Algal biorefinery to value-added products by using combined processes based on thermochemical conversion: A review

Algal Research 47 (2020) 101819

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Review article

Algal biorefinery to value-added products by using combined processes based on thermochemical conversion: A review

T

⁎⁎

Liangliang Fana, Haili Zhanga, Jingjing Lia, Yunpu Wangb, Lijian Lengc, , Jun Lia, Yanhong Yaoa, ⁎ Qian Lua, Wenqiao Yuand, Wenguang Zhoua, a

School of Resources, Environmental & Chemical Engineering, Key Laboratory of Poyang Lake Environment and Resource Utilization, Ministry of Education, Nanchang University, Nanchang 330031, China b Engineering Research Center for Biomass Conversion, Ministry of Education, Nanchang University, Nanchang 330047, China c School of Energy Science and Engineering, Central South University, Changsha, Hunan 410083, China d Department of Biological and Agricultural Engineering, North Carolina State University, Raleigh, NC 27695, USA

A R T I C LE I N FO

A B S T R A C T

Keywords: Algal biomass Algal components Gasification Liquefaction Pyrolysis Biofuels

Thermochemical processes, including gasification, liquefaction, and pyrolysis, are promising technologies for algal conversion. Gasification is effective to convert algal biomass into fuel gases while liquefaction and pyrolysis are favorable for the production of bio-oil with low molecular weight and biocrude with high energy density, respectively. To understand the role of algal components (proteins, lipids, and carbohydrates) on thermochemical conversion processes, this paper reviews the properties of biofuels from the thermochemical conversion of algal components and their model compounds. The characteristic fingerprints of algal components differ from one another. Consequently, the thermochemical conversion of the total algal biomass results in heterogeneity of the biofuels. The unfavorable nitrogenous compound production also leads to resource and energy losses, which are the critical bottleneck of algal biorefinery. As such, this review tackles some combined processes. The combination of the hydrothermal liquefaction of algal biomass and the hydrothermal gasification of an aqueous fraction shows potential for applications that improve fuel gas production. Lipid extraction combined with thermochemical residue conversion contributes to an increase in total oil yield. Protein extraction combined with thermochemical residue conversion decreases the risk of nitrogenous compound contamination in bio-oil and increases the recovery of value-added protein-derived products. Protein and lipid extraction before thermochemical conversion should be further explored to maximize the exploitation of multiple value-added products from algal biomass.

1. Introduction The world still largely relies on nonrenewable resources, such as fossil fuels, which can be exhausted in the near future [1]. Greenhouse gas emissions derived from the consumption of nonrenewable resources have been heavily implicated in global warming. Therefore, the resource crisis accompanied with the corresponding negative environmental consequences, has prompted the exploration of renewable resources for sustainable development. A promising renewable alternative to conventional resources is algal biomass. The growth rate and photosynthetic efficiency of algae are higher than those of traditional crops, and the substantial capacity of sequestering carbon dioxide of the former is higher than that of the latter [2]. They can grow in fresh

or sea water and do not compete with arable land [3]. The three main valuable chemical components of algae are proteins, lipids, and carbohydrates. Algal proteins are an attractive food, feed, and health product because of their nutritional characteristics [4]. Algal lipids, mainly consisting of triglycerides, phospholipids, free fatty acids, and glycolipids, exhibit high potential for application that replace conventional fuels and are generally used for biodiesel production through extraction and transesterification [5]. Algal carbohydrates mainly consist of cellulose, starch, glucose, and polysaccharides and are a desirable feedstock for the production of value-added chemicals, such as furans, ethanol, and acetone [6]. The last decades have witnessed an intensive development of various biorefinery technologies for the recovery and utilization of algal biomass and its constituents. Among

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Correspondence to: Wenguang Zhou, School of Resources, Environmental & Chemical Engineering, Key Laboratory of Poyang Lake Environment and Resource Utilization, Ministry of Education, Nanchang University, 999 Xuefu Ave., Nanchang, Jiangxi Province 330031, China. ⁎⁎ Correspondence to: Lijian Leng, School of Energy Science and Engineering, Central South University, Changsha, Hunan Province 410083, China. E-mail addresses: [email protected] (L. Leng), [email protected] (W. Zhou). https://doi.org/10.1016/j.algal.2020.101819 Received 29 October 2019; Received in revised form 24 January 2020; Accepted 25 January 2020 2211-9264/ © 2020 Elsevier B.V. All rights reserved.

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C + 2H2 ↔ CH 4

these technologies, thermochemical processes have been widely explored because of their high efficiency and economic viability [7]. The amount and properties of chemical components in algae play important roles in conversion efficiency and biofuel properties. However, reviews on the thermochemical conversion of different algal components or their model compounds remain limited. Thus, the characteristics of carbohydrate-, lipid-, and protein-derived biofuels from thermochemical processes, including gasification, liquefaction, and pyrolysis, are reviewed in the present study to help screen optimal processes for the recovery of multiple value-added products from algae. The advantages and challenges of gasification, liquefaction, and pyrolysis are also analyzed. The key bottleneck of the industrial application of algalderived products is weighing the cost of algal conversion against its benefits. Therefore, algal biomass value should be comprehensively exploited. However, any single rough thermochemical conversion of algal biomass challenges resource loss. Process integration biorefinery concepts for algal conversion are required for optimizing the exploitation of algal-derived value-added products. This review describes some of the combined processes based on thermochemical conversion, including hydrothermal liquefaction combined with hydrothermal gasification, lipid extraction combined with thermochemical residue conversion, protein extraction combined with thermochemical residue conversion, and protein and lipid extraction before thermochemical conversion, for advanced energy/resource recovery from algae.

ΔH = + 75 kJ/mol

(5)

5. Water gas shift reaction

CO + H2 O → CO2 + H2

ΔH = +41 kJ/mol

(6)

Algae are usually cultivated in water, and the harvested algal biomass contains a large amount of water, requiring an energy-intensive process to dry the biomass before conventional gasification [11]. In this case, hydrothermal gasification (HTG), a type of biomass gasification where water is used as the medium at high temperatures and pressures, is proposed to mitigate energy use for drying because it allows the direct gasification of wet biomass [12]. Among HTG processes, supercritical water gasification (SCWG), a type of biomass gasification where supercritical water (374 °C and 22.1 MPa) is used as the medium, has been considered as the most promising because of its high gasification efficiency and high-heating-value gas production [13]. Supercritical water acts as a nonpolar fluid resembling a gas, exhibiting some new properties, such as strong dissolving ability and high oxidizability. Biomass in supercritical water readily undergoes bond breakage, resulting in the high production of fuel gases rich in H2 and CH4 [14]. Water-gas shift reaction and methane reaction enhanced by supercritical water are two critical factors that promote H2 and CH4 formation. The H2 yield and gasification efficiency can exceed 100% according to the following formulas because the gasification agent, water, is involved [11].

2. Thermochemical processes for biofuels

Gas mass flow rate out × 100 Algal mass flow rate in

(7)

Moles of hydrogen in the gas product × 100 Moles of hydrogen in algae

(8)

Gasification efficiency (%) = 2.1. Gasification for fuel gases 2.1.1. Principle of gasification Gasification is an effective technology to convert biomass into gaseous fuels. A gasifying agent, such as air (oxygen), steam, or CO2, is generally used to convert carbonaceous polymers of biomass at high temperatures (800 °C–1000 °C) [7] to valuable combustible gases, such as CO and H2, with some light hydrocarbon gases as co-products. In brief, the reaction mechanisms of biomass gasification varying with gasifying agents can be illustrated with Eq. (1):

H2 yield (%) =

biomass + gasifying agent

2.1.2. Gasification of algal components and their model compounds The gasification, especially SCWG, of glucose and cellulose, which are the typical constituents of algal carbohydrates, has been widely studied. During carbohydrate SCWG, CO2 and H2 are the dominant gas products (accounting for 70%–90% of the total gas product) because of water gas shift reaction (6) and important reactions as follows [18,20]:

→ H2 + CO2 + CO + hydrocarbon gases + tar + H2O + char

Table 1 shows the characteristics of gas products from algal gasification under different technologies. The gasification efficiency and H2 formation of SCWG, especially with alkali catalysts, are possibly higher than those of other technologies. However, the carbon efficiency that reflects the mass percentage of carbon converted from the initial biomass towards product gases remains relatively low.

