Fermentative hydrogen production using algal biomass as feedstock

Renewable and Sustainable Energy Reviews 51 (2015) 209–230

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

Fermentative hydrogen production using algal biomass as feedstock Ao Xia a, Jun Cheng a,n, Wenlu Song b, Huibo Su c, Lingkan Ding a, Richen Lin a, Hongxiang Lu a, Jianzhong Liu a, Junhu Zhou a, Kefa Cen a a

State Key Laboratory of Clean Energy Utilization, Zhejiang University, Hangzhou 310027, China Department of Life Science and Engineering, Jining University, Jining 273155, China c COFCO Nutrition and Health Research Institute, Beijing 100020, China b

art ic l e i nf o

a b s t r a c t

Article history: Received 18 August 2014 Received in revised form 8 May 2015 Accepted 26 May 2015

Hydrogen is considered as an ideal alternative to fossil fuels due to its high energy density by mass and clean combustion product. Using anaerobic bacteria to ferment biomass and produce renewable hydrogen is receiving increased attention. Aquatic algal biomass, which can be sourced from natural algal bloom or mass cultivation, is considered as a promising substrate for hydrogen fermentation. This paper reviews the recent developments in fermentative hydrogen production from algal biomass, with the main focus on hydrogen production potential and its current technological state. The stoichiometric hydrogen yields of algal biomass in dark fermentation are predicted based on the theoretical contents of monosaccharides from carbohydrates and glycerol from lipids in biomass. Hydrogen yields of algal biomass by dark fermentation can be improved by using efficient pretreatments at optimized biomass carbon/nitrogen ratios with domesticated hydrogenproducing bacteria as the inoculum. The effluent of dark fermentation, which is rich in volatile fatty acids, should be used for the production of biofuels and biochemicals to further improve the energy efficiency and economic feasibility of hydrogen fermentation. & 2015 Elsevier Ltd. All rights reserved.

Keywords: Algae Hydrogen Fermentation Methane Anaerobic digestion Energy production

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stoichiometric potential of dark hydrogen production from algal biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Metabolism of carbohydrates in dark fermentation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Metabolism of proteins in dark fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Metabolism of lipids in dark fermentation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Calculation of stoichiometric hydrogen production potential of biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Components of algal biomass and stoichiometric hydrogen production potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hydrogen production from algal biomass through dark fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Hydrogen production from model chemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Reactors for hydrogen fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Hydrogen fermentation from microalgal biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Hydrogen fermentation from macroalgal biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dark fermentation followed by photo fermentation and anaerobic digestion to enhance energy conversion from algal biomass . . . . . . . . . . . 4.1. Comparison of single-stage anaerobic digestion and dark fermentation from algal biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Subsequent photo fermentation for hydrogen co-generation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Subsequent anaerobic digestion for methane co-generation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Dark fermentation as a platform for the production of biofuels and biochemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5. Impurities in biogas. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

210 210 210 211 212 212 213 214 214 216 216 221 221 221 223 225 225 225

Abbreviations: AF, anaerobic filter; ATP, adenosine triphosphate; COD, chemical oxygen demand; CSTR, continuous stirred tank reactor; DHAP, dihydroxyacetone phosphate; DW, dry weight; HPB, hydrogen-producing bacteria; HRT, hydraulic retention time; LCFA, long-chain fatty acid; MPB, methane-producing bacteria; NADH, reduced nicotinamide adenine dinucleotide; PKP, phosphoketolase pathway; PPP, pentose phosphate pathway; TAG, triacylglycerol; UASB, up-flow anaerobic sludge bed; VFA, volatile fatty acid; VS, volatile solids. n Corresponding author. Tel.: þ 86 571 87952889; fax: þ 86 571 87951616. E-mail address: [email protected] (J. Cheng). http://dx.doi.org/10.1016/j.rser.2015.05.076 1364-0321/& 2015 Elsevier Ltd. All rights reserved.

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5.

Efficient hydrogen fermentation from algal biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Hydrogen fermentation of algal biomass at optimized components. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Challenges of fermentative hydrogen production for large-scale applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Potential of fermentative hydrogen production from algal biomass in China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction The extensive utilization of non-renewable fossil fuels has led to serious energy crisis and environmental problems [1–3]. Hydrogen is considered as an ideal alternative to fossil fuels because of its high energy density by mass (higher heating value: 142 kJ/g) and clean combustion product (H2O) [4–6]. Hydrogen can be produced from many conventional processes, such as water electrolysis and steam reforming. Nevertheless, these processes are highly energy intensive and not environmentally friendly [4,7,8]. Renewable hydrogen production from biomass by hydrogen-producing bacteria (HPB) by biological anaerobic dark fermentation is receiving increased attention because of its energy saving, environmentally friendly, and carbon-neutral characteristics [9–13]. The choice of biomass feedstock is a crucial issue in biofuel production [14]. Biofuels may be derived from land-based crops, such as maize and sugarcane. The technologies for cultivation, harvesting, and biofuel conversion of land-based crops are mature. However, biofuels derived from land-based crops have drawn criticisms, due to the competition of food production and large consumption of fresh water and fertilizer [15,16]. In contrast, aquatic algae, which can be classified as either microalgae (e.g., Chlorella, Chlamydomonas, and Arthrospira) or macroalgae (e.g., Laminaria, Ulva, and Gelidium) based on their morphology and size [17–22], may offer promising options for the biofuel production because of the following reasons. Firstly, biofuel yields from algae in same cultivation area are 10–100 times higher than those from land-based crops because of their short biomass doubling time (as short as 3.5 h) and high productivities [up to 26,300 t dry weight (DW)/km2/yr] [11,18,23–28]. Secondly, algae do not need arable land for mass cultivation because they are aquatic species [19,29,30]. Thirdly, algal biomass contains little or no lignin, which enables easy hydrolysis of the biomass for subsequent hydrogen fermentation [17,20]. Hydrogen production by dark fermentation using algae as substrates has attracted considerable attention in recent years [10,31–37]. However, comprehensive review on this issue is limited. Furthermore, to our knowledge, the stoichiometric hydrogen production potential of complex biomass, such as algal biomass, has not been reported in the literature. Less than 1/3 of energy in glucose can be converted to hydrogen in dark fermentation, whereas more than 2/3 of energy remains in the dark fermentation effluent in the forms of soluble metabolite products (SMPs), including volatile fatty acids (VFAs; e. g., acetate and butyrate) and alcohols (e.g., ethanol) [38]. Further conversion of the SMPs to biofuels and biochemicals can significantly improve the energy efficiency and economic feasibility of hydrogen fermentation [39]. This paper focuses on the discussion of hydrogen production based on the monomers derived from biomass, with a particular attention for algal biomass. The theoretical hydrogen potential of algal biomass is comprehensively discussed, and the current state of hydrogen fermentation technology is evaluated. Furthermore, the challenges associated with algal hydrogen fermentation are highlighted. The detailed objectives of this paper are to (1) analyze

225 225 226 226 227 227 227

the metabolic pathways and theoretical yields of hydrogen production from the monomers of organic components (e.g., carbohydrates, proteins, and lipids) derived from algal biomass during dark fermentation, (2) discuss the effects of pretreatments on hydrogen production from algal biomass during dark fermentation, (3) compare the hydrogen production via dark fermentation and methane production via anaerobic digestion using algae as substrates, (4) discuss the further conversion of SMPs to biofuels and biochemicals, (5) propose an efficient process to convert algal biomass to hydrogen, and (6) estimate the potential of algal hydrogen fermentation in China.

