erlenmeyer 250 mL Erlenmeyer 250 mL Erlenmeyer 2 L Photobioreactor 1 L Erlenmeyer 250 mL Photobioreactor 1 L Bubble column photobioreactor 2.5 L

Botryococcus braunii

Botryococcus terribilis

Inoculum culture medium

Cultivation system

Microalga

0.10–0.29 0.25–0.52

0.17 0.37–1.14 0.16–0.28

0.70

0.05 0.18–0.32 0.38

0.31 0.02

0.32–0.73 0.39–0.41

0.10–0.14 0.21–0.32 0.04

0.04–0.11

0.87

0.06–0.15 0.18–0.22 0.10–0.22 0.12–0.24 0.21 0.10–0.18 0.11–0.24 0.11 0.04–0.17

Biomass productivity/g L−1 d−1

Table 1 Studies reported in literature on the cultivation of microalgae in medium enriched with CO2.

40.95 – – 11.0–34.6 – – 15.62–16.25 24.96–50.43 – – 11.2–25

16.74 – – 31.5–39.2 – – – 20.90–52.88 – – 27.9–63.4

– –

– –

–

– 28.67–33.07 – –

–

–

20.30–36.77 – –

– 32.4–34.1 35.6–54.7 – 39.61 45.7–61.5 – 20.62–21.87 –

Protein composition/ %DW

4–55 26.0–30.1 14.2–30.6 – 2.38 6.9–11.2 – – –

Carbohydrate composition/%DW

12.2–38.9 25.4–59.4

18.50–19.38 7.67–13.66 17.7

38.9–43.9

6.5–9.1 9.6–53.8 14

9.95 5.4–5.8

13.1–18.7 5.1

21.69–28.07 19.1–21.4 2.4–4.4

16–25

12–25.9

0–45 32.6–34.6 11.0–47.1 30.0–32.0 33 18.5–40.0 29.7–31.2 19.25–20.55 28–43

Lipid composition/% DW

0.20–0.55 –

0–0.50 0.63–1.99 –

0.77

– – –

0.25 –

[48] [49]

[37] [47] [42]

[46]

[42] [45] [39]

[36] [42]

[43] [44]

a

a

a

[41] [35] [42]1

– 0.36–0.61 – 0.02–1.28 –

[40]

[39]

[32] [33] [34] [35] [36] [34] [35] [37] [38]

Reference

–

–

– – – 0.29–0.56 0.50 – 0.26–0.61 0.11–0.17 0.07–0.24

CO2 biofixation/g L−1 d−1

G.F. Ferreira, et al.

Renewable and Sustainable Energy Reviews 109 (2019) 448–466

451 NPK (10:26:26) fertilizer (solid)

Autoclaved and non-autoclaved wastewater (aqueous) Diluted (50%) or clarified vinasse (aqueous) Autoclaved and non-autoclaved wastewater (aqueous) NPK (10:26:26) fertilizer (solid)

Urban wastewater (aqueous)

0.01–0.08

0.02–0.07

0.04–0.05

0.10–0.18

0.04–0.05

0.02–0.23

0.05–0.12

0.07–0.11

0.13–0.22

0.10–0.28

Biomass productivity/g L−1 d−1

COD (chemical oxygen demand); TN (total nitrogen); TOC (total organic carbon); TP (total phosphorous). a Fatty acid composition. b Maximum.

Spirulina platensis

Scenedesmus sp.

Erlenmeyer 250 mL Erlenmeyer 1 L

Photobioreactor “air-lift” (flat plate) 13 L Erlenmeyer 3 L

Micractinium sp.

Desmodesmus sp.

Ilmabor bottle 1L Erlenmeyer 3 L

Desmodesmus communis

Erlenmeyer 1 L

Diluted (50%) or clarified vinasse (aqueous) Urban and synthetic wastewater (aqueous) Domestic wastewater (aqueous)

Photobioreactor “air-lift” (flat plate) 13 L Pyrex flasks 2 L

Chlamydomonas biconvexa

Chlorella vulgaris

Domestic wastewater (aqueous)

Erlenmeyer 1 L

Botryococcus braunii

Residue used as culture medium (phase)

Cultivation system

Microalga

–

–

26.40–31.10 – 38.14–54.43

– –

39.50–39.62

25.80–34.80

18.10–19.50

17.55–21.79

15.90–17.70

9.60–26.60

21.25–21.85

–

34.70–61.90

39.92–41.68

–

– 11.71–13.50

Protein composition/ %DW

Carbohydrate composition/%DW

Table 2 Studies reported in literature about the cultivation of microalgae in enriched medium with aqueous or solid residues.

7.20–12.76

28.55b

12.50–13.40

2.21–2.50

a

8.30–10.80

2.10–9.30b

13.40–27.28

21.75–22.02

1.26–1.58a

9.55–26.00

Lipid composition/% DW

[51] [53] [54]

TOC, TP, PO43−, NO3−, NO2− NH4 (N), PO43–

[55]

[53]

NH4 (N), PO43-

–

[52]

[50]

[37]

[51]

[50]

Reference

COD, TN, NH4, NO3, PO4 N, P

COD, TN, NH4, NO3, PO4 TOC, TP, NO3−, NO2− TN, PO4

Effluent treatment (reduction)

G.F. Ferreira, et al.

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described by Nasir et al. [64]: ‘selection of novel strain, stress tolerance, resistance to pathogens, product development and metabolic pathways and cellular contents’.

Usually, studies with liquid wastes involve streams presenting high concentration of NPK nutrients (nitrogen, phosphorus, and potassium) and organic matter. However, wastewater sources have different nutrient concentrations, some of which could be toxic to microalgae. Collos and Harrison [67] evaluated the effect of nitrogen concentration from ammonia addition on six classes of microalgae. They obtained an optimal and toxic concentration of 7600 and 39,000 μM, respectively, for Chlorophyceae. This nutrient tolerance could be improved through acclimation of strains in culture. Furthermore, as the toxicity of ammonium and ammonia can be different, varying with other culture parameters such as pH, light, and temperature, the authors concluded that further research is needed. Besides the parameters already discussed for strain selection, it is also important to choose algae with high tolerance to organic pollutants for growth on wastewater, as the potential genera Scenedesmus and Chlorella [19,22]. Wen et al. [68] showed that a C. vulgaris strain could be grown in undiluted swine slurry, obtaining more than 90% TN and TP removal and also high tolerance to high concentrations of COD. Different liquid wastes used into microalgae cultivation include; industrial and agro-industrial wastes [66,69,70], domestic wastewater [8,71,72], livestock wastewater from animal farms [73], swine wastewater [74], stabilization lagoon from sanitation facility [53], poultry

2.2. Integration of effluent treatment and lipid production 2.2.1. Aqueous and gaseous waste streams as nutrient and carbon source Microalgae cultivation for lipid production integrated into effluent treatment may help processes to become environmentally and economically advantageous [65]. An alternative for making this possible is to enrich the culture medium with residues, such as wastewater and CO2 from industry or urban effluents [66]. The use of microorganisms to reduce contamination from the environment is known as bioremediation. Some studies approached microalgae growth on pretreated or raw wastewater from different industries, but others such as from Abdel-Raouf et al. [15] and Salama et al. [21] suggested they could be used as a tertiary and quandary treatment to remove remaining organic and inorganic pollution, after conventional primary and secondary treatment processes. Either way, effluent treatment can be accomplished and still provide lipid concentration in microalgae biomass. Fig. 1 was assembled to summarize the perspective of integrating microalgae cultivation in an existing industrial facility.