(1)

Biomass gasification generally proceeds in four stages, namely, drying, devolatilization (pyrolysis), oxidation, and reduction [8–10]. At the drying stage (100 °C–200 °C), moisture in biomass is released. At the pyrolysis stage (200 °C–700 °C), organic matters are volatilized from biomass, resulting in the formation of tar (mainly heavy organic compounds), water vapor, and solid char. Some gaseous products, such as CO2, CO, H2, and hydrocarbon gases, are obtained at this stage. At the oxidation stage (700 °C–1500 °C), combustible substances, including char carbon and organic volatiles, are oxidized into CO, CO2, and H2O, and this process is accompanied with large heat production. Reduction reactions generally occur at approximately 800 °C–1100 °C in an oxygen-free atmosphere, yielding syngas (CO and H2) and CH4. Five major reactions illustrated as follows are involved at this stage.

C6 H12 O6 + 6H2 O → 6CO2 + 12H2

ΔH = −131.4 kJ/mol

(2)

2. Bounded reaction

C + CO2 ↔ 2CO

ΔH = –172.6 kJ/mol

(3)

3. Shifted reaction

CO2 + H2 ↔ CO + H2 O

ΔH = –42 kJ/mol

CH 4 + 2H2 O → CO2 + 3H2

(10)

C6 H12 O6 → 3CO2 + 3CH 4

(11)

In most cases, CO2 yield is higher than H2 yield (average 20 mmol/g biomass vs. 15 mmol/g biomass) [21–23], indicating that partial oxidation reactions possibly occur during SCWG. Fortunately, the use of some catalysts, such as Ca(OH)2 and Na2CO3 [20] can inhibit CO2 production. Over 90% of carbon efficiency can be achieved during carbohydrate gasification [18,21,24]. However, gasification also results in a large volume of aqueous phase, containing some carbonaceous matters such as acids, acetones, and furans, whose isolation and recovery are difficult [20,25]. The direct gasification of algal lipids has been rarely reported. However, glycerol is sometimes used as an algal lipid model compound for further studies because it forms the backbone of lipids. The gasification of glycerol as a lipid-derived compound in supercritical water produces a gas product rich in H2 (molar fraction of over 50%), especially at high temperatures (> 500 °C) [13,26]. High H2 production can be attributed to the steam reforming of glycerol (C3H8O3 → 3CO + 4H2) [27]. Guo et al. [28] also stated that the glycerol pyrolysis

1. Water–gas reaction

C + H2 O → CO + H2

(9)

(4)

4. Methane reaction 2

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Table 1 Characteristics of fuel gas from gasification of algal biomass and algal components/model compounds under different gasification technologies. Feed

Microalgae Microalgae Microalgae Microalgae Microalgae

Gasifying agent

(Chlorella vulgaris) (Chlorella vulgaris) (Spirulina) (Chlorella vulgaris) (Nannochloropsis gaditana)

Microalgae (Chlorella Vulgaris) Macroalgae (Cladophora glomerata) Glucose Glycerol Glycerol Glycine Leucine Glutamic acid a b c

Air Air O2 Steam SCWc

SCW SCW SCW SCW SCW SCW SCW SCW SCW SCW

Conditions

Fuel gas composition (%)

900 °C, 10 wt% 5ZnO/5NiO –CaO 700 °C 1000 °C 850 °C, 0.0432 g/min of steam flow 663 °C, 24 MPa 663 °C, 24 MPa, 0.6 wt% K2CO3 663 °C, 24 MPa, 0.3 wt% Na2CO3 500 °C 460 °C, 27 MPa 650 °C, 28 MPa, 16 wt% Ni/AC 600 °C, 25 MPa 600 °C, 25 MPa, 0.5 wt% K2CO3 526 °C, 25 MPa 526 °C, 25 MPa, 0.5 wt% NaOH 663 °C, 24 MPa 663 °C, 24 MPa 663 °C, 24 MPa

H2

CO

CH4

C2-C3

42.86 19.1 48.2 ~45.4 41.9 55.4 52.0 50 28.3 27.3 50 55 57.5 68.9 78.5 49.5 57.7

8.66 22.9 9.8 ~17.2 1.8 0.2 0 32 6.7 13.9 32 1 19.2 1.4 0 1.9 0

19.64 18.7 9.1 ~9.4 19.9 13.7 17.9 5 13.6 16.0 5 5 3.4 1.2 1.6 23.8 10.0

/ / 0.1 ~7.4 10.8 6.7 7.1 3 5.4 4.2 3 9 0.54 0.08 0 6.4 4.1

CEa (%)

GEb (%)

Reference

/ 52.9 103.0 ~58 77.0 77.6 86.0 66 ~30 90.5 / / 64.2 68.6 42.0 63.4 75.2

82.12 73.8 / / 81.9 92.7 97.4 / / / 66 100 75.6 103.8 56.8 80.2 93.2

[10] [15] [16] [17] [11]

[13] [17] [18] [13] [19] [11]

CE: Carbon efficiency, is defined as the mass percentage of carbon converted from the initial biomass towards product gases. GE: Gasification efficiency, is defined as ratio between the mass of product gases and that of the feedstock. SCW: Supercritical water gasification, is a type of biomass gasification where supercritical water (374 °C and 22.1 MPa) is used as the medium.

proteins in algal biomass inhibit gasification correlated to free radical scavenging effect induced by amino acid anions [33]. The presence of protein/amino acids, especially glycine and alanine, contributes to the reduction of the gasification efficiency of carbohydrate- and lipid-derived compounds by increasing the coke yield [13,33]. Nitrogen-containing gases in fuel gas lower the heating value of gas products; otherwise, additional energy is needed for gas separation and purification. Intensive energy used in SCWG may be another drawback of algal biomass conversion. In this process, a large amount of energy is required for water preheating, especially the high temperature (around 600 °C) maintained for gasification reactions. The heat used to raise the temperature to 600 °C can outweigh the total energy of biomass when the amount of water is over 80% (w/w) of biomass [34]. Unfortunately, a high water-to-algal biomass ratio (> 10, water content > 90%) is generally used in SCWG to ensure gas quality and gasification efficiency and to consider operability. The high water content in the feedstock increases not only the energy input for biomass conversion but also the cost input for end-product recovery. A long processing time at high temperatures also increases energy consumption. The quenching of exit gas and tar with a high temperature also causes the loss of energy and is suggested to be developed to offset biomass preheating.

and steam reforming of intermediate products are the main routes of H2 production. In addition, some organic molecules, such as acetic acid, acetaldehyde, hydroxyacetone, and acrolein, can be formed through hydrothermolysis during glycerol SCWG [26]. A relatively high gasification efficiency (90%–110%) and H2 yield during glycerol SCWG indicates that algal lipid conversion through SCWG is a promising strategy [19,29]. Moreover, the addition of alkali catalysts [13,19] can significantly increase the GE. Protein gasification in supercritical water exclusively produces nitrogen-containing gases, such as N2 and NH3, in addition to H2, CO, CO2, and CH4. H2 accounts for 50%–80% of the gas composition from protein/amino acid gasification [11,30]. The gas composition from protein gasification varies with the profiles of amino acids in an algal protein. For example, alanine gasification results in a high CH4 yield because of its methyl groups [31]. Other amino acids with a high content of carboxylic groups, such as glutamic acid, can promote CO and CO2 production. Xu et al. [30] achieved a nitrogen gasification efficiency of 95.8% and stated that nitrogen elements are mainly converted to N2. However, a low carbon efficiency is one of the main barriers of protein gasification. Caputo et al. [11] observed that gasification resistance follows the order of glycine > leucine > glutamic acid. Furthermore, the yield of soluble organics in the water phase is high, contributing to a low gas yield [31]. The characteristics of the gas products of the SCWG of algal components/model compounds with various conditions are summarized in Table 1. In terms of carbon efficiency, glucose seems to be the most promising compound. Kruse et al. [31] also demonstrated that the gasification of carbohydrates is faster than those of lipids and proteins. Therefore, gasification can be a promising technology for gas production from algae with high carbohydrate contents [32]. Glycerol and amino acid gasification results in a relatively high H2 production. However, a low carbon efficiency remains unfavorable. The loss of nitrogen source is also a waste of energy.