2. Stoichiometric potential of dark hydrogen production from algal biomass In dark fermentation, high-molecular weight organic substrates (e.g., carbohydrates, proteins, and lipids) are first hydrolyzed to low-molecular weight ones (e.g., monosaccharides, amino acids, and glycerol), and then are converted to SMPs, hydrogen, and carbon dioxide by HPB [40]. Hydrogenase is the key enzyme that catalyzes molecular hydrogen formation by combining protons and electrons [9]. Typical bacteria genera that are related with dark fermentation are Clostridium, Enterobacter, Lactobacillus, Bacillus, Klebsiella, Citrobacter, Anaerobiospirillum, Thermotoga, and Caldicellulosiruptor [41,42]. Dark fermentation is mainly composed of hydrolysis and acidogenesis of anaerobic digestion [43]. However, given that slow hydrolysis conducted by HPB seriously constrains subsequent acidogenesis for hydrogen production, additional pretreatment for biomass with high-molecular weight components is necessary [11,44]. 2.1. Metabolism of carbohydrates in dark fermentation High-molecular weight carbohydrates should generally be hydrolyzed to monosaccharides, which can then be efficiently used by HPB during dark fermentation [45]. Glucose, which is the most abundant and typical hexose, can be stored in the forms of starch, glycogen, cellulose, and trehalose in algal biomass [10,20,46–48]. A number of studies have reported the metabolic pathways of glucose during dark fermentation (Fig. 1) [46,49–51]. Glucose is degraded by HPB into pyruvate, coupled with generation of reduced nicotinamide adenine dinucleotide (NADH). Pyruvate is degraded into lactate (end product) by consuming NADH, or converted into acetyl-CoA, coupled with (1) generation of NADH and carbon dioxide, or (2) generation of hydrogen and carbon dioxide, or (3) generation of formate. Formate is further degraded into hydrogen and carbon dioxide as shown in Eq. (1) [52]. AcetylCoA is further converted into end products, such as ethanol, butyrate, and acetate, with or without consuming NADH. NADH and H þ generate hydrogen by catalysis of HPB hydrogenase (1 mol NADH generates 1 mol hydrogen) as shown in Eq. (2) [4]. The NADH generation and consumption during glucose metabolism are shown in Table 1. 1 mol glucose can theoretically generate 4 mol NADH through the acetate pathway. Therefore, 1 mol

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211

Fig. 1. Metabolic pathways of glucose during dark fermentation. This figure is adapted from literature [46,49-51].

glucose can theoretically generate 4 mol hydrogen [Eq. (3)] [38]. However, the production of other SMPs (e.g., ethanol, lactate, and butyrate) consumes NADH, resulting in the decrease in hydrogen yield.

(4)] or 2 mol hydrogen by PKP [Eq. (5)], respectively. Although PPP is the most common pathway, many HPB can also metabolize xylose through the PKP [57].

HCOOH-CO2 þ H2

ð1Þ

5 5 5 10 C5 H10 O5 þ H2 O- CH3 COOH þ CO2 þ H2 3 3 3 3

ð4Þ

NADH þ H þ -NAD þ þ H2

ð2Þ

C5 H10 O5 þ H 2 O-2CH3 COOH þ CO2 þ 2H2

ð5Þ

C6 H12 O6 þ 2H2 O-2CH3 COOH þ 2CO2 þ 4H2

ð3Þ

Xylose, which is a typical pentose, can be stored in the form of hemicellulose in algal biomass [53–56]. In dark fermentation, xylose is first converted into xylulose-5-phosphate, which is further metabolized through either the pentose phosphate pathway (PPP, Fig. 2) or the phosphoketolase pathway (PKP, Fig. 3) [46,57]. The PPP involves a series of reactions in which xylulose-5phosphate is converted into glyceraldehyde-3-phosphate, which is also an intermediate of glucose metabolism and can be further converted into pyruvate. In PKP, xylulose-5-phosphate is directly cleaved to glyceraldehyde-3-phosphate and acetyl-phosphate that is further converted to acetate [57]. The NADH generation and consumption during xylose metabolism are shown in Table 1. 1 mol xylose can theoretically generate 10/3 mol NADH (PPP) or 2 mol NADH (PKP) through the acetate pathway. Therefore, 1 mol xylose can theoretically generate 10/3 mol hydrogen by PPP [Eq.

2.2. Metabolism of proteins in dark fermentation High-molecular weight proteins should generally be hydrolyzed into amino acids to facilitate their further use by HPB during dark fermentation. Amino acids are important nitrogen sources that can improve biological activity and growth of HPB [14,58]. However, studies on hydrogen production using pure amino acids or proteins as substrates by dark fermentation are limited [59]. Kobayashi et al. reported that biomass with abundant proteins but little carbohydrates (e.g., waste eggs) hardly produces hydrogen during dark fermentation [60]. Xia et al. reported that hydrogen yield is almost zero when pure glutamic acid is used as sole substrate during dark fermentation [59]. The glutamic acid metabolism during dark fermentation is shown in Eq. (6). Furthermore, HPB prefer to consume monosaccharides (e.g., glucose) than amino acids (e.g., glutamic acid, aspartic acid, and arginine). This

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Fig. 2. Metabolic pathways of xylose during dark fermentation (PPP). This figure is adapted from literature [46,57].

is because fermentation of monosaccharides is more thermodynamically favorable with more negative values of standard free energy changes that can generate more adenosine triphosphate (ATP) for HPB cells [45].

glycerol metabolism are shown in Table 1. 1 mol glycerol can theoretically generate 3 mol NADH through the acetate pathway. Therefore, 1 mol glycerol can theoretically generate 3 mol hydrogen [Eq. (7)] [41].

3 9 1 C5 H9 NO4 þ H2 O- CH3 COOH þ NH3 þ CO2 2 4 2

C3 H8 O3 þ H 2 O-CH3 COOH þCO2 þ 3H2

ð6Þ

ð7Þ

2.3. Metabolism of lipids in dark fermentation Triacylglycerol (TAG), which is the main component of lipids with the weight ratio of 90–98%, is an ester derived from three long-chain fatty acids (LCFAs) and one glycerol [61,62]. Fermentation of LCFAs to shorter chain equivalents is thermodynamically unfavorable and non-spontaneous (positive standard free energy changes of reactions), unless coupling with methanogenesis [63]. Therefore, LCFAs cannot be fermented due to lack of methaneproducing bacteria (MPB) in dark fermentation. Glycerol is a wellstudied substrate for hydrogen fermentation [41,64,65]. The metabolic pathways of glycerol during dark fermentation are shown in Fig. 4 [46,49]. Glycerol is first converted into dihydroxyacetone phosphate (DHAP), coupled with NADH generation. DHAP is then converted into glyceraldehyde-3-phosphate, which is also an intermediate of glucose metabolism and can be further converted into pyruvate. The NADH generation and consumption during

2.4. Calculation of stoichiometric hydrogen production potential of biomass Table 2 shows the stoichiometric hydrogen yields and contents of monomers by dark fermentation. Glucose and xylose exhibit the same values of stoichiometric hydrogen yields [497.8 mL H2/g glucose or xylose; the gas volumes in this paper are calculated under standard temperature (0 1C) and pressure (1 atm)] and contents (66.7%). The stoichiometric hydrogen yield and content of glycerol (730.4 mL H2/g glycerol and 75.0%) are higher than those of monosaccharides. The stoichiometric yields of hydrogen and carbon dioxide of biomass in dark fermentation are predicted by the weight ratios of monosaccharides, amino acids, and glycerol (based on complete biomass hydrolysis) as shown in Eqs. (8) and (9), respectively. The stoichiometric hydrogen content of biomass in dark fermentation

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213

Fig. 3. Metabolic pathways of xylose during dark fermentation (PKP). This figure is adapted from literature [46,57].

is predicted as shown in Eq. (10). Y HB ¼ Y HM  W M þY HG  W G

ð8Þ

where YHB is the stoichiometric hydrogen yield of biomass (mL H2/ g biomass), YHM is the stoichiometric hydrogen yield of monosaccharides (497.8 mL H2/g monosaccharides), WM is the theoretical weight ratio of total monosaccharides in biomass (%), YHG is the stoichiometric hydrogen yield of glycerol (730.4 mL H2/g glycerol), and WG is the theoretical weight ratio of total glycerol in biomass (%), which can be estimated as 10.4% of the total lipids (assumed in the form of TAG) for algal biomass [18]. Y CB ¼ Y CM  W M þ Y CA  W A þ Y CG  W G

ð9Þ

where YCB is the stoichiometric carbon dioxide yield of biomass (mL CO2/g biomass), YCM is the stoichiometric carbon dioxide yield of monosaccharides (248.9 mL CO2/g monosaccharides), YCA is the stoichiometric carbon dioxide yield of amino acids (calculated as 76.2 mL CO2/g amino acid), WA is the theoretical weight ratio of total amino acids in biomass (%), and YCG is the stoichiometric carbon dioxide yield of glycerol (243.5 mL CO2/g glycerol). C HB ¼