Fig. 1. Integrated biorefinery concept. 452

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considered high. Others aim at the discovery of new microalgae strains tolerant to extremely high CO2 concentrations, between 40 and 100% [85]. High concentrations increase CO2 mass transfer and can improve lipid accumulation. However, it decreases the medium pH [86,88]. Thus, it is necessary to work with high CO2-tolerant microalgae species, also improving CO2 fixation rate, which is light-dependent and limited by cell density [23]. Green microalgae that are efficient carbon sequesters generally belong to the genera Chlorococcum, Chlorella, Scenedesmus and Euglena [89]. According to Singh and Singh [90], Chlorella species are commonly used for carbon sequestration, because they contain chlorophyll a and b, which promote high photosynthetic efficiency to convert CO2 to O2. Furthermore, B. braunii can grow under high CO2 concentrations in the flue gas, enhancing biomass production. Despite industrial implementation being interesting due to the carbon footprint reduction that CO2 removal could result in, it is also limited by the presence of toxic substances in exhaust gases [91]. Other abiotic factors influence CO2 sequestration such as temperature, light intensity or salt concentration. Carbon dioxide solubility changes with cultivation temperature, once the CO2 removal rate is temperature dependent [92], and high light intensity usually increases CO2 removal rates due to photosynthesis. However, as any microorganism, algae also have an optimal cultivation condition that limits these modifications in culture medium and overall system. In general, taking into consideration that limitation, several studies in the literature show that CO2-enriched environments can increase biomass production, as discussed previously. For example, by analyzing Table 1, C. vulgaris and S. obliquus showed the best results for CO2 biofixation, of 1.28 and 1.99 g L−1 d−1, cultivated under mixotrophic and autotrophic regimes, respectively. Also, CO2 could contribute to nutrient removal, as suggested by Yao et al. [93]; the aeration of CO2 improved the tolerance of Chlorella sorokiana and Desmodesmus communis to high concentrations of NH4eN. After selecting a tolerant microalgae strain and culture medium, it is necessary to decide between growth conditions and culture systems, as well as evaluating downstream processes to ensure viability, such as harvesting and dewatering, and lipid extraction. It is important to highlight that CO2 biofixation is not only vital to

litter [75], among others. An exciting industry for microalgae integration is the bioethanol industry, which could provide CO2, nutrient-rich streams as biofertilizers from vinasse and bagasse, with the potential valorization of its residues [76,77]. Santana et al. [51] analyzed two different microalgae strains cultivated in the synthetic medium Bold's Basal Medium (BBM) and in water-diluted vinasse to produce fatty acid (FA). The authors obtained the highest FA productivity using a 50% water-diluted vinasse for Micractinium sp. and 100% clarified vinasse for Chlamydomonas biconvexa. Although biomass and FA productivities increased, carotenoid content was significantly lower using 50% diluted vinasse, and decreased further for 100% clarified vinasse. Tasic et al. [78] studied Desmodesmus sp. growth in biodigested and in natura vinasse, monitoring carbon and nitrogen consumption. Their results were biomass concentrations of 0.3 and 0.5 g L−1, respectively; so biodigested vinasse could be an alternative to reduce costs. Sydney et al. [65] evaluated the growth of some microalgae species in vinasse and CO2, obtaining a lipid content up to 19.5% with B. braunii cultivated in aqueous medium with 30% vinasse during 15 days. However, it is important to mention that despite vinasse being a promising source of nutrients and organic carbon, there are still challenges regarding low light transmittance as it is a dark medium and prone to contamination [51]. When gaseous effluents are combined with microalgae cultivation for lipid production, due to its impact in photosynthesis, the streams of interest are frequently rich in CO2. Studies involving bio-fixation of CO2 from different sources often use combustion gases from coal [27,28,79–81], flue gases from a steel plant [82], flue gas from a coke oven [29], CO2 from cement manufacturing facilities [25], among others. Solid residues are also explored but used in the minority. Da Silva Vaz et al. [79] used gaseous effluents and solid residues from the thermoelectric energy industry and evaluated biomass concentration of Chlorella fusca and its bio-fixation of CO2, obtaining maximum values of 0.84 g L−1 and 42.8% (v/v), respectively. The authors also showed that microalgae could be grown on a pilot scale. Kao et al. [82] cultivated Chlorella sp. using aeration with flue gases from a coke oven, hot stove and power plant, rich in CO2, NOx, and SO2. It was obtained in promising results of a maximum specific growth rate of 0.827 d−1 and lipid production of 0.961 g L−1. Thus, existing gaseous effluents could be used for microalgae cultivation, simultaneously for CO2 biofixation and possible biomass and lipid production improvements. However, appropriate gas exhausts should be selected to avoid inorganic contaminants that could cause toxic effects [83]. In summary, studies that used wastewater as nutrient source for microalgae growth suggest that this is a viable alternative, however, nutrient concentrations causing inhibitory effects and contamination still require further research. Gaseous effluents rich in CO2 also poses as a promising addition to culture medium once it could improve biomass, and mostly, lipid productivities. 2.2.2. CO2 effect on microalgae growth Independent of nutrient deprivation, biomass or lipid production is not possible without carbon. Therefore, the highest lipid concentrations can be achieved with high concentrations of inorganic carbon together with N and/or P limitations [62]. When nitrogen is limited, but the light is in excess, photosynthetic fixation of carbon continues while growth ceases; consequently, the C:N ratio increases and TAGs will be produced from excess carbon [84]. Several studies search for CO2-tolerant strains that can accumulate lipids in CO2-rich environments [85]. Biological sequestration of inorganic carbon by microalgae occurs, in general, through photosynthesis, i.e., in the presence of light and gaseous CO2. As can be observed graphically in Fig. 2, during the Calvin Cycle, CO2 from the atmosphere or other sources is converted into sugar by the Rubisco enzyme with an energy source, ATP [86]. The optimal CO2 level for growth varies among different microalgae strains, ranging from a minimum and maximum that inhibits their growth. Most studies evaluate CO2 concentrations from 0 to 20% in volume [87], which is