2.2. Liquefaction for biocrude 2.2.1. Principle of liquefaction Among thermochemical processes, hydrothermal liquefaction (HTL) is generally applied to biomass liquefaction. HTL is a depolymerization process that converts the carbonaceous matters of biomass into liquid products in the presence of a solvent at moderate temperatures below 400 °C and high pressures of up to 20 MPa. The resultant liquid product from HTL generally contains some soluble macromolecules and small molecules (usually hydrocarbons, amines, aldehydes, acids, and esters) and is defined as biocrude. The HTL of algal biomass significantly reduces oxygen and nitrogen contents and increases carbon content in biocrude. HTL facilitates the direct conversion of wet algal slurry to biocrude without investment on drying. Water in the HTL serves as an organic solvent and hydrogen donator. It can act as an acid or base catalyst, facilitating the hydrolysis of the organic fractions of algal biomass. HTL involves three major steps, namely, hydrolysis, decomposition, and repolymerization [35]. In hydrolysis, the processing temperature increases gradually, and biomass begins to hydrolyze into

2.1.3. Advantages and challenges of gasification In comparison with other thermochemical processes, algal biomass gasification shows potential for the efficient conversion of carbonaceous matters into fuel gases containing most of the biomass carbon energy. Consequently, solid residue is dominated by ash. Furthermore, the development of SCWG permits the direct gasification of wet algal sludge and avoids an energy-intensive pre-drying process. However, 3

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Fig. 1. Potential reaction pathways for HTL of algal biomass [39]. (a) hydrolysis; (b) decomposition; (c) dehydration; (d) polymerization; (e) deamination; (f) Maillard reaction; (g) decarboxylation; (h) Aminolysis; (i) cyclization; (j) halogenations; (k) dehydrohalogenation; (l) condensation + pyrolysis.

to a high biocrude yield because of the free hydrogen radicals released from hot-compressed solutions, which promote the hydrocracking of macromolecules into small molecules. Nonpolar solvents are believed to positively affect the decreasing oxygen content and facilitate the separation of an organic fraction without additional solvent extraction [47].

some fragments such as carbohydrates, lipids, peptides and their derivatives. In decomposition, these fragments are further degraded into small molecules or oligomers via a series of reactions such as dehydration, deoxygenation, and decarboxylation. Decomposition also contributes to the formation of water and CO2 [36]. However, some highly active radicals can also be produced during biomass decomposition and they easily undergo repolymerization to form char and macromolecular compounds. The identified compounds in biocrude are limited because only a portion of biocrude is within the temperature range in which GC/MS operates. The detected compounds are generally dominated by ketones, alcohols, phenols, nitrogen heterocycles, and saturated fatty acids with a heating value ranging from 30 MJ/kg to 40 MJ/kg [37,38]. Fig. 1 shows the potential reaction pathways during the HTL of algal biomass. The main components of algae are initially decomposed to the corresponding monomers and then converted to their end products. During monomer decomposition, decarboxylation and deamination are dominant, releasing oxygen and nitrogen as small molecules, such as CO2, amines, acids, and ketones. Furthermore, the interaction between algal components occurs, producing some complicated heterocyclic compounds. Several organic solvents have been exploited to assist liquefaction because of their attractive properties, such as a high dissolving capacity and a possible high reactivity to react with biomass intermediates, to enhance biocrude yield and quality [40–42]. These organic solvents include polar solvents, such as ethanol [43], glycerol [44], ethylene glycol [45], isopropyl alcohol [45], and acetone [46], and nonpolar solvents, such as n-heptane, toluene, and anisole [47]. Table 2 shows the product yield from the HTL of algal biomass with different organic solvents. Polar organic solvents, such as alcohols, typically contribute

2.2.2. Liquefaction of algal components and their model compounds Carbohydrate liquefaction is usually applied to yield some platform chemicals, such as 5-hydroxymethyl-2-furaldehyde (HMF) and carboxylic acids (formic acid, acetic acid, lactic acid, and levulinic acid) [53,54]. HMF formation involves the protonation of C-2-OH to stabilize the furanic ring, and followed by dehydration. Carboxylic acids can be formed through a retro-aldol reaction, dehydration, and keto-enol and benzylic rearrangements [55]. Yin et al. [54] stated that the formation of HMF and carboxylic acids from cellulose are strongly affected by the final pH of solutions. When the final pH remains higher than 7, the alkaline pathway is dominant, resulting in the primary production of carboxylic acids. At a final pH lower than 7, the acidic route occurs, contributing to the main production of HMF. However, under acidic conditions, an increase in acid concentration can accelerate the decomposition of HMF to carboxylic acids [53,56]. The near-complete conversion [57] and high carbon yield of platform chemicals (up to 60%) [53] can be obtained from the HTL of C6 sugars. However, the conversion efficiency of some polysaccharides, such as cellulose, is low (< 10 wt% biocrude yield) [54,58] because of their stubborn structures. Therefore, the highly efficient hydrolysis of carbohydrate polymers to monosaccharides is a key step of value-added chemical production. Cao et al. [57] demonstrated that in addition to HMF and 4

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Table 2 Product yield from hydrothermal liquefaction of algal biomass and algal components/model compounds with different solvents. Feed

Microalgae (Chlorella)

Microalgae (Chlorella pyrenoidosa) Microalgae (Spirulina) Microalgae (Tetraselmis sp.)

Solvent

Water Ethyl acetone Acetone Ethanol Methanol Ethanol/water (5:2, v/v) Ethanol/water (1:1)

Microalgae (Chlorella pyrenoidosa)

Isopropyl alcohol/water (1/8) Acetone

Microalgae (Spirulina)

1,4-dioxane

Egg albumin Soy protein Sunflower oil Glucose Starch Soy protein Sunflower oil Cornstarch

Water

Water

Conditions

Product yield (wt%)

275 °C, 60 min, biomass/solvent (1/ 5, w/v)

280 °C, 60 min, 30% dry biomass 300 °C, 45 min, biomass/solvent (1/ 10, w/v) 350 °C, 30 min, biomass/solvent (1/ 9, w/w) 290 °C, 60 min, biomass/solvent (2.5/16, w/v) 377 °C, 20 min, biomass/solvent (3/ 40, w/v) 350 °C, 60 min, biomass/solvent (1/ 9, w/v)

350 °C, 60 min, 15 wt% of biomass

Reference

Bio-crude

Water phase and gas

Solid residue

20.3 26.15 40.16 62.70 68.34 57.3 59.5

/ 49.34 30.13 31.80 26.53 33.3 35.2

/ 24.51 30.13 5.50 5.13 9.4 5.3

[48]

35.4

/

/

[45]

80.2 (including water phase) 57

4.0 (only gas)

20.7

[46]

18

25

[41]

~18 ~18 ~80 ~3 ~6 ~30 ~90 ~15

~79 ~72 ~17 ~77 ~74 ~66 ~10 ~66

~3 ~10 ~3 ~20 ~20 ~4 ~0 ~18

[51]

[49] [50]

[52]

pyrans, which are easily dissolved in aqueous phase.