Y HB Y HB þ Y CB

ð10Þ

where CHB is the stoichiometric hydrogen content of the produced biogas (%). 2.5. Components of algal biomass and stoichiometric hydrogen production potential The organic components of microalgal biomass are mainly composed of 6.7–68.4% carbohydrates, 14.9–84.0% proteins, and 0.8–63.2% lipids based on the mass percentage of volatile solids (VS; VS of algal biomass mainly comprise carbohydrates, proteins and lipids), as shown in Table 3. The variations in organic components of microalgae are considerably large between different species under different growth conditions. Carrieri et al. reported that the carbohydrate content of Arthrospira maxima significantly increases from approximately 20% to 50% of DW dominated by low-molecular weight trehalose and glucosylglycerol under sodium stress [46]. Aoyama et al. reported that the carbohydrate content of Arthrospira platensis remarkably increases from approximately 15% to 50% of DW dominated by high-molecular weight glycogen under nitrogen starvation [66]. Liu et al. reported that the lipid content of Chlorella vulgaris remarkably increases from 7.8% to 56.6% of DW at optimal iron concentration [67]. Lv et al. reported that the carbohydrate content (7–70% of DW), protein content (13–70% of DW), and lipid content

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– 0 – – – 2 – –

2 0 1 –

1 3 1 –

(14.5–28% of DW) of C. vulgaris significantly vary at different growth phases [68]. Fernandes et al. reported that the lipid content of Parachlorella kessleri increases from near 0% to 29% of DW, whereas its carbohydrate content decreases from approximately 25% of DW to 10% of DW under nutrient depletion [69]. Based on the determined components of microalgal biomass (Table 3), the stoichiometric hydrogen yield and content are in the ranges of 46.5–386.3 mL H2/g VS and 33.7–65.4% (calculated using the method described in Section 2.4). Overall, the microalgal species with high carbohydrate content can produce high stoichiometric hydrogen yield and content. Macroalgal species are typically composed of 67.0–87.2% carbohydrates, 9.4–25.4% proteins, and 0–7.6% lipids based on the mass percentage of VS (Table 3). The various organic components of macroalgae are relatively low compared with those in microalgae. Based on the components of macroalgal biomass, the stoichiometric hydrogen yield and content are in the ranges of 376.3–485.0 mL H2/g VS and 64.3–66.0% (calculated using the method described in Section 2.4). Compared with microalgal species, the macroalgal species produce relatively high and stable stoichiometric hydrogen yields and contents because of their relatively high carbohydrate contents and fixed organic components. Water hyacinth (Eichhornia crassipe) is a noxious weed, which is receiving worldwide attention because of its fast spread and crowded growth, resulting in serious problems in irrigation, navigation, hydropower generation, and biodiversity [70–72]. It possesses similar contents of carbohydrates (59.7–68.6% of VS), proteins (24.0–26.5% of VS), and lipids (1.1–2.1% of VS) to macroalgae [44,73]. The stoichiometric hydrogen yield (334.2–385.5 mL H2/g VS) and content (63.8–64.4%) of water hyacinth are also similar to those in macroalgae.

– 2 – –

3 3 2 –

Generation (mol NADH/ mol glycerol)b Consumption (mol NADH/ mol xylose) Generation (mol NADH/ mol xylose)b

3. Hydrogen production from algal biomass through dark fermentation

0 10/3 0 5/3

Net Generation (mol NADH/mol xylose)

Net Generation (mol NADH/mol xylose)

Glycerol Xylose (PKP)

Net Generation Consumption (mol NADH/mol (mol NADH/mol glycerol) glycerol)

214

b

a

All of substrate is assumed to be converted into sole end product. Maximum generation potential.

10/3 0 5/3 5/3 10/3 10/3 5/3 10/3 0 4 0 2 4 0 2 2 4 4 2 4 Ethanol Acetate Lactate Butyrate

Generation (mol NADH/ mol xylose)b Generation (mol NADH/ mol glucose)b

Net Generation Consumption (mol NADH/mol (mol NADH/mol glucose) glucose)

Xylose (PPP) Glucose Metabolic pathwaya

Table 1 Generation and consumption of NADH from monomers by dark fermentation

Consumption (mol NADH/ mol xylose)

3.1. Hydrogen production from model chemicals Temperature and pH are considered two key environmental factors affecting dark fermentation [9,74]. Dark fermentation may be divided into mesophilic (e.g., 25–40 1C), thermophilic (e.g., 40– 65 1C), as well as hyperthermophilic (e.g., 4 65 1C) conditions [40,75,76]. The mesophilic condition is more widely applied due to its less energy requirement, compared with thermophilic and hyperthermophilic conditions [9,74,77,78]. Nevertheless, high hydrogen yields may be achieved under the thermophilic and hyperthermophilic conditions due to the following reasons. Firstly, most of the hydrogen consumers are inhibited under the thermophilic and hyperthermophilic conditions. Secondly, thermophilic HPB exhibit higher hydrogen tolerances and faster metabolic activities than mesophilic HPB. Thirdly, high temperature is more thermodynamically favorable for hydrogen fermentation [9,41]. However, volumetric hydrogen production rates under the thermophilic and hyperthermophilic conditions are relatively low due to the low cell densities of HPB [42]. Hydrogen production is coupled with VFA production that can significantly decrease the pH of liquid phase [77]. Optimal pH values have been commonly reported in the range of 5.5–6.5 for dark fermentation [9,74,77]. Low pH is unfavorable for hydrogen production by HPB because such condition can result in charge variation of cell membrane, decrease in hydrogenase activity, and change in metabolic pathway (e.g., ethanol production) for NADH consumption [9,74]. Many studies are available about hydrogen production by both pure and mixed HPB from glucose, xylose, and glucose-based carbohydrates (e.g., trehalose and starch) by dark fermentation

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Table 2 Stoichiometric hydrogen yields and contents of monomers by dark fermentation Substrate

Glucose Xylose Glycerol a b

Stoichiometric H2 yielda

Stoichiometric CO2 yielda b

Stoichiometric H2 content (%)

(mol H2/mol monomer)

(mL H2/g monomer)

(mol CO2/mol monomer)

(mL CO2/g monomer)

4 10/3 3

497.8 497.8 730.4

2 5/3 1

248.9 248.9 243.5

b

66.7 66.7 75.0

Stoichiometric value is obtained via acetate pathway. Calculation is based on the molecular weights of hydrogen (2 g/mol), carbon dioxide (44 g/mol), glucose (180 g/mol), xylose (150 g/mol), and glycerol (92 g/mol).

Table 3 Stoichiometric hydrogen yields and contents of algal biomass by dark fermentation Classification Algal genus

Microalgae Microalgae Microalgae Microalgae Microalgae Microalgae Microalgae

Scenedesmus Chlorella Nannochloropsis Chlamydomonas Tetraselmis Dunaliella Microcystis (Taihu blue algae) Microalgae Arthrospira Microalgae Euglena Microalgae Anabaena Macroalgae Laminaria Macroalgae Gelidium Macroalgae Ulva Aquatic plant Eichhornia (water hyacinth)

Organic composition (% of VS)

Stoichiometric H2 yield (mL H2/g VS) Stoichiometric H2 content (%) Reference

Carbohydratesa Proteinsb

Lipidsc

15.4–68.4 14.0–43.5 26.1–58.4 19.8 10.8–52.2 6.6–33.7 8.2–37.2

21.1–71.8 22.8–69.0 14.9–53.2 55.8 31.1–74.3 35.5–80.3 57.8–72.4

10.5–22.6 0.8–63.2 19.8–50.6 24.4 4.3–22.5 6.3–48.4 2.9–18.3

94.9–386.3 91.8–241.2 160.1–338.0 128.0 76.8–301.4 46.5–191.2 47.6–209.5

46.7–64.8 47.0–62.7 56.4–65.4 53.9 45.1–63.2 33.7–59.0 38.8–57.6

[18,21,31] [11,18,30,99,100,102] [36,45,122] [18] [19,21] [18,21,99] [28,125,137]