Fig. 2. Scheme of CO2 up-take and lipid production in microalgae cells. 453

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cultivation. It is possible to conclude that in an efficiency point of view, pure CO2 supply would be more appropriate. However, the most viable and feasible case would be to integrate microalgae cultivation with an existing plant, hence using an effluent gas. Commonly used flue gases are coal combustion gases, in power generation plants [28,81]. Its composition varies among CO2, NOx, and SOx gases [27]. Several other industries produce combustion gases containing CO2, thus being a potential recipient for this technology. According to Borowitzka and Moheimani [97], as 1.8 g of CO2 is required for each gram of algae produced, this biomass represents a natural and efficient tool for CO2 capture. Another quite suitable option is to explore the integration in a 1st ethanol plant where pure CO2 is available as a byproduct of sugar fermentation. The interesting point in such integration is to be able to use the biomass in the context of a biorefinery in a more accessible way since ethanol production plant may also produce sugar and electricity besides ethanol [98].

improving biomass and lipid productions but also to reduce carbon footprint, attending local and global environmental agreements. In pursuit of greenhouse gases (GHGs) emission reduction, there are important international agreements on climate action such as the Kyoto Protocol and Paris Agreement. In Brazil, a recent government initiative promotes sustainable development, by encouraging research into the production of biofuels and renewable bioproducts, known as the RenovaBio program. RenovaBio is a National Biofuel Policy, instituted by Law 13.576/2017. The program aims, among other goals, to reduce the emission of GHGs in the production, commercialization, and use of biofuels. 2.3. Growth conditions There are three types of microalgae cultivation: autotrophic, heterotrophic, and mixotrophic. In autotrophic cultivation, the microalgae absorb energy from natural (sunlight) or artificial sources and produce organic matter by photosynthesis, bio-fixating CO2. The heterotrophic culture consists of growing it in a dark environment with an external source of organic matter. Finally, mixotrophic is the junction of both, where the microalga has periods of photosynthesis and consumes other carbon source [94]. Therefore, to improve biomass and lipid production with CO2 sequestration, microalgae could be grown under autotrophic or mixotrophic conditions, which allow photosynthetic conversion. Moreover, aiming at an industrial scale, mixotrophic cultivation would be desirable, integrated with effluent treatment.

2.3.2. Mixotrophic In addition to CO2 bubbling in the medium, an organic carbon source can be added in aiming to improve biomass and lipid productivities. Table 4 shows different studies involving mixotrophic cultivation. Usually, microalgae present a faster growth when adding pure carbohydrates (ex. glucose, glycerol) to the medium [113,114], but efforts are made to use an effluent stream from an existing industry such as agro-industrial wastes. Which could increase biomass productivity in some cases. Cabanelas et al. [50] achieved biomass and lipid productivities of 224.81 mg L−1 d−1 and 56.2 mg L−1 d−1, respectively, for Botryococcus terribilis cultivated in wastewater medium with 2.5% CO2 supplementation, which was superior to the 116 mg L−1 d−1 and 36.2 mg L−1 d−1 obtained using synthetic medium Chu13 [35]. On the other hand, there are obstacles yet to be overcome, such as; culture contamination due to bacteria or fungus growth, the presence of inhibitors such as toxic metals, lower photosynthetic efficiency when dark media is used, among others. By improving those aspects of using a sustainable culture medium, microalgae cultivation would be closer to economic viability [91,129,130]. To couple biomass production, bioremediation of aqueous streams, and CO2 sequestration, the mixotrophic growth would be chosen. It is not only advantageous during climate variations where sunlight is not abundantly available but also because it works as a dual carbon source. Furthermore, naturally occurred microalgal blooms are not axenic, thus an option to avoid a strong bacteria and fungus contamination would be two- or more microalgae consortium that allow a larger population growth. For example, a CO2tolerant microalgal consortium formed by Chlorella sp., Scenedesmus sp., Sphaerocystis sp. and Spirulina sp. demonstrated high growth performance in wastewater, removing nutrients [131].

2.3.1. Autotrophic Autotrophic culture is mainly advantageous for industrial scale because it has the lowest risk of contamination [25]. In regards to this condition, it is more promising to migrate from a closed to an open system aiming at cost reduction without compromising biomass productivity. As it requires light to produce organic matter through photosynthesis, a natural source is desirable once an artificial one would further increase costs. However, this would be dependent on the environment weather conditions. Light intensity and photoperiod are usually proportional to biomass growth up to the limit of photo-inhibition. For example, the results obtained by Ruangsomboon [95] showed that for B. braunii microalgae, the highest biomass concentration was observed under a 24:0 light cycle, which was four times the biomass under 12:12 light/dark cycles. However, lipid yield was highest under a 16:8 photoperiod. Increasing light intensity, on the other hand, improved lipid production, but demonstrated various biomass concentration uniformly. Thus, despite using the same species, other parameters than light intensity and photoperiod influence biomass production. Light spectra can also contribute to the photosynthetic performance of some microalgae strains, affecting lipid and chlorophyll content, as demonstrated for Nannochloropsis sp. by Vadiveloo et al. [96]. Table 3 shows the advantages and disadvantages of autotrophic culture using different inorganic carbon sources for microalgae

2.4. Cultivation systems Cultivation systems can be open or closed. Open systems are

Table 3 Comparison of different gaseous streams on microalgae autotrophic cultivation. Inorganic carbon source

Advantages

Disadvantages

References

Air

Lower cost than pure CO2. Higher biomass productivity. Clean source. Fixed carbon diverted from protein to lipids. Improved photosynthesis. Higher lipid production. Higher added value products. pH controller. Effluent treatment. Higher lipid production. Low cost.

Competition between respiration and photosynthesis rates. Lower lipid productivity (increasing oxygen concentration). Higher cost. Mass transfer limitations. SFA concentration when associated with N depletion.

[99,100]

Growth inhibition by other gases (e.g., NOx, SO2). Possible medium contamination (metals). Presence of ash.

[83,108–112]

CO2

Flue gases (CO2, SOx, NOx)

454

[101–107]

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Table 4 Comparison of different aqueous streams on microalgae mixotrophic cultivation. Organic carbon source

Advantages

Disadvantages

References

Glycerol

Usually lower biomass yield than glucose.

[115–118]

High cost.

[111,115,116,118,119]

Sodium acetate

High lipid productivity. May present higher biomass and TAGs productions compared to synthetic medium. Lower cost than glucose. Clean source. High biomass production. High lipid productivity. Clean source.

[116]

Sucrose

Clean source.

Higher cost and lower biomass productivity than glucose. Higher cost and lower biomass productivity than glucose. Same as glycerol. Toxic compounds (high ammonia concentration). High contamination.