carboxylic acids, water can be produced during the HTL of glucose. The formation of a significant amount of the water phase is also a vital issue for polysaccharide liquefaction [59]. Algal-derived lipids can be directly used as transport fuels and the conversion of lipids through HTL is rarely investigated. However, some lipid-derived compounds, such as vegetable oil and fatty acids, are usually used as algal lipid model compounds for further study. Teri et al. [52] selected sunflower oil as an algal lipid model compound for HTL and showed that fatty acids are the main compounds of biocrude. The HTL of lipids by using alcohols, such as methanol and ethanol, can directly yield biodiesel [60,61]. The decarboxylation and hydrogenation of fatty acids to hydrocarbons through hydrothermal catalytic cracking are widely studied [62–64]. During the hydrothermal catalytic conversion over Pt/C, the saturated fatty acids undergo decarboxylation to form n-alkanes; while the unsaturated fatty acids undergo hydrogenation before decarboxylation [62]. Fu et al. stated that either water or fatty acid molecules serve as the hydrogen donor during the hydrothermal catalytic conversion [64]. The catalytic cracking of fatty acids over HZSM-5 generally produces aromatic hydrocarbons as the main products because of the strong aromatic-shape selectivity of HZSM-5 [63]. A high amount of biocrude can be produced from the HTL of proteins, indicating the feasibility of protein liquefaction. Cyclic nitrogencontaining compounds are dominant in biocrude. Amino acids with phenolic/aromatic structures also result in phenol and aromatic production, which can be enhanced by catalysts, such as Ru/C, under hydrogen pressure [65]. However, the specific pathways of protein conversion through HTL are still largely unknown because of the complicated structures of proteins and various amino acid profiles. NH3 is also a major product of protein liquefaction. Over 60 mol% of NH3 can accumulate in the aqueous phase [65]. Table 2 presents the yields of products from the HTL of algal components/model compounds. It can be observed that lipids are more feasible to be qualified to biocrude than proteins and carbohydrates. However, the aqueous phase yield from the HTL of carbohydrates is relatively high. Water production from intermolecular and intromolecular dehydration reactions between HTL intermediates is the main factor to the high aqueous phase yield. In addition, some carbonaceous matters of algal biomass are converted to acids, furans, and

2.2.3. Advantages and challenges of liquefaction The major advantage of HTL lies in the direct conversion of wet biomass without drying, thereby avoiding energy losses. HTL also generates a high biocrude yield under mild conditions. The biocrude with a high energy content exhibits a high potential to alter petroleum and aviation fuel [66]. With sub-/super-critical water as a reaction medium, the mass transfer of algal biomass is enhanced. However, some challenges, including organic solvent recovery, biocrude extraction, and further upgrading processes, inhibit the HTL processing of algal biomass. Although the cosolvent-assisted HTL of algal biomass is a promising strategy, the recovery of organic solvent is still energy intensive. After liquefaction, biocrude usually needs to be extracted with additional organic solvents, such as dichloromethane (DCM) [67], ethyl acetate [44], chloroform [68], and diethyl ether [69]. The additional solvent extraction increases the energy input for biocrude recovery. Watson et al. [70] screened several solvents, including acetone, DCM, and toluene for the extraction of biocrude from the HTL of algae and calculated the net energy production. The net energy outputs of acetone-, DCM-, and toluene-extracted biocrude are −2223.4 MJ, −1516.9 MJ, and − 2024.6 MJ, respectively. The negative net energy gain indicates the high energy consumption of HTL process and biocrude recovery. Bio-crude is usually viscous and should be upgraded before use. The viscidity of biocrude is partly derived from the large formation of oligomers (such as dimers and trimers) [71]. Oligomers dissolved in extraction solvents cannot be detected through GC/MS and are usually disregarded by researchers. The high boiling point (> 538 °C) [48] and high molecular weight (up to 1000 Da) [38] of algal biocrude also indicate the existence of oligomers during HTL. Upgrading of nitrogenous compounds, especially N-heterocyclic compounds, such as carbazoles, indoles, pyridines, pyrroles, and nitriles, is also challenging. Although denitrogenation can occur under catalytic conditions, the efficiency of HTL remains low [72]. In addition, some homogeneous catalysts used for biocrude upgrading are difficult to be separated and recycled from the mixture.

5

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conventional pyrolysis. However, in addition to the above factors, product yield is also affected by many other complicated factors, such as pyrolysis reactors, operating ways, biomass loading weight, and cooling system. Therefore, product yields from different studies vary significantly.

2.3. Pyrolysis for bio-oil 2.3.1. Principle of pyrolysis Pyrolysis is a promising technology to efficiently convert organic matters of algal biomass into liquid fuels at temperatures of 400 °C–600 °C in the absence of oxygen. The obtained liquid product from pyrolysis mainly consists of small molecular chemicals and is defined as bio-oil. The bio-oil from algal pyrolysis is relatively different from the biocrude from algal HTL. HTL generally produces higher liquid yield than pyrolysis [73]. HTL biocrude has higher energy density and storage stabilities than pyrolysis bio-oil [73]. However, the molecular weight of pyrolysis bio-oil (280–360 Da) is much lower than that of HTL biocrude (700–1330 Da) and the percentage of low boiling point (< 400 °C) fraction in pyrolysis bio-oil is much higher than that in HTL biocrude [74]. Algal biomass is more feasible for pyrolysis than lignocellulosic biomass because of its more stable properties of algal-derived bio-oil [75]. Furthermore, the pyrolysis of algal biomass yields higher bio-oil yield than that of lignocellulosic biomass [76]. In brief, four main stages constitute pyrolysis, namely, dehydration for moisture release, primary decomposition for bio-oil production, secondary decomposition for gas production, and repolmerization for char formation. These stages, especially the last three, are not strictly ordered, and they usually co-occur. The pyrolytic products in bio-oil from algal biomass mainly consist of hydrocarbons, carboxylic acids, esters, alcohols, furans, cyclopentanones, phenolics, and nitrogenous compounds [77,78], which are derived from the decomposition of algal components and the interaction between components. In general, reactions related to pyrolysis include dehydration, cracking, decarboxylation, decarbonylation, cyclization, isomerization, and repolymerization [79,80]. Depending on the heating rate, pyrolysis can be categorized into slow and fast pyrolysis. Slow pyrolysis is generally used for solid fuel (biochar) production at a relatively low temperature (300 °C–500 °C) and a low heating rate (0.1–1 °C/s). The long residence time correlated with a low heating rate also provides sufficient time (450–550 s) for a secondary repolymerization reaction, maximizing solid fuel yield. However, fast pyrolysis generally occurs at 500 °C–800 °C at a heating rate of 10 °C–200 °C/s and has gained increasing attention because of its high efficiency on the conversion of biomass into bio-oil, which has the potential to produce value-added chemicals. A technology named microwave-assisted pyrolysis for biomass conversion has gained wide interest because of its advantages over conventional pyrolysis including higher energy efficiency, noncontact volumetric heating, higher heating rate, higher tolerance to particle size, quick start and stop, and more even heating. Table 3 presents the algal-derived product yield under different pyrolysis technologies. In general, high liquid and gas yields are obtained from fast pyrolysis and favored at high temperatures. The char yield of microwave-assisted pyrolysis is lower than that of

2.3.2. Pyrolysis of algal components and their model compounds The glycoside bond cleavage, ring-opening, and rupture of branched chains are three main reactions that occur during carbohydrate pyrolysis, resulting in the production of pyrans, furans, acids, ketones, and aldehydes. Pyranose rings exclusively exist in glucose. Glucose pyrolyzed bio-oil constituents are dominated by furans, which possess more stable structures than pyrans do. However, during cellulose pyrolysis under appropriate conditions, levoglucosan yield is the highest among pyrolysis products, which may be attributed to the more susceptible cleavage of glycosidic linkages than carbon–carbon bonds within glycosidic units. The order of levoglucosan formation is the pyrolysis of polysaccharides > oligosaccharides > disaccharides > monosaccharides [87]. Intermolecular and intramolecular dehydration reactions also commonly occur during pyrolysis, and water is then produced. Long-chain hydrocarbons and phenols can also be obtained because of the chain-aliphatic structures of lipopolysaccharides and phenolic structures of lignin [86]. Among these pyrolysis compounds, furans are generally produced at low temperatures (approximately 200 °C) [88], whereas phenols are formed at high temperatures (over 500 °C) [89]. Abundant active hydroxyl groups in carbohydrates easily undergo condensation reactions, contributing to char formation. The wide varieties and high oxygen content of bio-oil constituents from carbohydrate pyrolysis impede the industrial application of bio-oil. As a possible solution, a catalytic process with zeolites effectively upgrades the carbohydrate-derived oxygenates to aromatic and aliphatic hydrocarbons [90]. In terms of aromatic formation, the carbon yield from the zeolite cracking of carbohydrates ranges from 20% to 30% [90,91]. Pyrolysis effectively converts lipids into hydrocarbons because of the abundant aliphatic structures of lipids. Triglycerides are typical lipid compounds and generally undergo a two-step cracking mechanism during pyrolysis [92]. The process includes the primary breakage of CeO bonds of a carboxylic group to fatty acids and the secondary cracking of the primary products to short-chain organics including hydrocarbons, whose short olefin contents can be further converted to aromatics through Alder–Diels reactions. During the cracking of fatty acids, unsaturation favors the cracking of CeC bonds adjacent to the C]C bonds [93]. Pyrolysis results in a high liquid yield, ranging from 45 wt% to 80 wt%, because of the simple chain structure of lipids [86,94,95]. Catalysts, such as zeolites, can produce a large gasolinerange fraction with high aromatic selectivity because of enhanced cracking and aromatization by catalysts [91,92].