6.7–55.6 15.7–23.4 29.4–37.5 75.8–86.1 79.7–86.5 67.0–87.2 59.7–68.6

30.0–84.0 50.6–68.5 53.8–65.9 11.7–21.6 12.6–19.6 9.4–25.4 24.0926.5

5.0–19.3 15.7–26.0 4.7–8.8 2.2–3.4 0–1.2 3.5–7.6 1.1–2.1

48.0–318.5 98.8–149.2 166.2–214.1 407.0–477.9 441.3–479.1 376.3–485.0 334.2–385.5

34.6–63.4 48.0–56.4 54.3–58.4 64.8–65.8 65.0–65.7 64.3–66.0 63.8–64.4

[10,18,19,113] [18] [21] [20,55,116] [20,118] [20] [44,73]

VS (volatile solids)¼ carbohydratesþ proteinsþ lipidsþ lignin. a Carbohydrates (except hemicellulose) are assumed to be glucan with molecular formula of (C6H10O5)n, while hemicellulose is assumed to be xylan with molecular formula of (C5H8O4)n. Theoretical glucose weight is calculated from carbohydrate weight (except hemicellulose) by multiplying a factor of 1.111, and theoretical xylose weight is calculated from hemicelluloses by multiplying a factor of 1.136 [73]. b Proteins are assumed to be polymer of glutamic acid (the most abundant amino acid in algal biomass) with molecular formula of (C5H7NO3)n, and theoretical glutamic acid weight is calculated from protein weight by multiplying a factor of 1.140 [22]. c Molecular formula of lipids (assumed in the form of TAG) is used C57H104O6 for algal biomass, and theoretical glycerol weight is calculated from lipid weight by multiplying a factor of 0.104 [18].

[38,77–80]. Su et al. reported that the hydrogen yield of glucose by Clostridium butyricum under a mesophilic condition (35 1C) reaches 214.0 mL H2/g VS, which is only 43.0% of the stoichiometric yield. The hydrogen content (73.4%) is a little higher than the stoichiometric value of glucose (66.7%), which could be attributed to dissolve of produced carbon dioxide [38]. The hydrogen yield of glucose by Caldicellulosiruptor saccharolyticus under a hyperthermophilic condition (72 1C) significantly increases to 448.0 mL H2/g VS, which is 90.0% of the stoichiometric yield [81]. Genetic modification of HPB is considered an effective method to enhance hydrogen production [42]. Song et al. reported that the hydrogen yield of glucose by recombinant Enterobacter cloacae with overexpressed hydrogenpromoting protein gene under a mesophilic condition (37 1C) reaches 316.6 mL H2/g VS, which is approximately 2 times higher than that by wild strain [52]. Alternatively, mixed bacteria obtained in heatpretreated anaerobic digestion sludge produces a hydrogen yield from glucose up to 342.2 mL H2/g VS under a mesophilic condition (35 1C) [77]. Heat pretreatment can effectively inactivate most of the hydrogen consumers (e.g., MPB) in the anaerobic digestion sludge. Nevertheless, spore-forming HPB are enriched through the subsequent acclimation. As compared with pure cultures of HPB, mixed HPB from anaerobic digestion sludge may be more likely to be used as the inoculum for large-scale application due to the following reasons. Firstly, they can resist contamination when unsterilized

materials are used as substrates, thereby ensuring stable hydrogen fermentation during continuous operation. Secondly, they can use more different substrates, thereby increasing energy conversion of complex materials [42]. Heat-pretreated anaerobic digestion sludge has also been demonstrated as an effective inoculum to use xylose as substrate for hydrogen production (hydrogen yields and contents are in the ranges of 190.6–336.0 mL H2/g VS and 42.2–55.0%) [79,82,83]. When the stable low-molecular weight disaccharides (e.g., trehalose) and high-molecular weight polysaccharides (e.g., starch) are used as substrates, pretreatment process is recommended to facilitate carbohydrate hydrolysis and subsequent hydrogen production [74,78,80]. Xia et al. reported that when trehalose is pretreated by microwave heating with dilute acid, hydrogen yield increases to 396.2 mL H2/g VS, which is 1.4 times higher than that for raw trehalose [78]. Su et al. and Cheng et al. reported that when cassava starch is pretreated by steam heating, hydrogen yield increases to 351.0 mL H2/g VS, which is 1.5 times higher than that for raw cassava starch [74,80]. Overall, hydrogen yields of carbohydrates are commonly in the range of 160.1–448.0 mL H2/g VS, which are 32.2–90.0% of the stoichiometric yield (Table 4). A number of studies have recently been conducted to investigate hydrogen production from both purified glycerol and crude glycerol obtained from biodiesel industries by dark fermentation [41,64,65,84–88]. Reungsang et al. and Liu et al. reported that

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A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Fig. 4. Metabolic pathways of glycerol during dark fermentation. This figure is adapted from literature [46,49].

hydrogen production from purified glycerol is better than that from crude glycerol, because the impurities such as methanol and soap in crude glycerol inhibit dark fermentation [87,88]. However, Lo et al. indicated that crude glycerol is more suitable for hydrogen production because the impurities such as phosphates in crude glycerol show positive effects on hydrogen production [84]. Most studies have reported low hydrogen yield under a mesophilic condition (30–37 1C) in the range of 29.2–219.1 mL H2/g VS (Table 4). However, Maru et al. obtained a high hydrogen yield of 696.3 mL H2/g VS (95.3% of the stoichiometric yield) using Thermotoga neapolitana under a hyperthermophilic condition (80 1C). The yields of acetate and carbon dioxide reach 97.0% and 93.0% of stoichiometric values [Eq. (7)] [41]. 3.2. Reactors for hydrogen fermentation The continuous stirred tank reactor (CSTR) has been widely used in hydrogen fermentation [89]. Substrates and HPB biomass are suspended in the liquid phase in a traditional CSTR. HPB have the same retention time with the hydraulic retention time (HRT), and may be easily washed out under a short HRT [89–91]. Cell immobilization offers an alternative to a traditional CSTR. It can maintain a high biomass concentration without biomass washout under a short HRT, which improves the substrate degradation and hydrogen production. Cell immobilization can be realized by the formation granules or biofilms. Granule-based and biofilm-based reactors can retain more active and effective HPB [89,90]. Up-flow anaerobic sludge bed (UASB) reactor and anaerobic filter (AF) reactor are more stable than CSTR under short HRTs [91,92]. Kongjan and Angelidaki found that the HRT reduction to 2.5 d results in cell biomass washout in the CSTR, whereas the UASB and AF reactors show fluctuating and reducing hydrogen production at an HRT of 0.5 d [92].

3.3. Hydrogen fermentation from microalgal biomass Microalgal biomass may comprise a high lipid content (e.g., 430% of VS, see Table 3). The LCFAs derived from lipids are not advantageous for fermentative hydrogen production (see Section 2.3). Lipid extraction for biodiesel production prior to hydrogen fermentation can be used for microalgal biomass rich in lipids [93– 97]. Fermentative hydrogen production from the whole microalgal biomass with a low lipid content and lipid-extracted microalgal biomass residues has been widely reported [10,35,96–98]. The intact microalgal cells without pretreatment have been reported with low hydrogen yields (7.1–33.8 mL H2/g VS corresponding to 4.1–17.7% of the stoichiometric yields) under a mesophilic condition (30–37 1C) [99–103]. Nguyen et al. found that hydrogen yield by T. neapolitana under a hyperthermophilic condition (75 1C) is near zero when Chlamydomonas reinhardtii is used as substrate without pretreatment [48]. This phenomenon occurs because HPB cannot readily access and consume highmolecular weight components that are tightly surrounded by rigid cell wall structure during dark fermentation [10,11,48]. Pretreatment is not only used to disrupt cell wall of microalgae, but also to hydrolyze intracellular high-molecular weight polymers. Carbohydrates in microalgae are the primary substrates responsible for hydrogen fermentation and they are typically in the forms of high-molecular weight starch and glycogen that should be hydrolyzed to achieve high hydrogen yield and production rate [11,48,104]. Yan et al. found that when Microcystis sp. (Taihu blue algae) is pretreated with dilute alkali at room temperature for 12 h, hydrogen yields are enhanced to 105.0–133.0 mL H2/g VS by heat-pretreated and acetate-pretreated anaerobic digestion sludge under a mesophilic condition (35 1C) [34,105]. Steam heating at 120 1C with dilute acid for 20 min is efficient in Chlorella pretreatment to significantly improve hydrogen yield