Glucose

Urea Aqueous residue

Piggery slurry Sewage Vinasse

Other wastewaters

Low cost. Effluent treatment. Low cost. Abundant source. Same as piggery slurry. Same as piggery slurry. Source of NPK and carbon.

Nutrients removal. Reduction of chemical and biochemical oxygen demands for disposal. Same as piggery slurry.

Contaminants. Dark medium. Solid particles. Varying composition between crops. Growth rate decrease. Scale-up limitations.

[116] [115] [120–122] [111,123] [51,65]

[110,124–128]

employed [140,141], thus avoiding the necessity of cell disruption. It has been known that the efficiency of a cell disruption method varies among different species, which is reasonable to assume once cell walls and membranes have a varying composition between strains. These methods include microwave, water bath, blender, ultrasonic and laser treatment [142], but are commonly physical (thermolysis/autoclave) or mechanical (bead mill) followed by oven or freeze-drying [138]. Finally, following cell disruption, microalgae biomass can be fractionated into lipids, carbohydrates, proteins, pigments or others [143]. Oil/lipids extraction, in turn, can be divided into two groups: mechanical and chemical extractions. Chemical extraction mainly consists of organic solvents, widely used and preferred in comparison to mechanical methods due to lower initial capital investment [144]. Nonetheless, there is little testing of non-solvent extractions except in laboratory

preferred for cost reduction [101] and consist mainly of open ponds with different agitation systems (lagoons, circular ponds, raceway ponds, tanks, etc.). According to Chen et al. [132], phototrophic cultivation is desired for open pond systems, because heterotrophic cultivation can be easily contaminated and requires an organic carbon source. Slade and Bauen [133] show that raceway pond systems have a lower net energy ratio for microalgae biomass production that it drastically decreases due to algae cultivation and harvesting. However, there are still challenges in productivity, as demonstrated by Nwoba [134]. The authors compared microalgae growth in a tubular photobioreactor and a raceway pond, obtaining volumetric biomass productivity 2.1 times higher in the closed system. Therefore, it is a question of balancing economic feasibility and product yield to decide between culture medium conditions and cultivation systems. Closed systems enclose all photobioreactors (plastic bags, horizontal/vertical tube, bubble column, airlift, flat panel, among others) or not commonly used systems such as membranes. PBRs are advantageous because they prevent evaporation and reduce both contamination risks and CO2 losses [135]. They are mainly used for producing high-added value products; however, they present an economical limitation in comparison to open ponds as shown so far for biodiesel production from microalgae. Currently, the best cultivation system consists most likely in using hybrid systems, to obtain a resistant and concentrated inoculum in PBRs followed by large-scale cultivation in an open system, as depicted on Fig. 3. Recent studies have also evaluated possible configurations and operating conditions of PBRs to optimize biomass yields and pollutants removal, being the best-known options; flat plate for biomass and soft-frame or membrane for bioremediation [136]. 3. Oil extraction After harvesting, which could be performed through sedimentation, filtration, centrifugation, flocculation and/or flotation [26,132], a disruption of microalgae cells is necessary to ensure that the oil produced is available [137]. Different methods to disrupt microalgae cell walls are arranged as mechanical, and non-mechanical (thermal, chemical, and biological) [138,139]. As Botryococcus are the only known exception of extracellular lipid accumulation, continuous cultivation could be achieved and non-destructive methods of lipid extraction could be

Fig. 3. Hybrid systems for microalgae cultivation. 455

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highly purified extracts that are free of potentially harmful solvent residues [145,152]. Moreover, CO2 wastes from industry could be potentially used under supercritical conditions, which would reduce costs and be environmentally advantageous. Santana et al. [153] evaluated the supercritical carbon dioxide extraction of lipids from B. braunii, obtaining higher recovery of polyunsaturated fatty acids as pressure increased (optimal condition of 250 bar and 50 °C). Mendes et al. [154] evaluated supercritical CO2 extraction, comparing four microalgae, and observed high purity extracts in contrast with those obtained with organic solvents. The selective extraction of hydrocarbons from B. braunii also increased with pressure. Supercritical CO2 has another advantage of scaling-up once it is solvent free and studies have demonstrated its superior efficiency for TAGs recovery and fatty acids composition in relation to hexane Soxhlet extraction [155]. Therefore, this technique would be the most suitable to extract high-value bioproducts to be applied in the pharmaceutical and food industries, on top of being eco-friendly. The only disadvantage compared to more conventional methods is still costs regarding high energy demands [156].

scale [145]. Depending on the process selected, different oil compositions are obtained once microalgae consist of a mixture of various lipids. Besides neutral lipids, mainly TAGs and free fatty acids, microalgae lipid composition can consist of polar lipids (glycolipids, phospholipids, sterols, and chlorophyll derivatives), unsaponifiable matter and others [146]. 3.1. Chemical extraction Commonly used solvents in chemical extraction are alcohols (e.g., isopropanol, ethanol or methanol), hydrocarbons such as hexane or more efficient but toxic solvents such as chloroform. In a laboratory scale, conventional methods include Bligh and Dyer (a mixture of water, methanol, and chloroform) and Soxhlet extractions. Hussain et al. [147] compared lipid extraction in C. vulgaris by hexane Soxhlet, Halim (a mixture of hexane and isopropanol), and Bligh and Dyer. The authors applied the methods on freeze- and oven-dried biomass and obtained the highest lipid extraction with Halim method on oven-dried C. vulgaris. It was observed that different drying and extraction methods did not significantly influence the lipid's fatty acid profile, also confirmed from other studies [147,148]. Focusing on Soxhlet extraction, Ramluckan et al. [149] evaluated 13 different solvents on lipid extraction from a mixed algal culture containing mostly Chlorella sp. The highest lipid content was obtained with a combination of ethanol and chloroform (11.76%), being the latter also the best single solvent extraction (10.78%). These results are consistent with the fact that a large quantity of microalgae cultivation studies uses the Bligh and Dyer [150] method for lipid extraction, which comprises an alcohol and chloroform. Other known chemical methods include ionic liquid extraction. This technology has the advantage of using ionic liquids that are non-volatile, thermally stable and can be synthesized from different routes [144]. Despite results that present higher lipid yields using ionic liquids with organic solvents or ultrasonication, this process would result in higher capital costs: reagents and their purification/reuse.