Table 3 Product yield from pyrolysis of algal biomass and algal components/model compounds under different pyrolysis technologies. Feed

Microalgae (M. aeruginosa S. japonica) Microalgae (Chlorella) Microalgae (Chlorella sp.) Microalgae (Chlorella sp.) Microalgae (Scenedesmus) Microalgae (Chlorella vulgaris) Glucose Soy protein Castor oil Algae-derived carbohydrate Algae-derived lipid Algae-derived protein

Pyrolysis technology

Temperature (°C)

Fast pyrolysis in fluid bed Fast pyrolysis in fixed bed Fast pyrolysis in fixed bed Fast microwave-assisted pyrolysis Slow microwave-assisted pyrolysis Slow pyrolysis in tube furnace Slow pyrolysis in fixed bed Fast pyrolysis in fixed bed

500 350 450 550 569 450 600 /

Fast pyrolysis in fixed bed

475

6

Product yield (%)

Reference

Bio-oil

Char

Gas

23.7 40.9 55 57 28.6 (Oil) + 20 (Aqueous) 31 (Oil) + 27 (Aqueous) 28.5 + 5.46 (Aqueous) 44 34 64 28.56 67.76 38.61

~20 37.1 30 27 ~24 30 22.33 ~30 ~25 ~5 35.57 15.56 24.77

~56 22.0 15 16 ~26.5 12 43.71 ~26 ~41 ~31 35.87 16.68 36.62

[81] [78] [82] [83] [84] [74] [76] [85]

[86]

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the energy and resource recovery from biomass and reduce the influence of inhibitory factors, thereby offsetting the high input cost. The combined processes mainly include HTL combined with HTG, lipid extraction combined with thermochemical residue conversion, protein extraction combined with thermochemical residue conversion, and cascading process of protein extraction, followed by lipid extraction and thermochemical remnant conversion.

Aromatic/phenolic and N-heterocyclic compounds are dominant in liquid products from protein pyrolysis. The former are mainly derived from the cleavage of side chains of amino acids with aromatic/phenolic structures [96]. The latter are formed from the decomposition of heterocyclic amino acids and the cyclization of aliphatic amino acids [97]. Some active amino acids can undergo condensation and dehydration reactions with their neighboring amino acids to form heavy cyclic compounds, such as dialkyl substituted 2,5-diketopiperazines (DKPs) [98]. The complex heterocyclic structures in nitrogen-containing compounds are not only difficult to be converted into aromatics but also favorable to coke formation during catalytic conversion, resulting in nitrogen retention in solid residue [98]. Among the algal compounds, algal protein yields the lowest aromatic hydrocarbons during catalytic pyrolysis [91]. NH3 is the best form of nitrogen because it can be recycled as fertilizers for algal cultivation. However, its formation during pyrolysis is strongly affected by the amino acid profiles of proteins. For example, the nitrogen of leucine can be converted into NH3, whereas the nitrogen of proline prefers to remain in solid residue [99]. Table 3 shows that algal carbohydrates and proteins are more difficult to be converted into bio-oil than lipids and may decrease the conversion efficiency of algal biomass. The bio-oil yield of the pyrolysis of glucose is likely higher than that of the pyrolysis of algal carbohydrates with a complex structure, indicating that the first decomposition of polysaccharides to monosaccharides is a key step to improve the conversion efficiency.

3.1. Hydrothermal liquefaction combined with hydrothermal gasification During the HTL of algal biomass, a large volume of aqueous fraction ranging from 20 wt% to 80 wt% of algal biomass is also obtained and hard to be recycled as fuels [45,102]. The disposal of aqueous waste containing 35–40 wt% of carbon and over 50 wt% of nitrogen of the algal biomass [103,104] causes energy loss and environmental pollution. Therefore, studies have focused on the reuse and recycling of the aqueous fraction from the HTL of algae in view of economic and environmental perspectives. HTL combined with HTG for algal biorefinery has been developed to maximize the exploitation of algal energy and resource. In brief, the aqueous fraction from the HTL of algal biomass is processed using HTG to produce fuel gases. Chemical compounds in an aqueous fraction are mainly composed of acids, ketones, and nitrogenous compounds, which are derived from the hydrolysis of carbohydrates and proteins [105]. Approximately 20%–80% of acetic acid varying with algal species can be obtained in aqueous products because of the high hydrophilia of acetic acid [105]. Amides and 2-pyrrolidinone derivatives dominate nitrogenous compounds, indicating the occurrences of complex reactions between proteins and other algal components or their derivatives [106,107]. The HTG of aqueous products can result in an almost complete gasification of organics as a result of the production of mainly H2 and CH4 because of gas–water shift reaction, and methane reaction [14,105]. Cherad et al. [14] proposed a novel biorefinery concept summarized in Fig. 2. The combination of HTG and HTL makes the best use of aqueous organics and produces sufficient amount of hydrogen for the complete hydrotreatment of biocrude from the HTL of algae. Mineral remnants left in the post-HTG aqueous provide proper nutrients for algal cultivation, facilitating the recycling of algal resources. Although the direct use of aqueous phases from HTL for algal cultivation has been widely investigated [108,109], some inhibitory compounds, such as phenolics, N-heterocyclic compounds, heavy metals, and other toxic substances, inhibit algal growth [110]. However, HTG consumes most of the “inhibitory compounds” to fuel gases, making the pretreated aqueous phase more favorable to algal cultivation. However, the corresponding techno-economic analysis of the combined process should be further investigated.

2.3.3. Advantages and challenges of pyrolysis The main advantage of algal pyrolysis depends on the efficient conversion of algal biomass into bio-oil, which can be partly used as transport fuels or further upgraded through catalytic conversion. During pyrolysis, the primary vapors can be promptly released from biomass during pyrolysis (especially fast pyrolysis) and quenched in separated containers, reducing secondary complex reactions. Bio-oil is obtained through volatilization and then quenching. Although solvent extraction could be required to separate aqueous phase from the bio-oil, the filtration for the separation from solid residue can be avoided. Furthermore, the compounds in bio-oil are generally small molecules that are conducive to further refining. However, the development of algal pyrolysis is impeded by the drying of algae, upgrading of nitrogenous compounds, mitigating of toxic gases, and decreasing energy efficiency. Importantly, the high moisture content of algae after being harvested impedes pyrolysis and predrying is difficult to avoid. However, drying technologies, such as direct thermal drying and partial mechanical dewatering [100], require conspicuous energy input and incur capital costs, which are some key challenges for algal pyrolysis conversion to biofuels. Nitrogenous compounds seriously affect bio-oil quality. Zeolite catalysts show the catalytic effect of reducing the nitrogen content of bio-oil [101]. However, its aromatic yield is still much lower than that from lipids and carbohydrates because of the stable structure of N-heterocyclic compounds, such as indole and pyridine [91]. A considerable amount of hydrogen cyanide, an extremely toxic gas, can be produced during a catalytic pyrolysis process [101]. The capture and treatment of toxic gases remain challenging. The low energy transfer efficiency of conventional heating is also a burden to algal conversion. Although microwave-assisted pyrolysis has been developed for algal conversion because of its advantages over conventional pyrolysis, the development of a continuous fast microwave-assisted pyrolysis system coupled with a continuous feeding system, stirring, and fast char discharging remains to be explored.