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

217

Table 4 Hydrogen production from model chemicals by dark fermentation Substrate

Main pretreatment

Inoculum

Fermentation type

Temperature (1C)

H2 yield (mL H2/g VS)

Stoichiometric H2 yield (mL H2/g VS)

Percentage of stoichiometric H2 yield (%)

H2 content (%)

Stoichiometric H2 content (%)

Reference

Glucose Glucose

– –

Batch Continuous

35 72

214.0 448.0

497.8 497.8

43.0 90.0

73.4 70.6

66.7 66.7

[38] [81]

Glucose Glucose

– –

Batch Batch

37 37

160.1 316.6

497.8 497.8

32.2 63.6

– –

66.7 66.7

[52] [52]

Glucose

–

Batch

35

342.2

497.8

68.7

–

66.7

[77]

Trehalose

Batch

35

396.2

524.2

75.6

–

66.7

[78]

Batch

35

276.1

553.1

49.9

–

66.7

[80]

Cassava starch

Microwave heating with dilute H2SO4 Steam heating and enzymatic hydrolysis Steam heating

Clostridium butyricum Caldicellulosiruptor saccharolyticus Enterobacter cloacae Recombinant Enterobacter cloacae Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge

Batch

31

351.0

553.1

63.5

–

66.7

[74]

Xylose

–

Batch

35

336.0

497.8

67.5

55.0

66.7

[79]

Xylose

–

Batch

70

274.8

497.8

55.2

–

66.7

[75]

Xylose

–

Batch

37

190.6

497.8

38.3

–

66.7

[83]

Xylose

–

Continuous

50

209.1

497.8

42.0

42.2

66.7

[82]

Batch

35

0.5

–

–

–

–

[59]

Batch

37

99.8

730.4

13.7

51.5

75.0

[64]

Batch Batch Continuous Continuous

80 37 80 35

696.3 149.9 586.8 121.7

730.4 730.4 730.4 730.4

95.3 20.5 80.3 16.7

75.4 46.8 76.0 78.3

75.0 75.0 75.0 75.0

[41] [65] [41] [84]

Continuous

37

99.8

730.4

13.7

37.1

75.0

[87]

Batch

37

219.1

730.4

30.0

54.1

75.0

[85]

Batch

37

29.2

730.4

4.0

–

75.0

[86]

Batch

30

158.3

730.4

21.7

–

75.0

[88]

Continuous

35

187.5

730.4

25.7

72.7

75.0

[84]

Continuous

37

78.9

730.4

10.8

24.2

75.0

[87]

Cassava starch

Glutamic acid –

Glycerol

Glycerol Glycerol Glycerol Glycerol

– – – –

Glycerol

–

Crude glycerol Crude glycerol

–

Crude glycerol Crude glycerol  Crude glycerol

–

– – –

Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Thermoanaerobacter related bacteria Heat-pretreated and domesticated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Thermotoga neapolitana Enterobacter aerogenes Thermotoga maritima Clostridium pasteurianum Immobilized Enterobacter aerogenes on heat-pretreated anaerobic sludge Enriched activated sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated organic soil Clostridium pasteurianum Immobilized Enterobacter aerogenes on heat-pretreated anaerobic sludge

[201.6 mL H2/g chemical oxygen demand (COD) and 85.3 mL H2/g VS] and production rate (148.0 and 246.0 mL H2/L/h) under a mesophilic condition (37 1C) using E. cloacae and C. butyricum as the inoculum, respectively [33,106]. The yield of low-molecular weight reducing sugars from Chlorella is approximately 100% of the theoretical value [33]. Compared with steam heating, microwave heating exhibits several advantages, such as short duration, high selectivity, and high uniformity, because electromagnetic field can selectively and instantly elicit thermal effects on polar

molecules, such as water, during microwave heating [45,107]. Microwave heating at 140 1C with dilute acid for 15 min is favorable for pretreatment of Nannochloropsis oceanica and A. platensis, resulting in considerable enhancement in hydrogen yield (up to 101.7 mL H2/g VS) and hydrogen production rate (up to 547.0 mL H2/L/h) using heat-pretreated anaerobic digestion sludge under a mesophilic condition (35 1C) [45,104]. Xia et al. found similar characteristics of biomass saccharification and subsequent hydrogen production of Chlorella pyrenoidosa pretreated with

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A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

microwave heating with dilute acid and steam heating with dilute acid [11]. Steam heating technology is more promising than microwave heating technology for large-scale pretreatment because excess heat (e.g., waste heat of boiler) can be reused in steam heating, thereby decreasing electricity input and reducing economic cost. Jeon et al. and Choi et al. reported that ultrasonication for 15–60 min at room temperature to 45 1C is efficient for Scenedesmus obliquus to enhance the subsequent hydrogen yield (up to 168.4 mL H2/g VS) and hydrogen production rate (120.3– 300.0 mL H2/L/h) [35,98]. However, the electricity input for ultrasonication technology should also be considered for large-scale pretreatment. Some other pretreatments including enzymatic hydrolysis, autoclave, and combined mechanical pressing and centrifugation have also been demonstrated as effective methods in improving hydrogen production by S. obliquus, C. reinhardtii, and Thalassiosira weissflogii [31,48,108]. Although pretreatment is necessary for efficient hydrogen production from microalgal biomass, it still exhibits some negative effects on dark fermentation. Pretreatment for long duration or at high temperature could degrade some organic components, thereby decreasing the overall hydrogen production potential, and could also convert some organic components (e.g., glucose) to byproducts (e.g., furfural), which could inhibit the subsequent hydrogen fermentation [78,107]. In addition, acid or alkali pretreatment generally need NaOH to neutralize pH after pretreatment or to be used as pretreatment reagent, and thus, excess Na þ is added into the biomass hydrolyzate, which could inhibit HPB activities during dark fermentation [11,33,34,45,94,104–106,109]. Studies on effective pretreatment method with little unfavorable biomass conversion and additional inhibitor are necessary. Current pretreatments, such as heat and ultrasound, usually consume electricity. They are energy intensive and expensive. Cho et al. found the energy requirements in thermal (50–120 1C, 30 min) and ultrasonic (130 W, 30–180 s) pretreatments of microalgal biomass are 8–18 kJ/g VS and 39–234 kJ/g VS [110]. These values are very high compared with the energy contents in microalgal biomass (e.g., 25.9 kJ/g VS) [14]. Ometto et al. reported negative energy balances in biogas production from pretreated microalgal biomass under most of the thermal and ultrasonic conditions [111]. Passos and Ferrer suggested the low temperature heat pretreatment under 75 1C may provide a positive energy balance in biogas production from microalgal biomass [112]. More effective pretreatments should be developed to improve the fermentative biogas production whilst reducing energy consumption. Efficient biological pretreatment (e.g., enzymatic hydrolysis) can be potentially used prior to hydrogen fermentation. Alternatively, continuous pretreatment system based on excess heat utilization combined with heat recovery unit is also recommended for future pretreatment research. Furthermore, energy input and economic cost of pretreatment should also be considered for largescale application [11]. Mixed HPB domesticated by microalgal biomass can accumulate special bacteria that can adapt to microalgal biomass, leading to improved hydrogen production during dark fermentation [10,95,113,114]. Cheng et al. reported that the hydrogen yield and production rate of A. maxima pretreated with grinding and enzymatic hydrolysis significantly increase to 82.8 mL H2/g VS and 195.6 mL H2/ L/h, respectively, when heat-pretreated anaerobic digestion sludge domesticated with the same microalgal biomass is used as the inoculum under a mesophilic condition (35 1C) [113]. Cheng et al. also found that hydrogen yield and production rate of A. platensis pretreated by ultrasonication and enzymatic hydrolysis are increased to 96.8 mL H2/g VS and 500.0 mL H2/L/h, respectively, when heatpretreated anaerobic digestion sludge domesticated with the same microalgal biomass is used as inoculum under a mesophilic condition (35 1C) [10]. Xia et al. conducted continuous operation using C.