4. Fatty acid profile Microalgae fatty acids are common carboxylic acids with hydrocarbon chains between 4 and 36 carbons [157]. They are usually divided between saturated, monounsaturated, and polyunsaturated fatty acids. Main saturated fatty acids (SFA) in microalgae range from butanoic (C4:0) to octanoic (C28:0), being palmitic (C16:0) acid the most common. Monounsaturated fatty acids (MUFA) can also have different hydrocarbons chains (mainly from 14 to 24 carbons), but oleic acid (C18:1), also known as omega-9, is usually the most present in microalgae composition. Polyunsaturated fatty acids (PUFA) represent the highest added-value lipid components, such as linoleic (C18:2) and linolenic (C18:3) acids, also known as omega-6 and -3, respectively. Most microalgae with high contents of omega-3 are seawater species, such as Schizochytrium sp., and Nannochloropsis sp. However, freshwater species, for example, Desmodesmus sp., have also been investigated as a source of omega-3 long-chain PUFA, eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids (Fig. 4) [158]. Omega-3 FAs consumption has been associated with fetal development, cardiovascular function, and Alzheimer's disease, thus being a valuable food supplement. As human bodies cannot produce some of these FAs, it is necessary to obtain adequate amounts through food supplements that are usually attended through fish and fish-oil products [159]. However, due to increasing interest in a vegetarian or vegan diet, microalgae could be an alternative source for this food supplement. Moreover, many species of fatty fish also contain mercury contaminants, which could cause neurotoxic effects. Thus, it is recommended for its consumption to be prevented for pregnant or breastfeeding women and young children [84]. Seawater microalgae require a medium with high salt concentration

3.1.1. Green solvents Most solvents used for lipid extraction at a laboratory scale are toxic and not recommended or impracticable to use at large scales such as conventional hexane Soxhlet and Bligh and Dyer. Therefore, in an attempt to avoid the use of highly toxic solvents, green solvents are studied as an alternative. Results of Soxhlet extraction already showed that lipid extracts obtained using ethanol and hexane exhibit similar lipid composition and yields [149]. Also, a recent study suggested that chloroform and methanol in Bligh and Dyer extraction could be replaced by 2-methyltetrahydrofuran and isoamyl alcohol obtained from sugarcane industry residues [151]. Another promising alternative includes supercritical CO2. Supercritical fluid extraction is a promising method because it produces

Fig. 4. EPA, DHA and omega-3 molecules. 456

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4.1. Fatty acid profile of microalgae cultivated in wastewater

that can affect negatively downstream processes such as harvesting, so its application is limited [160]. Furthermore, aiming the integration of microalgae cultivation with effluent treatment, freshwater microalgae is the most viable option once it can be cultured in wastewater, and the use of seawater species would be viable only in coastal areas, where the required medium is abundantly available and transportation cost would be minimum. Therefore, this review focused on the evaluation of freshwater microalgae as a source of unsaturated fatty acids, highlighting PUFAs production. The screening of different microalgae strains’ fatty acid profile is shown in Table 5. The most commonly studied microalgae genera were evaluated, found exclusively in freshwater or both fresh and seawater, and compared to marine microalga Nannochloropsis sp. Botryococcus species show a high concentration of MUFA (59.6% of oleic acid), and both Desmodesmus and Chlorella species are promising PUFA sources, comprising around a third or more than half of total FAs. Furthermore, it was possible to observe that these freshwater species are possible substitutes to omega-3 and -6 production from seawater species. Additionally, it is important to mention that the fatty acid profile can vary for the same microalgae species depending on cultivation conditions or culture medium. For example, Scharff et al. [161] evaluated the photoperiod effect on FA profile, obtaining that longer photoperiods (24:0, 22:2, 20:4) may reduce α-linolenic acid synthesis and induce linoleic acid synthesis, as observed more expressively for C. vulgaris than S. obliquus. On the other hand, Chandra et al. [162] observed that both linoleic and α-linolenic acids content increased along with an increase in light intensity, being a continuous light condition for the optimal photoperiod. The variation of air inlet flow rates did not exhibit significant variations. Calixto et al. [163] evaluated four microalgae species grown in sewage and agro-industrial residues. The authors observed mostly an increase in SFAs content, up to 36%, and different results for PUFAs (69% increase and 62% decrease for different species) when cultivating microalgae in residual water in comparison to synthetic medium (Zarrouk).

Recent researches have focused on lipid production from microalgae associated with effluent treatment, comparing the fatty acid profile obtained using synthetic medium and mainly wastewater streams as a nutrient source. A review of these comparative studies is presented in Table 6. Some species exhibited a meaningful change in specific FAs, but it was not possible to identify similar patterns in the categories (SFA, MUFA, and PUFA). Overall, literature research indicates that growing microalgae in wastewater is more likely to produce lipids with higher SFA content and less unsaturated fatty acids. Fernández-Linares et al. [164] compared the primary fatty acids in C. vulgaris cultivated using treated wastewater with and without the addition of fertilizer. For both strains evaluated, oleic acid content decreased to more than half by adding the fertilizer, linolenic acid increased, but palmitic, stearic, and linoleic acid contents showed contrasting results. Therefore, a fatty acid profile may vary not only by the medium source but also between different strains using the same medium. Moreover, Han et al. [165] compared the fatty acid profile of S. obliquus grown is wastewater with no aeration and aerated with 2% CO2-enriched air. The authors observed, in general, a decrease in SFA content, increase in MUFA, and a slight reduction of PUFAs (mostly 18carbon chain FAs). Although enriching the medium with waste streams may reduce lipid accumulation (Table 2), fatty acid profile will not be necessarily negatively affected. As observed in Table 6, some types of wastewater increased the content of omega-3. For example, Chlorella and Scenedesmus quadricanda, increased C18:3 content almost by three-fold and 36%, respectively, compared to microalgae grown using synthetic medium. Furthermore, lipid productivity could be significantly improved with CO2 injection, which will also be environmentally beneficial.

Table 5 Studies reported in the literature on the fatty acid profile of microalgae. Microalga/FA profile

B. braunii1

B. terribilis2

Chlorella sp.3

C. sorokiniana4

C. vulgaris5

D. brasiliensis6

Desmodesmus sp.7

Nannochloropsis sp.8

S. obliquus9

S. obtusiusculus10

C4:0 C10:0 C12:0 C13:0 C14:0 C14:1 C16:0 C16:1 C16:2 C17:0 C17:1 C18:0 C18:1 C18:1t C18:2 C18:2t C18:3 C18:3t C20:0 C20:1 C20:4 C20:5 C22:0 C22:1 C22:6 SFA MUFA PUFA

0.37 – – – 0.68 – 9.36 0.32 – – 2.68 1.27 59.55 – 7.00 – 11.20 – – 0.55 0.92 2.23 – – 3.88 11.69 63.10 25.21

2.41 – – – 0.38 – 6.27 0.23 – 0.27 0.96 1.28 75.19 – 3.09 – 5.20 – – 0.66 0.57 1.24 – – 2.26 10.60 77.03 12.37

– – 0.51 – 0.69 – 19.03 21.97 – – – 2.35 48.21 – 1.29 – 1.54 – 3.57 0.14 – – 0.12 0.58 – 26.27 70.90 2.83