3.2. Lipid extraction combined with thermochemical conversion 3.2.1. Lipid extraction from algal biomass A substantial amount of lipids ranging from 25% to 75% of dry algal biomass demonstrates the potential of biodiesel production from algae Algal biomass

HTL

Bio-crude

Aqueous

HTG

Cultivation

3. Combined processes based on thermochemical conversion

Upgrading

H2 Hydrotreating

Mineral remnants

Fig. 2. Combination of HTL and HTG for optimizing energy recovery and resource recycling from algal biomass (Adapted from Cherad et al. [14]). HTL: Hydrothermal liquefaction, is a thermal depolymerization process that converts biomass into crude-like oil under moderate temperature and high pressure; HTG: Hydrothermal gasification, is a type of biomass gasification where water is used as the medium at high temperatures and pressures.

The high input cost, the loss of energy and resource, and the inhibitory effect of nitrogenous compounds are three main barriers to the development of the thermochemical conversion of algal biomass. Therefore, some combined processes have been proposed to enhance 7

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Table 4 Yield and fatty acid profile of crude lipid extracted from algal biomass using different methods. Feed

Extraction

Crude lipid yield (wt%)

Fatty acids profiles

Reference

Pretreatment

Medium

Microalgae (Pavlova sp.)

None

44.7

15.6 wt% total yield

[122]

Microalgae (Tetraselmis striata M8) Microalgae (Chlorella vulgaris)

None None Bead-beating Free nitrous acid (2.19 mg/L), 48 h None

Ethyl acetate/ methanol, 3 h n-Hexane, 15 h n-Hexane, 100 h SCCO2a, 6 h n-Hexane

13.5 18.5 17.9 21.9

7.2 wt% total yield 9.8 wt% total yield 15.7 wt% total yield /

[123]

[Bmim][CF3SO3]/ Methane Liquid CO2/methane Liquid CO2/methane Liquid CO2/methane SCCO2, 60 °C, 60 min

19.0

29.5% of C16:0, 37.9% C18:2, 11.8% C18:3, and 7.9% C18:0 dominated the fatty acids 3.6 wt% total yield 4.1 wt% total yield 4.1 wt% total yield 0.013 g/g dry biomass with dominant C16:0 (25.9%), C18:1 (52.7%), and C18:2 (18.7%)

Microalgae (Scenedesmus sp.)

Microalgae (Chlorococcum sp.)

a

None Ultrasonication Microwave None

6.1 5.7 12.1 0.058 g/g dry biomass

[113] [120]

[124]

SCCO2: Supercritical CO2, is a fluid state of CO2 where it held at or above its critical temperature and critical pressure. Natural gas

Solid waste

3.2.2. Thermochemical conversion of residues With lipid extraction, a large amount of residue biomass concentrated with proteins and carbohydrates is retained. In view of the maximum utilization of biomass resources, thermochemical conversion provides a promising method for the energy recovery of lipid-extracted residues. Few studies have investigated the gasification of lipid-extracted residues. Nevertheless, lipid-extracted residues are believed to be a good source of syngas, especially hydrogen production through gasification [125]. However, protein content is prominent in algal residues after lipid extraction and can inhibit gasification efficiency because of free radical scavengers induced by amino acids [33]. Biocrude yield from the HTL of lipid-extracted residues is lower than that from the total algal biomass because of the following HTL efficiency order: lipids > proteins > carbohydrates [51]. However, Vardon et al. [74] indicated that the higher heating value of biocrude from the HTL of defatted microalgae and total microalgae is similar. Biocrude from the HTL of lipid-extracted residues is mainly composed of cyclic nitrogenates and cyclic oxygenates, which should be upgraded prior to being used as transport fuels. Zhu et al. [126] proposed a system combining the HTL of lipid-extracted residues and further upgrading of fuels, as illustrated in Fig. 3. Briefly, the lipid-extracted residue slurry is introduced into a reactor for HTL, generating biocrude, gas, and solid residue as the products. The organic fraction is extracted from the biocrude for further upgrading, such as hydrocracking and hydrotreating; while the gas product from the HTL process and upgrading process is recycled for organic upgrading. The proposed process is energy-saving and environmentally friendly. However, the hydrogen amount produced from the lipid-extracted residue HTL is insufficient for the post-upgrading. A steam reforming process and a water-gas shift process are required to increase the hydrogen content. Furthermore, catalysts for the upgrading process are conducive to improve the upgrading efficiency. Nevertheless, the results from the techno-economic analysis of this process reveal that the minimum fuel selling price may range from $2.07 to $7.11/gal gasoline-equivalent [126].

Steam

Offgas Hydrogen generation H2

LAR

Hydrothermal liquefaction

Wastewater

Bio-oil

Hydrotreating

Offgas

Heavy oil

H2

Hydrocracking

Liquid fuels

Fig. 3. Block flow diagram of hydrothermal liquefaction and upgrading of lipidextracted algal residues [126]. LAR: Lipid-extracted algal residues, are the residue materials of algal biomass after lipid extraction.

as a promising technology [111]. Lipids can be extracted through several methods, such as solvent extraction [112], ionic liquid extraction [113], and supercritical CO2 [114]. One of the challenges for lipid extraction is the thick cell envelope. The assistance of press [115], milling [116], ultrasound [117,118], nozzle spraying [119], microwave, acid/ base hydrolysis, and enzymes [111] facilitates cell disruption and consequently enhances lipid extraction. Viner et al. [120] stated that microwave is the most promising among several cell disruption methods in terms of lipid yield. Fatty acids, such as C18:1, C18:2, C18:3, C16:0, and C16:1, depending on extraction conditions and algal species are dominant in the extracted lipid fraction. Several extraction methods for the production of lipids with fatty acid profiles are summarized in Table 4. The proper mixing of organic solvents facilitates lipid release. Although supercritical CO2 is a solvent-free and environmentally friendly method for lipid extraction, its extraction efficiency is low. One of the advantages of lipid extraction is that the wet algal slurry can be directly used as feedstock without predrying because the obtained oil product can be easily separated from the water phase through organic extraction. High oil yield can be obtained under mild reactions (low temperature or room temperature). With proper extraction methods, such as cyclic extraction with organic solvents, 90% lipid recovery can be obtained [121], leaving the lipid-extracted algal residues concentrated with proteins and carbohydrates. Furthermore, lipid extraction facilitates cell envelope disruption, which is conducive to the further conversion of lipid-extracted residues.