pyrenoidosa pretreated by steam heating with dilute acid and heatpretreated anaerobic digestion sludge as the inoculum under a mesophilic condition (35 1C). They reported stable production of hydrogen (51.7–62.0 mL H2/g VS) and SMPs after HPB adaption and domestication. The microbial community of HPB is developed from a simple structure of one genus (Clostridium) comprising one dominating species (C. butyricum) at earlier unstable stage of fermentation to a complex structure of three genera (Clostridium, Eubacterium, and Sporanaerobacter) comprising three main species (Clostridium cochlearium, Clostridium acetireducens, and Sporanaerobacter acetigenes) at later stable stage. HPB after adaption and domestication efficiently and stably convert microalgal biomass to hydrogen and SMPs [114]. Alternatively, high-performance HPB strains for microalgal biomass utilization can also be obtained by advanced breeding methods, such as physiochemical mutation and genetic modification. The lipid-extracted microalgal biomass, which is rich in carbohydrates and proteins, is also a promising substrate for fermentative hydrogen production [95,96]. Yang et al. used thermal heating at 100 1C with dilute NaOH for 8 h to pretreat Scenedesmus sp. residues after lipid extraction. The subsequent hydrogen yields of 45.5–46.0 mL H2/g VS are obtained by heat-pretreated anaerobic digestion sludge under a mesophilic condition (37 1C) [94,109]. The same authors conducted repeated batch operations from Scenedesmus sp. residues after lipid extraction pretreated by thermal heating with dilute NaOH using heat-pretreated anaerobic digestion sludge as inoculum under a mesophilic condition (37 1C). They found that hydrogen yield and production rate at final batch significantly increase to 66.2 mL H2/g VS and 397.0 mL H2/L/h, corresponding to 1.4 and 8.4 time increases compared with those in the initial batch [95]. This result also confirms that HPB domestication can significantly enhance hydrogen production from microalgal biomass, particularly the hydrogen production rate. Nobre et al. used Nannochloropsis sp. as a feedstock for the production of biodiesel, pigments and fermentative hydrogen. The remaining microalgal biomass after lipid and pigment extraction can be efficiently fermented by Enterobacter aerogenes, with a hydrogen yield of 60.6 mL H2/g DW [97]. The C/N ratio of substrate is an important factor in dark fermentation [58,115]. Excess C/N ratio inhibits biological activity and growth of HPB, resulting in inefficient hydrogen production. By contrast, inadequate C/N ratio indicates that substrate contains too much nitrogen sources, such as proteins, which are not advantageous for hydrogen production (as described in Section 2.2) [14]. The high protein content leads to low C/N ratio of microalgal biomass, which seriously constrains hydrogen production from sole microalgal biomass [58]. Xia et al. reported that hydrogen production is remarkably enhanced from mixed biomass of C. pyrenoidosa and cassava starch. The hydrogen yield of 276.2 mL H2/g VS, which corresponds to 3.7 and 1.8 times compared with those for the sole C. pyrenoidosa and cassava starch, respectively, is obtained at C/N molar ratio of 25.3. The hydrogen production rate of 540.9 mL H2/L/h, which corresponds to 3.4 and 3.7 time increases compared with those for sole C. pyrenoidosa and cassava starch, respectively, is obtained at C/N molar ratio of 15.6 [14]. Waste biomass with high C/N ratios (e.g., agricultural and food wastes) exhibits significant potential in improving the C/N ratio of microalgal biomass to facilitate hydrogen production. Little difference in hydrogen production is found using either dry biomass or wet biomass of microalgae as substrates in dark fermentation [31]. However, considering the high energy input in algae drying process (e.g., latent heat of vaporization of water is 2.26 kJ/g), wet biomass of microalgae without energy-intensive drying process is strongly recommended for future study. As shown in Table 5, hydrogen yields of microalgae-related biomass are in the range of 7.1–276.2 mL H2/g VS (with common hydrogen contents of 16.3–64.0%), which correspond to 4.1–70.0% of the

Table 5 Hydrogen production from algal and other aquatic biomass by dark fermentation Biomass type

Main pretreatment

Microalgae

Scenedesmus obliquus Scenedesmus obliquus Scenedesmus obliquus

Wet biomass

Autoclave

Scenedesmus obliquus Scenedesmus obliquus

Dry biomass

Microalgae Microalgae

Microalgae Microalgae

Dry biomass Wet biomass

Wet biomass

Scenedesmus sp.

Microalgae

Scenedesmus sp.

Microalgae

Scenedesmus sp.

Microalgae

Scenedesmus sp.

Microalgae

Microalgae

Chlamydomonas reinhardtii Chlorella Dry biomass sorokiniana Chlorella vulgaris Wet biomass

Microalgae

Chlorella vulgaris Dry biomass

Microalgae

Chlorella vulgaris Wet biomass

Microalgae

Chlorella pyrenoidosa

Dry biomass

Microalgae

Chlorella pyrenoidosa

Microalgae

Chlorella pyrenoidosa

Dry biomass mixed with cassava starch Dry biomass

Microalgae

Chlorella sp.

Dry biomass

Microalgae

Chlorella sp.

Dry biomass

Microalgae

Nannochloropsis oceanica

Dry biomass

Microalgae

Algal biomass residues after lipid extraction Algal biomass residues after lipid extraction Algal biomass residues after lipid extraction Algal biomass residues after lipid extraction Wet biomass

Enterobacter aerogenes Autoclave Clostridium butyricum Ultrasonication Heat-pretreated anaerobic digestion sludge Clostridium Heating with diltue butyricum H2SO4 Ultrasonication Heat-pretreated anaerobic digestion sludge Steam heating with dilute Heat-pretreated NaOH anaerobic digestion sludge Steam heating with dilute Heat-pretreated NaOH anaerobic digestion sludge – Heat-pretreated anaerobic digestion sludge Thermal heating with Heat-pretreated dilute NaOH anaerobic digestion sludge Enzymatic hydrolysis Thermotoga neapolitana Steam heating with dilute Enterobacter cloacae HCl – Bacteria in algae slurry – Heat-pretreated anaerobic digestion sludge Steam heating with dilute Clostridium HCl butyricum Microwave heating with Heat-pretreated anaerobic digestion dilute H2SO4 sludge Steam heating with dilute Heat-pretreated H2SO4 anaerobic digestion sludge Steam heating with dilute Heat-pretreated H2SO4 anaerobic digestion sludge – Heat-pretreated anaerobic digestion sludge – Dilute anaerobic digestion sludge Microwave heating with Heat-pretreated anaerobic digestion dilute H2SO4 sludge

Fermentation type

Temperature (1C)

H2 yield (mL H2/ Percentage of g VS) stoichiometric H2 yield (%)b

Energy yield (kJ/g VS)e

H2 content (%)

H2 production rate (mL H2/L/h)

Energy production rate (kJ/L/ h)e

Reference

Batch

30

57.6

0.7

54.1

–

–

[31]

Batch

37

113.1

1.4

62.5

–

–

[31]

2.2

–

300.0

3.8

[98]

–

–

–

–

[37]

–

–

120.3

1.5

[35]

23.8 46.7 a

c

Batch

55

168.4

Batch

37

Batch

35

360.9 ml H2/g – monosaccharides 236.4 ml H2/g – monosaccharides

Batch

37

45.5

18.9c

0.6

–

26.8

0.3

[94]

Batch

37

46.0

19.1c

0.6

–

–

–

[109]

Batch

37

30.0

12.5c

0.4

–

28.2

0.4

[96]

Repeated Batch

37

66.2

27.5c

0.8

–

397.0

5.1

[95]

Batch

75

–

64.0

227.3

2.9

[48]

Batch

37

–

–

148.0

1.9

[106]

Batch

37

– 311.1 ml H2/g monosaccharides – 201.6 ml H2/g COD 10.8 6.5c

0.1

16.3

–

–

[99]

Batch

35

33.8

14.0

0.4

–

257.0

3.3

[102]

Batch

37

85.3a

51.2c

1.1

–

246.0

3.1

[33]

Batch

35

83.3

41.2

1.1

54.3

182.6

2.3

[11]

Batch

35

276.2

56.4

3.5

54.6

540.9

6.9

[14]

Continuous

35

62.0

37.2c

0.8

49.7

20.1

0.3

[114]

Batch

35

7.1

4.1

0.1

45.3

–

–

[100]

Batch

30

29.5a

17.7c

0.4

–

–

–

[101]

Batch

35

39.9

18.2

0.5

–

52.6

0.7

[45]

70.0

219

Microalgae

Inoculum

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Classification Species

220

Table 5 (continued ) Biomass type

Main pretreatment

Inoculum

Fermentation type

Temperature (1C)

H2 yield (mL H2/ Percentage of g VS) stoichiometric H2 yield (%)b

Energy yield (kJ/g VS)e

H2 content (%)

H2 production rate (mL H2/L/h)

Energy production rate (kJ/L/ h)e

Reference

Microalgae

Nannochloropsis sp.