– – 0.80 – 7.90 12.40 6.20 – 13.0 – – 19.00 – – – – 33.00 – – 3.8 – – – – – nd nd nd

– – 2.11 – 0.86 – 35.77 1.63 – 1.31 8.51 11.35 12.55 – 7.36 – 13.54 4.18 – 0.83 – – – – – 25.08 22.69 52.23

– – 1.76 – 0.70 – 26.19 2.48 – 0.80 8.59 7.05 15.49 – 14.62 – 20.24 2.08 – – – – – – – 36.94 26.56 36.50

– 0.45 14.96 – 7.30 – 18.91 0.46 – 0.65 – 14.66 27.97 – 12.37 – – 1.61 – 0.67 – – – – – 13.98 28.43 57.59

– – – – 6.8 – 31.58 – – – – 3.54 34.48 9.34 4.97 9.24 – – 0.21 – – – 0.65 – – nd nd nd

– – 0.24 0.33 0.21 0.08 27.39 0.70 – 0.76 0.14 11.88 32.08 – 9.08 – 8.11 – – 0.68 – – 0.16 – – nd nd nd

– – – – – – 30.2 7.3 – – 4.0 – 26.2 19.5 – – 12.8 – – – – – – – – nd nd nd

SFA (saturated fatty acid), MUFA (monounsaturated fatty acid) and PUFA (polyunsaturated fatty acid); nd (not determined). 1,2 [34], 3[40], 4[38],.5-7[42].8[39].9[48].10[49]. 457

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Table 6 Comparative studies reported in the literature on the fatty acid profile of microalgae cultivated with a wastewater-enriched medium. Cultivation parameters/FA profile

C12:0 C14:0 C14:1 C16:0 C16:1 C16:2 C16:3 C18:0 C18:1 C18:2 C18:3 C20:0 C20:1 C20:3 C20:4 C20:5 C22:2 C22:6 C24:0 SFA MUFA PUFA UFA

Chlorella1

Chlorella sp.2

Nannochloropsis sp.2

S. dimorphus3

S. quadricanda4

Annular PBR

Erlenmeyer

Erlenmeyer

Bubble column PBR

BBM

5% palm oil mill effluent

f/2

Shrimp farm wastewater

f/2

Shrimp farm wastewater

BG11

Brewery wastewater

BG11

Municipal wastewater

1.0 1.6 0.7 48.5 1.3 – – 12.3 22.4 6.8 3.6 0.7 0.3 0.2 – 0.04 0.04 – 0.4 64.8 nd nd 35.2

0.7 1.3 2.1 38.5 4.0 – – 21.4 6.5 9.8 13.7 0.5 0.3 – – 0.1 – – 0.3 63.6 nd nd 36.4

– 0.5 4.8 14.5 7.1 9.1 – 2.7 19.3 24.9 12.8 – – – – – – – – 17.7 31.2 46.7 nd

– 0.5 0.7 20.8 5.8 3.3 – 6.5 31.4 23.7 5.3 – – – – – – – – 27.8 37.8 32.3 nd

– 5.7 3.6 21.2 29.8 – – 0.1 3.8 1.8 0.7 – 5.4 – – 24.8 – – – 27.0 42.6 27.3 nd

– 3.0 0.6 41.2 36.9 – – 2.6 7.2 1.1 0.7 – 2.5 – – 4.1 – – – 46.8 47.1 5.8 nd

– 0.2 – 28.1 1.0 3.7 1.9 3.4 30.9 11.9 12.4 – – – 3.1 0.3 – 3.1 – 31.8 31.8 36.4 68.2

– 1.2 – 30.2 4.0 2.4 1.8 5.6 31.6 11.0 7.4 – – – 2.2 – – 1.8 – 37.0 35.6 26.4 62.0

– 1.5 – – 0.8 – – 5.3 21.2 13.4 28.9 1.2 0.2 – – – – – – nd nd nd 67.7

– 1.3 – – 3.7 – – – 19.7 1.8 39.4 0.1 0.4 – 1.2 – – – – nd nd nd 66.4

SFA (saturated fatty acid), MUFA (monounsaturated fatty acid), PUFA (polyunsaturated fatty acid), and UFA (unsaturated fatty acid); nd (not determined); PBR (photobioreactor). 1 [166], 2[167], 3[168], 4[169].

4.2. CO2 effect on microalgae lipid accumulation and fatty acid profile

supplementation may increase high-value target compounds in lipid fractions such as omega-3 PUFAs, so its use for microalgae cultivation is not only desirable in an environment point of view, but also to improve product's yield.

Although the increase in CO2 concentration in culture medium increases biomass production and usually also increases total lipid content, studies have approached its impact on fatty acid profile. Carpio et al. [170] evaluated C. vulgaris FAME composition under different concentrations of Fe and CO2. The authors found that increasing CO2 concentration from the air (0.037%) to 2%, SFA content increases; from 16.2 to 69.8% with low Fe3+ concentration, and from 24.4 to 25.6 with high concentration. Consequently, MUFA and PUFA decreases; from 18.4 to 0.0% and 65.5 to 30.2%, respectively, at low Fe concentration; and slightly changes at high concentration. Therefore, CO2 sequestration and lipid accumulation are also influenced by iron and other element's concentration, which may affect drastically the fatty acid profile [171,172]. Nascimento et al. [35] compared fatty acids profiles of C. vulgaris, B. braunii, and B. terribilis, under CO2 concentrations from 2.5 to 20.0%. They also obtained an increase in the palmitic acid of C. vulgaris but no change for Botryococcus strains, as CO2 supplementation increased. However, oleic and linolenic acids concentrations increased for B. terribilis and B. braunii. Bouaid [173] achieved a 20-fold increase in lipid content for Dunaliella salina, with CO2 aeration from 0.01 to 12.0%, with little to none impact on saturated and unsaturated fatty acids content. Moreno et al. [174] compared five different microalgae strains, obtaining different results. For example, for C. vulgaris, it was observed a productivity increase in all categories (SFA, MUFA, and PUFA), when CO2 concentration varied from air to 5%, also increasing total FAs by three-fold. Carvalho and Malcata [175] studied the effect on microalga Pavlova lutheri, obtaining an increase both on SFA content and some MUFA and PUFA as CO2 concentration increased from 0 to 2%. It can be concluded that the effect of CO2 on microalgae fatty acid profile varies among different strains and cultivation conditions. However, it usually results in total lipid content increasing drastically and varying changes in the categories of FAs. Moreover, CO2