3.2.2.1. Steam. In terms of lipid-extracted residue pyrolysis, bio-oil is dominated by protein- and carbohydrate-derived compounds, such as N-heterocyclic compounds, nitriles, amines, ketones, aldehydes, alcohols, furans, and phenols [127]. Furthermore, Wang et al. [128] indicated that some complex nitrogenous compounds with a large molecular weight (up to 1200 Da) exist in pyrolyzed bio-oil, which may be attributed to the complex reactions between protein and sugars, such as Maillard reaction, which is one of the affecting factors of Nheterocyclic compound production. The possible interactions between protein and sugar are illustrated in Fig. 4. The basic Maillard reaction is the reaction of amino groups with aldehyde or ketone groups. The 8

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Fig. 4. Decomposition of the products from the Maillard reaction between protein and glucose [85].

process is the low energy input for the optimal pyrolysis of lipidextracted residues because of low temperature for maximum oil production of protein and carbohydrate pyrolysis [85,86].

complex Maillard reaction products (MRPs) undergo further decomposition to form N-heterocyclic compounds with high oxygen and nitrogen contents, such as pyrazine, pyrrole, pyrazol, piperazine, piperidine, azetidine, pyrimidin, and so on [85]. However, the knowledge on the decomposition mechanism of MRPs and interactions between protein and glucose remains limited. The effects of monosaccharide type distribution in algal carbohydrates and amino acid profile in algal proteins on Maillard reactions need to be further studied. The oil yield from lipid-extracted residue pyrolysis is generally lower than that from the total biomass [74] because lipid-extracted residues have a low content of lipids, which exhibit a higher liquefaction index than those of proteins and carbohydrates [86]. However, the total oil yield of the combined process is higher than that of the direct pyrolysis of total algal biomass [127]. A detailed comparison between the two processes is depicted in Fig. 5. Furthermore, the lipid extraction process can destroy the cell structure of algae, facilitating the further decomposition of biomass remnants during pyrolysis [129]. Another advantage of the combined

3.3. Protein extraction combined with thermochemical conversion 3.3.1. Protein extraction from algal biomass Algal proteins with large quantity and good quality are more advantageous than conventional protein sources, such as soy protein, egg white protein, and animal protein [130,131]. Several types of algal protein, including concentrates, isolates, hydrolysates, and bioactive peptides, can be obtained depending on the refining degree [132]. The well-balanced amino acid profiles of algae establish bioactive peptides with various permutations, which are the main contributors to biofunctionalities of algal proteins [133]. However, algal protein in its unprocessed raw form without extraction is difficult to digest and assimilate. Several methods, including physical processes, chemical processes, and enzymatic hydrolysis, have been applied to extract algal 9

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products, such as recalcitrant N-heterocyclic compounds, and the undesirable reactions between proteins and carbohydrates. Lipid- and carbohydrate-derived compounds are the major constituents of biofuels from the thermochemical conversion of protein-extracted residues. The gasification of protein-rich biomass generally yields a low gas yield, especially compared with that of carbohydrate-rich biomass [31]. This is because proteins in the biomass are important resistance to gasification [11]. Proteins hinder gas production through two pathway [31]: (1) Protein gasification proceeds a longer time than carbohydrate gasification; (2) Proteins and their derivatives disturb the decomposition of carbohydrates. Samiee-Zafarghandi et al. [32] also stated that an increase of carbohydrate content in algal biomass results in an increase in hydrogen yield because of the fact that proteins hinder hydrogen production. Although the gasification of protein-extracted residues needs to be further explored, it can be deduced that the gasification of protein-extracted residues shows more promising prospect than that of algal biomass in terms of gasification efficiency and gas yield. Parimi et al. [141] showed that the biocrude yield from the HTL of protein-extracted residues is lower than that from the original algal biomass because of the high content of carbohydrates with recalcitrant structures in the residual biomass. However, a high gas yield with a greater proportion of H2 and CO is obtained in the HTL of the residues, partly because lipids and carbohydrates are more favorable to gasification than proteins. Garcia-Moscoso et al. [142] proposed flash hydrolysis under mild subcritical water conditions (< 240 °C) for algal biorefinery. The process enables > 60 wt% of the total nitrogen content to be released as a protein dissolved in the aqueous faction and most of the carbon to be concentrated as energy-dense biofuel intermediates in the solid fraction. In this process, excess energy used for the separation of protein and biofuels can be exempted. However, further refining/ upgrading processes are required for the conversion of biofuel intermediates into transportation fuels. Compared with the pyrolysis of the total algal biomass, the pyrolysis of protein-extracted residues can produce a higher yield of oil phase with a high carbon content [143], indicating that protein ingredient is unsuitable for biofuel production. Moreover, protein extraction reduces lower sulfur content in bio-oil from algal residues [143]. The pyrolysis of protein-extracted residues also shows an advantage of promoting lipid decomposition by carbohydrate-derived compounds [85].

Algal biomass

Lipid extraction

Direct pyrolysis

LAR

Pyrolysis

Pyrolysis oil

Lipid

Total oil

Higher oil yield

Pyrolysis oil

Total oil

Fig. 5. Comparison between lipid extraction combined with pyrolysis of lipidextracted algal residues and the direct pyrolysis of the whole biomass. LAR: Lipid-extracted algal residues, are the residue materials of algal biomass after lipid extraction.

proteins. Physical processes, such as mechanical grinding and osmotic shock, followed by aqueous extraction slightly influence the protein properties and structures but obtain a relatively low extraction efficiency. Therefore, physical processes are generally used as auxiliary strategies for the disruption of the tough cell wall, which is conducive to protein extraction by further chemical or enzymatic treatment [134]. Some novel physical treatment technologies, such as ultrasound pretreatment and pulsed electric field, which effectively reduces the processing time, have also been developed to disrupt cell [135] and improve protein extraction [136]. Chemical processes involving the use of acid or alkali reagents generally result in a high protein yield (60%–80%) [135,137] because they effectively break the bonds between proteins and other algal components, facilitating the release of proteins. Enzymatic hydrolysis is more environmentally friendly and safer than chemical processes in producing peptides as the main products, which exhibit some biofunctionalities, such as antioxidative activity, antihypertensive activity, anticoagulant activity, antiproliferation activity, and immune-stimulant activity [138]. The proteolytic enzymes used for algal hydrolysis can be divided into gastrointestinal proteases, microbial enzymes, and exogenous enzymes [139]. Temperature and pH are the main factors affecting enzyme activity, further influencing the hydrolysis efficiency of algal protein. Fractionation and separation are required to obtain target bioactive peptides. During the thermochemical conversion of algal biomass, the obtained nitrogenous compounds not only inhibit the conversion efficiency of other components but also cause a wastage of resources and an increase in investment for biofuel refining. Therefore, thermochemical conversion after protein extraction remarkably reduces the influence of nitrogenous compounds and provides an important strategy of obtaining biofuels and food/feed ingredients from algal biomass. Furthermore, the exploitation of some novel technologies with a low cost and a high efficiency for protein extraction is vital. Although enzymatic hydrolysis is efficient and environmentally friendly, it may not be commercially acceptable. However, the combination of enzymatic pretreatment and chemical extraction, which can significantly increase protein yield (> 70%) [140], should be further explored. After protein extraction, the cell disruption of algal biomass is also triggered. Consequently, protein-extracted algal residues mainly composed of lipid and carbohydrate becomes capable of thermochemical conversion.

3.4. Cascading biorefinery processes for protein and biofuel recovery from algae The direct conversion of proteins through thermochemical conversion affects the conversion efficiency and challenges the loss of nitrogen energy. The oil yield produced by lipid extraction under mild conditions is higher than that by direct thermochemical conversion. Thus, both lipid extraction and protein extraction before thermochemical conversion are progressive for algal biorefinery in according with the principle of value maximization. Muñoz et al. [144] proposed an integrated route of algal biomass processing to various valuable products. The processing route is cascaded by protein extraction, followed by lipid extraction and remnant pyrolysis, as illustrated in route (1) in Fig. 6. During the cascading process, 10.2% of soluble protein and 14.0% of lipid based on the total biomass weight are obtained. Furthermore, the remnant pyrolysis produces 33.2% of bio-oil, which is lower than that of the total biomass because of high content of stubborn carbohydrate existing in the remnant. Although the results need to be further optimized, this study provides an idea for the comprehensive conversion of algal biomass. Proteins are difficult to be completely extracted and can inevitably contaminate bio-oil from residual biomass. Therefore, the reduction of these compounds remains a critical target in future research in terms of improving protein extraction efficiency and bio-oil quality. Furthermore, in the biorefinery concept, each separate step of the cascading process should be optimized to increase the costeffectiveness of algal-derived products. The recalcitrant structure of

3.3.2. Thermochemical conversion of residues Biofuels from the thermochemical conversion of protein-extracted residues can eliminate the contamination of unfavorable nitrogen 10

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Algal biomass

Protein extraction Soluble protein 10.2 ± 6.9% (70% of total protein)

Biomass/water (1/16) Solubilization: pH 11, 150 rpm, 13 min Centrifugation: 4400 rpm × 15 min De-protein biomass 89.8 ± 4.5%

Lipid extraction

Lipid 14.0 ± 0.7%

Biomass/petroleum ether (1/14), 16 h

Dried at 40 °C for 1 h

Spent biomass 75.8 ± 3.4%

Hydrothermal liquefaction

(1)

Hydrothermal gasification (2)

Remnant pyrolysis 500 °C Fig. 6. Cascading processing of algal biomass for value-added foods and biofuels [144].

carbohydrates inhibits the efficiency of pyrolysis. Thus, the first HTL of carbohydrate-rich residues to monosaccharide-rich paste and then HTG (See route [2] in Fig. 6) may be a promising conversion route. Other integrating models, such as “lipid extraction followed by protein extraction and then thermochemical conversion of residues” should also be explored.

the algal exploiting value. Nevertheless, the prospective and most promising process is the cascading of protein and lipid extraction, followed by the thermochemical conversion of the carbohydrate-rich residues for value-added products.