–

Enterobacter aerogenes

Batch

30

63.8a

25.6c

0.8

–

–

–

[97]

Microalgae

Nannochloropsis sp. Thalassiosira weissflogii

Algal biomass residues after lipid extraction Wet biomass

Steam heating with dilute H2SO4 Mechanical pressing and centrifugation

Clostridium acetobutylicum Thermotoga neapolitana

Batch

37

–

–

–

–

7.9

0.1

[36]

Batch

80

236.4 ml H2/g – monosaccharides

–

–

36.2

0.5

[108]

–

Bacteria in algae slurry Heat-pretreated and domesticated anaerobic digestion sludge Heat-pretreated and domesticated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Enterobacter aerogenes

Batch

37

12.6

10.6c

0.2

48.3

–

–

[99]

a

29.5

1.1

–

195.6

2.5

[113]

Microalgae

Microalgae Microalgae

Dunaliella tertiolecta Arthrospira maxima

Carbohydrates and proteins from algal biomass Wet biomass Dry biomass

Grinding and enzymatic hydrolysis

Microalgae

Arthrospira platensis

Wet biomass

Ultrasonication and enzymatic hydrolysis

Microalgae

Arthrospira platensis

Wet biomass

Microalgae

Anabaena sp.

Microalgae

Microcystis sp. (Taihu blue algae) Microcystis sp. (Taihu blue algae) Laminaria japonica

Algal biomass residues after autofermentation Wet biomass

Microwave heating with dilute H2SO4 and enzymatic hydrolysis –

NaOH hydrolysis

Wet biomass

NaOH hydrolysis

Dry biomass

–

Microalgae

Macroalgae

Macroalgae

Laminaria japonica

Dry biomass

Grinding and thermal heating

Macroalgae

Laminaria japonica

Wet biomass

Ball mill and steam heating

Macroalgae

Laminaria japonica

Dry biomass

–

Macroalgae

Gelidium amansii

Dry biomass

Macroalgae

Gelidium amansii

Dry biomass

Grinding, heating with diltue H2SO4, and activated carbon detoxification Grinding, heating with diltue H2SO4, and activated carbon detoxification –

Dry biomass

Batch

35

82.8

Batch

35

96.8a

36.8

1.2

–

500.0

6.4

[10]

Batch

35

101.7

38.7

1.3

–

547.0

7.0

[104]

Batch

30

15.1a

7.9

c

0.2

–

–

–

[103]

Batch

35

105

50.1d

1.3

–

–

–

[105]

Batch

35

133

63.5d

1.7

44.3

–

–

[34]

Batch

35

107.5

26.4

1.4

–

260.0

3.3

[116]

Batch

35

158.0

33.5

2.0

–

620.0

7.9

[55]

Batch

35

29.5a

6.7c

0.4

34.3

70.0

0.9

[117]

Continuous

35

92.3

20.9c

1.2

–

–

–

[116]

Batch

35

64.5

14.0c

0.8

–

142.1

1.8

[118]

Heat-pretreated Batch anaerobic digestion sludge

35

44.6

9.7c

0.6

–

510.0

6.5

[32]

45–55

28.2a

7.8c

0.4

–

206.5

2.6

[71]

Heat-pretreated anaerobic digestion sludge Acetate stressed anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge Heat-pretreated anaerobic digestion sludge

Batch

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Classification Species

– –

221

stoichiometric values of dark fermentation, equal to energy yields of 0.1–3.5 kJ/g VS. Hydrogen production rates are in the range of 7.9–547.0 mL H2/L/h, which are equal to energy production rates of 0.1–7.0 kJ/L/h. Studies on pretreatment, HPB domestication, and co-fermentation of microalgae and waste biomass with high C/N ratio are necessary to improve hydrogen production. Furthermore, most of studies on hydrogen production using microalgal biomass as substrate were conducted in batch systems, which is unsuitable for large-scale application [114]. More future studies should be conducted in continuous systems.

[73]

2.5 194.8

[72]

3.2 249.2

[44]

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

c

b

Aquatic plant

a

Dry biomass

Dry biomass

Eichhornia crassipes (water hyacinth) Eichhornia crassipes (water hyacinth) Aquatic plant

Components of algae dry biomass is assumed to be composed of 95% VS and 5% ash. Percentage of stoichiometric H2 yield is calculated based on the specified components of each algal biomass reported in literature. Stoichiometric hydrogen yield used in calculation is assumed to be average value of each algae genus presented in Table 3. d Stoichiometric hydrogen yield used in calculation is assumed to be maximum value of Microcystis presented in Table 3. e Higher heating value of hydrogen (286 kJ/mol) is used in calculation of energy yield and production rate.

– 0.7 51.7 35

14.4c

– 1.4 29.1 112.3 35

Batch Heat-pretreated anaerobic digestion sludge Batch Heat-pretreated anaerobic digestion sludge

Batch Heat-pretreated anaerobic digestion sludge Aquatic plant

Aquatic plant

Eichhornia crassipes (water hyacinth) Eichhornia crassipes (water hyacinth)

Dry biomass

Steam heating, microwave heating with dilute NaOH, and enzymatic hydrolysis Microwave heating with dilute H2SO4 and enzymatic hydrolysis Dilute NaOH pretreatment and enzymatic hydrolysis

Anaerobic digestion sludge

35

76.7

23.0

1.0

83.2

3.4. Hydrogen fermentation from macroalgal biomass Macroalgal biomass is rich in carbohydrates (67.0–87.2% of VS) with small but suitable amount of proteins (9.4–25.4% of VS) and little or no lipids (0–7.6% of VS), and thus, it is a promising substrate for dark fermentation. As shown in Table 3, macroalgal biomass shows high stoichiometric hydrogen yield (376.3–485.0 mL H2/g VS) compared with microalgal biomass (46.5–386.3 mL H2/g VS). However, only a few recent studies have reported the hydrogen production from macroalgal biomass by heat-pretreated anaerobic digestion sludge under a mesophilic condition (35 1C) as shown in Table 5. Shi et al. achieved 107.5 mL H2/g VS hydrogen yield and 260.0 mL H2/L/h production rate from Laminaria japonica. Continuous operation produces a hydrogen yield of 92.3 mL H2/g VS, which is a little lower than that of batch operation because of the growth of propionic acidproducing bacteria [116]. Jung et al. found significant improvements in hydrogen production rate (620.0 mL H2/L/h) and yield (158.0 mL H2/g VS) when L. japonica is pretreated by grinding and thermal heating at 170 1C [55]. However, Park et al. found that ball mill and steam heating at 120 1C is less efficient for pretreatment of L. japonica, with 29.5 mL H2/g VS hydrogen yield and 70.0 mL H2/L/h production rate [117]. Park et al. found that thermal heating (150 1C) with dilute acid is efficient for hydrolysis of Gelidium amansii. However, the byproducts in biomass hydrolyzate (e.g., 5-hydroxymethylfurfural) inhibit hydrogen production. Detoxification by activated carbon leads to recovery of hydrogen production, with 64.5 mL H2/g VS hydrogen yield and 142.1 mL H2/L/h production rate [118]. The hydrogen production rate is further improved to 510.0 mL H2/L/h at optimal parameters of thermal heating with dilute acid [32]. As shown in Table 5, hydrogen yields of macroalgal biomass are in the range of 29.5–158.0 mL H2/g VS, which correspond to 6.7– 33.5% of the stoichiometric values of dark fermentation, equal to energy yields of 0.4–2.0 kJ/g VS. Hydrogen production rates are in the range of 70.0–620.0 mL H2/L/h, which are equal to energy production rates of 0.9–7.9 kJ/L/h. Although results of the analysis of organic components indicate that macroalgal biomass exhibits higher hydrogen production potential than microalgal biomass, results of recent studies are insufficient to indicate obvious higher hydrogen production results from macroalgae. Similar studies on microalgal biomass (e.g., pretreatment, co-fermentation, HPB domestication, and continuous operation) should be devoted to the use of more macroalgal species (e.g., Ulva lactuca) as substrates to enhance hydrogen production and improve the feasibility for large-scale application.