5. Applications of oil rich in unsaturated fatty acids As many microalgae exhibit high growth rate and produce TAG or oils, they are a promising feedstock to produce fatty acid esters in substitution to plants. Therefore, most studies have focused on the production of biodiesel, also as an alternative to the negative environmental impacts that soy and palm oil have been associated with. However, some species show fatty acid profiles with potential use for more valuable products, such as the presence of EPA and DHA that are usually found in fatty fish [84]. The production and accumulation of PUFA-rich TAGs using microalgae are advantageous for the food and pharmaceutical industries, mostly, once they exhibit a positive influence on human nutrition and health. Therefore, besides biofuel production, several companies are exploring the possibility for food oil or omega-3 and other bioproducts from microalgae biomass, for instance, Sapphire Energy Inc., Cellana Inc., TerraVia Inc. (recently acquired by Corbion), and Algenol Biotech LLC [176]. Omega-3 consumption have many health benefits. On top of what was previously described, long-chain n-3 PUFA produce anti-inflammatory compounds that reduce the risk of chronic diseases [84]. The low intake may also influence the development of heart disease, stroke and type II diabetes [177], and if provided during embryonic development, it can improve growth performance, as tested in ducks [178]. Furthermore, supplementation with conjugated linoleic acid may cause a reduction in body fat and change FA metabolism in healthy humans [179]. Consequently, studies indicate that the ingestion of FA can be related to coronary heart disease, and also that the consumption of mono- or polyunsaturated oils without trans is indicated [180]. B. braunii strains can accumulate high content of lipids, as shown in 458

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from FAs present in different molecules [189], PUFAs for food and pharmaceutical industries [190], and others [146,191]. Applicability of microalgae is mostly evaluated as biofuel's feedstock, and it has been vastly studied for biodiesel production [192,193] through transesterification reaction [176] usually catalyzed by an acid or a base. Also, this reaction usually exhibits high yields not only due to high TAG content in microalgae lipids, but also to polar lipids, as can be seen on Fig. 5, which can be efficiently converted into biodiesel [194]. Finally, hydrocarbons are another explored constituent of microalgae lipids, which could be converted into biofuels through thermochemical liquefaction [195] or catalytically cracking microalgae lipids into light alkenes (olefins) [196]. Consequently, research has been increasingly focusing on bio-oil production rather than biodiesel once different lipid fractions can be obtained.

Table 1, with TAG consisting mainly of oleic acid (Table 5). This MUFA is typically encountered in olive oil [181], which in turn can reduce the incidence of a major cardiovascular event in people at high cardiovascular risk [182]. Other food supplements include eicosanoids, derivatives of 20-carbon PUFAs [183], which act as inflammatory regulators [184]. Carotenoids are another type of polyunsaturated molecules that are important for human health, such as α and β-carotenes, b-cryptoxanthin, lutein, zeaxanthin, violaxanthin, neoxanthin and astaxanthin [185–187]. They are typically found as pigments in plants and can act as precursors of vitamin A, for example. Other molecules, such as fucoxanthin, can be found in some microalgae species and are of interest for anti-obesity and anti-carcinogenic effects [188]. A summary of different microalgae lipid applications in industry was assembled and is displayed in Fig. 5, such as biodiesel produced

Fig. 5. Different lipid applications from microalgal biomass. 459

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7.47 years for biofuel production and 18.1% internal rate of return; Collota et al. [24] showed through a life cycle analysis, positive environmental impacts in using wastewater and waste CO2; and Slade and Bauen [133] obtained significant cost reductions by using waste streams. As Peng et al. [11] evaluated cost and revenue, showing that nutrients are the major fraction of material costs, which in turn represent 65% of a first-year structure for biodiesel production from microalgae, these results are in agreement. Moreover, results obtained by Rezvani et al. [209] showed that exploring different bioproducts from microalgal biomass, for chemical, food, pharmaceutical, and energy industries, is a vital step towards a large-scale production with CO2 capture from power plants. Consequently, minimizing waste production by integrating microalgae to a biorefinery, while valuing all microalgal components is essential to integrate a circular bioeconomy [210]. A complete techno-economic analysis of microalgae biorefinery integrating wastewater and CO2 in cultivation and multiple byproducts lacks information in the literature. Many studies have attempted to estimate costs, energy demands, and environmental impacts in biorefineries, mainly for biofuels production [211,212]. Table 7 summarizes a few economic analyses found in the literature for microalgae use. Open systems are cheaper systems, but recent research has already demonstrated that closed PBRs may be more advantageous due to higher productivity, as discussed. Additionally, biomass fractionation would increase total revenue, evaluating how to best utilize both primary and secondary metabolites. More recently, microalgae-base bioplastics have been considered as another high-value product that can be biodegradable [143,213]. Therefore, it is a highly-potential biomass feedstock for numerous bioproducts. Besides many economic analysis of a profitable microalgae biorefinery, it is also essential to focus on the imminent problem of water scarcity. As one of the most important commodities on Earth, water valorization should be a priority for society. Studies have already showed that global water footprint of production is mainly due to agriculture (7404 Gm³ y−1), followed by industry (913 Gm³ y−1) and domestic supply (46 Gm³ y−1) [214], with increasing demands from both developed and developing countries [215]. Hence a biomass that could be grown using wastewater exhibits great potential not only as a renewable and sustainable feedstock, but also to assist water treatment to be used for irrigation, which corresponds to the majority of water consumption [215]. Furthermore, its ability to sequester CO2 can be also advantageous to industry as carbon credits, showing both economic and environment benefits.

5.1. Industrial applicability of omega-3 rich lipids Microalgal oil consumption can provide nutritional benefits not only due to omega-3 PUFA intake but also carotenoids [197], thus making it more advantageous compared to fish oil [198]. If not consumed directly, it could also be applied as a food ingredient, increasing the amount of EPA in pasta, for example [199]. Besides marine species that are commonly studied as EPA and DHA sources, other freshwater species can produce high quantities of PUFA, as Scenedesmus, Chlorella, and Chlorococcum [200], which could be suitable for growth in wastewater streams. After strain selection, growth conditions must be determined to optimize biomass and lipid productivities together with PUFA content. Some studies have approached this topic, obtaining that oxygen supply is usually detrimental to PUFA production [201], but bicarbonate combined with nitrogen limitation and alkaline pH stress, as well as inorganic carbon supply, can influence positively long-chain PUFA production [202]. Regarding cultivation systems, photobioreactors still provide superior results than open systems, but Hamilton et al. [214] were able to cultivate a genetically modified diatom in a raceway pond, also obtaining high EPA and DHA concentrations. Chauton et al. [204] evaluated the techno-economic viability of marine microalgae industrial production under various scenarios, and indicate a lower PUFA production cost using flat panel photobioreactors in locations with clear sky conditions. Therefore, there have been some advances in the study of largescale production of marine microalgae rich in EPA and DHA, but literature still lacks research on combining microalgae integration to a biorefinery by using wastes to reduce costs and producing high-added value bioproducts as omega-3 FAs. It can be seen an increasing number of studies evaluating the economic viability and technical feasibility of microalgae growth, by improving and/or developing new technologies for intermediate steps and integrating to wastewater treatment [205,206]. However, the effect of different methods on the chemical stability, such as oxidation of edible oils, requires further investigation [145]. Thus, it is essential to choose among those upstream and downstream processes [207] the best ones for the desired product. Furthermore, to obtain lipids rich in PUFAs that could be commercialized for consumption, processes involving low-temperatures, non-toxic solvents would be recommended. 5.2. A techno-economic perspective of a microalgae biorefinery using waste streams