CRediT authorship contribution statement 4. Conclusions

Liangliang Fan: Conceptualization, Formal analysis, Investigation, Methodology, Writing - original draft, Writing - review & editing, Visualization. Haili Zhang: Formal analysis, Investigation, Writing review & editing. Jingjing Li: Formal analysis, Investigation, Writing review & editing. Yunpu Wang: Formal analysis, Methodology, Writing - review & editing. Lijian Leng: Conceptualization, Methodology, Writing - review & editing, Visualization. Jun Li: Conceptualization, Investigation, Writing - review & editing. Yanhong Yao: Conceptualization, Investigation, Writing - review & editing. Qian Lu: Conceptualization, Investigation, Writing - review & editing. Wenqiao Yuan: Conceptualization, Writing - review & editing. Wenguang Zhou: Conceptualization, Funding acquisition, Project administration, Supervision, Visualization, Writing - review & editing.

Several thermochemical technologies for algal biomass conversion were introduced, and the characteristics of biofuels from different algal components and their model compounds were reviewed. The gasification of carbohydrate generally yields a higher amount of gas product, especially hydrogen, than those of lipids and proteins. Meanwhile, lipids are more feasible to be converted to liquid fuel through HTL and pyrolysis than proteins and carbohydrates. The advantages and challenges of the thermochemical conversion processes, including gasification, HTL, and pyrolysis, were concluded. The gasification shows high efficiency to convert most of the biomass carbon energy into fuel gases, leaving solid residue dominated by ash; while HTL and pyrolysis are promising strategies to convert algal biomass into liquid fuels. Furthermore, the main advantage of HTG and HTL lies in the direct conversion of algal slurry without drying. The main challenges include the high input cost, the loss of energy and resource, and the production of unfavorable nitrogenous compounds during the thermochemical conversion of the total biomass. Some combined algal biorefinery processes, including HTL combined with HTG and lipid/protein extraction combined with thermochemical residue conversion, amplify

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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This work was supported by the National Natural Science Foundation of China (Nos. 51906096, 51668044, 51808278 and 21766019) and Key Research and Development Program of Jiangxi Province (Nos. 20171BCB23015, 20171BBG70036, 20181BBH80004, and 20171BBF60023). Declaration of author contributions Wenguang Zhou and Liangliang Fan proposed the conception of the work; Liangliang Fan, Wenguang Zhou, and Lijian Leng designed the framework of this article; Wenqiao Yuan, Jun Li, Yanhong Yao, and Qian Lu provided suggestions for the design of the article framework; Liangliang Fan wrote this manuscript; Haili Zhang, Jingjing Li, and Yunpu Wang participated in the analysis and interpretation of data; All authors participated in the revision or edition of the manuscript. The paper was reviewed and approved by all authors prior to submission. Statement of informed consent, human/animal rights No conflicts, informed consent, or human or animal rights are applicable to this study. References [1] J. Asomaning, S. Haupt, M. Chae, D.C. Bressler, Recent developments in microwave-assisted thermal conversion of biomass for fuels and chemicals, Renew. Sust. Energ. Rev. 92 (2018) 642–657. [2] Q. Xie, M. Addy, S. Liu, B. Zhang, Y. Cheng, Y. Wan, Y. Li, Y. Liu, X. Lin, P. Chen, R. Ruan, Fast microwave-assisted catalytic co-pyrolysis of microalgae and scum for bio-oil production, Fuel 160 (2015) 577–582. [3] M.F. Demirbas, Biofuels from algae for sustainable development, Appl. Energ. 88 (2011) 3473–3480. [4] M. Francavilla, M. Franchi, M. Monteleone, C. Caroppo, The red seaweed Gracilaria gracilis as a multi products source, Mar. Drugs 11 (2013) 3754–3776. [5] J.-Y. Lee, C. Yoo, S.-Y. Jun, C.-Y. Ahn, H.-M. Oh, Comparison of several methods for effective lipid extraction from microalgae, Bioresour. Technol. 101 (2010) S75–S77. [6] Y.A. Castro, J.T. Ellis, C.D. Miller, R.C. Sims, Optimization of wastewater microalgae saccharification using dilute acid hydrolysis for acetone, butanol, and ethanol fermentation, Appl. Energ. 140 (2015) 14–19. [7] W.-H. Chen, B.-J. Lin, M.-Y. Huang, J.-S. Chang, Thermochemical conversion of microalgal biomass into biofuels: a review, Bioresour. Technol. 184 (2015) 314–327. [8] P. McKendry, Energy production from biomass (part 1): overview of biomass, Bioresour. Technol. 83 (2002) 37–46. [9] P. McKendry, Energy production from biomass (part 3): gasification technologies, Bioresour. Technol. 83 (2002) 55–63. [10] A. Raheem, G. Ji, A. Memon, S. Sivasangar, W. Wang, M. Zhao, Y.H. Taufiq-Yap, Catalytic gasification of algal biomass for hydrogen-rich gas production: parametric optimization via central composite design, Energ. Convers. Manage. 158 (2018) 235–245. [11] G. Caputo, M. Dispenza, P. Rubio, F. Scargiali, G. Marotta, A. Brucato, Supercritical water gasification of microalgae and their constituents in a continuous reactor, J. Supercrit. Fluid. 118 (2016) 163–170. [12] D. Elliott, L. Sealock Jr, Chemical processing in high-pressure aqueous environments: low-temperature catalytic gasification, Trans. Inst. Chem. Eng.. 74 (1996) 563–566. [13] A.G. Chakinala, D.W.F. Brilman, W.P.M. van Swaaij, S.R.A. Kersten, Catalytic and non-catalytic supercritical water gasification of microalgae and glycerol, Ind. Eng. Chem. Res. 49 (2010) 1113–1122. [14] R. Cherad, J.A. Onwudili, P. Biller, P.T. Williams, A.B. Ross, Hydrogen production from the catalytic supercritical water gasification of process water generated from hydrothermal liquefaction of microalgae, Fuel 166 (2016) 24–28. [15] A. Raheem, V. Dupont, A.Q. Channa, X. Zhao, A.K. Vuppaladadiyam, Y.-H. TaufiqYap, M. Zhao, R. Harun, Parametric characterization of air gasification of Chlorella vulgaris biomass, Energ. Fuel. 31 (2017) 2959–2969. [16] A. Hirano, K. Hon-Nami, S. Kunito, M. Hada, Y. Ogushi, Temperature effect on continuous gasification of microalgal biomass: theoretical yield of methanol production and its energy balance, Catal. Today 45 (1998) 399–404. [17] F. Safari, O. Norouzi, A. Tavasoli, Hydrothermal gasification of Cladophora glomerata macroalgae over its hydrochar as a catalyst for hydrogen-rich gas production, Bioresour. Technol. 222 (2016) 232–241. [18] I.-G. Lee, S.-K. Ihm, Catalytic gasification of glucose over Ni/activated charcoal in supercritical water, Ind. Eng. Chem. Res. 48 (2009) 1435–1442. [19] S. Guo, L. Guo, C. Cao, J. Yin, Y. Lu, X. Zhang, Hydrogen production from glycerol by supercritical water gasification in a continuous flow tubular reactor, Int. J.

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