5.3. Implications of using recycled nutrients for food and feed Integrating microalgae growth with bioremediation in existing plants by using waste streams seems a promising alternative due to several cost-effective outcomes: residues valorization, wastewater treatment, valuable bioproducts, not to mention all environmental benefits of cultivating microalgal biomass. A few studies have already approached this goal, as Xin et al. [150] estimated a payback period of

Although microalgae have been mostly directed for feed and biofuels, economic viability entails more valued products, for applications in food and cosmetic industries, for example. Moreover, capital and operating cost reductions are required. The development of a sustainable process with integrated microalgae cultivation would be most cost-

Table 7 Economic analysis of a microalgae biorefinery. Review study

Economic analysis

Different scenarios revenue

Biodiesel ($/kg) Glycerol ($/kg) 0.7 0.33 Lipids ($/kg) Proteins ($/kg) 0.84 1.23 TAG, Open ponds ($/L) 1.87 Open ponds ($/L) 2.39–2.93 Lipids, Open ponds ($/L) 2.80 Open ponds ($/kg biomass) 0.44–1.98

Biorefinery (200,000 t/y) Fuel production Biofuels production Fuel production Biomass production

References Algae feed ($/kg) Animal feed ($/kg) 0.31 0.31 Sugars ($/kg) Residual biomass ($/kg) 0.90 0.11 TAG, Photobioreactor ($/L) 3.98

Organic fertilizer ($/kg) 0.041

[14] [216] [217] [218]

Lipids, Photobioreactor ($/L) 6.95 Photobioreactor ($/kg biomass) 4.19–11.02

460

[219] [76,133]

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removal from wastewater are Botryococcus, Chorella, and Scenedesmus. These species also showed important fatty acids in their lipid composition, which could be crucial for economic viability. Cultivation is most effective using hybrid systems and flat plate PBRs for PUFA production. Also, lipid extraction obtained using green solvents, specially supercritical CO2 are the best alternatives. However, further research on wastewater-grown microalgae effects on product quality must be assessed before implementation.

efficient if nutrients were recycled from waste, by growing microalgae that can assimilate these molecules. As nutrients are the major influence in material costs, it would not only be advantageous at an environment perspective, but also economical. On the other hand, applicability in food and feed demands a more rigorous evaluation of products quality and safety. Wang et al. [220] have assessed the nutrient recycle between an algal-bacteria combination with activated sludge. It was possible to efficiently reduce COD, nitrogen from ammonia, and TP, while producing Chlorella sp. biomass with higher C/H/N content compared to sludge, that could be used for feed, fertilizer or fuel. Furthermore, an economy of 3.9 $ kg−1 was achieved due to recycle of nutrients from poultry wastewater used to grow Chlorella sp. and Spirulina platensis [221]. A more rigorous study was developed by Moheimani et al. [222], evaluating the pathogen load, nutritional value, and in vitro digestibility of microalgae cultivated on undiluted anaerobic digested piggery effluent. Microalgae could be applied as feedstock for pigs, but are still, in general, inferior to commonly used soybean meal. The pathogen load was within regulatory limits, and nutritional value and digestibility could increase after further biomass processing through fermentation and enzyme treatment. Despite the used microalgal consortium (Chlorella sp. and Scenedesmus sp.) showing great potential, further in vivo studies and feeding trails are needed to elucidate dietary effects, as the authors indicated.

Declarations of interest None. Checklist table Item

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Full-length article (less than 10,000 words) Manuscript All details included. Cover letter Submitted the first version. Layout of paper Minor headings differences (review paper). English, grammar and syntax Yes Title Yes Author names and affiliations Yes Corresponding author Done. Highlights Uploaded as a separate file in the second submission. Graphical abstract yes Copyright yes Referencing style yes Single column yes Logos/emblems etc. yes Embed graphs, tables and figures/other images yes in the main body of the article Figures/Graphs/other images yes Tables yes Line numbering yes Acknowledgements yes Ethics in Publishing Checked carefully by all the authors named on the paper.

5.4. Future work and recommendations This work proposes a critical review of existing research that approaches upstream, and downstream processes involved in microalgae cultivation for lipid production, emphasizing on PUFA. Although substantial advances have been made towards microalgae application on a large scale, there are still improvements to make this biomass competitive in the market. Freshwater species may have a crucial role in viabilizing microalgae cultivation integrated into a biorefinery, to reduce costs and produce high-value bioproducts. However, the influence of using wastewater as a nutrient source in the final product quality must be assessed to guarantee this integration. Furthermore, it is necessary to improve biomass productivity in open systems or develop cheaper photobioreactors, also overcoming contamination issues of wastewater. Finally, a life cycle assessment involving microalgae integration to an existing plant and producing different bioproducts would be interesting for decision-making, to evaluate environment and economical advantages.

Acknowledgments This work was supported by National Council for Scientific and Technological Development (CNPq) grant # 166844/2017-9 and The São Paulo Research Foundation (FAPESP) grants # 2014/10064-9 and 2015/20630-4. The authors thank Espaço da Escrita – Pró-Reitoria de Pesquisa – UNICAMP – for the language services provided.

6. Conclusions Microalgae biomass composition indicates a wide range of possible applications, such as biofuels, food and feed. Concerning biodiesel production, technical and economic analyses suggest that this feedstock is not yet a viable competitor to petrol diesel. Therefore, a different approach towards microalgae use viability is: (1) to reduce cultivation costs by growing microalgae in sustainable media, improving its photosynthetic efficiency by consuming CO2; and (2) to produce oils with a composition of high-value co-products, such as PUFAs. Based on several studies, mostly on a laboratory scale and some on a pilot scale, microalgae cultivation could be integrated into a biorefinery. Possible beneficial outcomes are the reduction of GHG emission by capturing CO2, bioremediation by wastewater treatment and the production of different bioproducts (biofuels, cosmetic, pharmaceutical, fertilizers, etc.). Strain selection, growth conditions, harvesting, and lipid or other constituent extraction, are steps that require attention when balancing economic and ecologic viability. Also, a wide range of possible microalgae applications is interesting to utilize all biomass and open the market range. The data evaluated in this review showed that promising Chlorophyta species for CO2 biofixation, lipid production and nutrient

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