4. Dark fermentation followed by photo fermentation and anaerobic digestion to enhance energy conversion from algal biomass 4.1. Comparison of single-stage anaerobic digestion and dark fermentation from algal biomass Anaerobic digestion comprises four typical steps (i.e., hydrolysis, acidogenesis, acetogenesis, and methanogenesis) that convert

222

Table 6 Methane production from algal biomass by anaerobic digestion Biomass type

Main pretreatment

Microalgae

Scenedesmus obliquus

Wet biomass

–

Microalgae

Scenedesmus obliquus

Wet biomass

Microalgae

Scenedesmus obliquus

Wet biomass

Microalgae

Scenedesmus sp.

Wet biomass

Microalgae

Nannochloropsis sp.

Dry biomass

Microalgae

Nannochloropsis sp.

Microalgae Microalgae

Chlamydomonas reinhardtii Chlorella sorokiniana

Algal biomass residues after lipid extraction Wet biomass

Microalgae

Chlorella kessleri

Wet biomass

Microalgae

Chlorella vulgaris

Wet biomass

Microalgae

Chlorella vulgaris

Wet biomass

Microalgae

Chlorella vulgaris

Wet biomass

Microalgae

Chlorella sp.

Wet biomass

Microalgae

Chlorella sp.

Microalgae

Euglena gracilis

Algal biomass mixed with waste activated sludge Wet biomass

Microalgae

Wet biomass

–

Wet biomass

–

Microalgae

Phaeodactylum tricornutum Phaeodactylum tricornutum Arthrospira platensis

Dry biomass

–

Microalgae

Arthrospira platensis

Dry biomass

–

Microalgae

Arthrospira platensis

Wet biomass

–

Microalgae

Arthrospira platensis

Wet biomass

–

Microalgae

Dunaliella salina

Wet biomass

–

Microalgae

Dunaliella tertiolecta

Wet biomass

–

Microalgae

Microcystis sp. (Taihu blue algae) Microcystis sp. (Taihu blue algae) Microcystis sp. (Taihu blue algae)

Wet biomass

–

Wet biomass

–

Wet biomass

–

Microalgae

Microalgae Microalgae

Wet biomass

Inoculum

Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge Thermal pretreatment Sludge collected at sugar factory Thermal pretreatment Anaerobic digestion sludge Thermal pretreatment Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge – Anaerobic digestion sludge –

Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge

Digestion type

Temperature (1C)

CH4 yield (mL CH4/g VS)

Energy yield (kJ/g VS) a

CH4 content (%)

CH4 production Energy rate (mL CH4/L/h) production rate (kJ/L/h) a

Reference

Batch

38

177.9

7.1

62.0

–

–

[121]

Batch

33

210.0

8.3

–

–

–

[76]

Continuous 54

170.0

6.7

77.1

19.3

0.8

[76]

Continuous 35

–

75.0

–

–

[129]

16.5

–

–

–

[122]

Batch

35

111.4 ml CH4/g COD 417.0

Batch

35

381.0

15.1

/

–

–

[122]

Batch

38

387.4

15.4

66.0

–

–

[121]

Batch

37

–

77.0

–

–

[123]

Batch

38

517.5 ml CH4/g COD 217.8

8.6

65.0

–

–

[121]

Batch

35

228.8

9.1

62.5

–

–

[130]

Batch

37

286.0

11.4

68.0

–

–

[99]

Continuous 35

240.0

9.5

–

7.5

0.3

[131]

Batch

37

123.0

4.9

–

–

–

[138]

Batch

37

262.0

10.4

–

–

–

[138]

Batch

38

325.0

12.9

–

–

–

[121]

Batch

33

350.0

13.9

–

–

–

[76]

Continuous 54

290.0

11.5

78.6

26.2

1.0

[76]

Batch

35

355.0

14.1

70.1

–

–

[124]

Batch

50

358.4

14.2

65.9

–

–

[124]

Batch

38

293.4

11.6

61.0

–

–

[121]

Batch

33

280.0

11.1

–

–

–

[76]

Batch

38

323.2

12.8

64.0

–

–

[121]

Batch

37

24.0

1.0

49.0

–

–

[99]

Batch

55

386.8

15.4

–

–

–

[125]

Batch

35

287.6

11.4

9

2.0

0.1

[28]

Continuous 35

160.0

6.4

68.8

40.0

1.6

[137]

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Classification Species

[136] 2.7 59.8 12.8

a

Higher heating value of methane (889 kJ/mol) is used in calculation of energy yield and production rate.

321.4 – Mixed algae

223

organic components into methane, carbon dioxide, and other metabolites (e.g., ammonia) by complex microbial community [43,119,120]. Methane yield and content of anaerobic digestion can be predicted by the Buswell equation [Eq. (11)] [18].     3 b d a 3 d b Ca Hb Nc Od þ a þ c   H2 O- þ c þ  b CO2 4 4 2 2 8 4 8   a b 3 d þ  c  CH4 þ cNH3 þ ð11Þ 2 8 8 4

67.0

[136] 0.9

– Mainly green algae, brown algae, and seaweed Mainly Scenedesmus sp. Wet biomass and Chlorella sp. Mainly Scenedesmus sp. Algal biomass mixed and Chlorella sp. with waste paper Mixed algae

Mixed algae

Mainly Scenedesmus sp. Algal Biomass residues after lipid extraction Mainly Rhizoclonium sp. Wet biomass Mixed algae

Mixed algae

Mainly Scenedesmus sp. Wet biomass Mixed algae

Dry biomass Sargassum muticum Macroalgae

–

Anaerobic Continuous 35 digestion sludge Anaerobic Continuous 35 digestion sludge

143.0

5.7

69.0

23.9

[135] 0.03 Batch

35

256.0

10.2

70.0

0.8

[134] – – 53 Batch

216.3

8.6

–

[133] – – 38 Batch

380.0

15.1

–

[133] – – 38 Batch

330.0

13.1

–

[127] – – 35 Batch

130.0

5.2

–

[127] – – 279.0 35 Batch

Anaerobic digestion sludge Grinding Anaerobic digestion sludge High pressure thermal Anaerobic hydrolysis digestion sludge High pressure thermal Anaerobic hydrolysis digestion sludge Size reduction and Anaerobic enzymatic hydrolysis digestion sludge Grinding Anaerobic digestion sludge Dry biomass Palmaria palmata

Homogenized paste obtained by maceration Grinding Macroalgae

Microalgae

Wet biomass Ulva lactuca Macroalgae

– Macroalgae

–

11.1

–

[132] – – 55 Batch

271.0

10.8

–

[126] – – 37 Batch

250.2

9.9

–

[137] 2.3 Continuous 35

234.0

9.3

62.4

58.5

[125] Microalgae

Algal biomass mixed with kitchen wastes Algal biomass mixed with corn straw Dry biomass Microcystis sp. (Taihu blue algae) Microcystis sp. (Taihu blue algae) Ulva lactuca

–

Anaerobic digestion sludge Anaerobic digestion sludge Anaerobic digestion sludge Effluent from digester

Batch

55

462.6

18.4

–

–

–

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Previous studies have focused on anaerobic digestion of algal biomass (e.g., microalgae Scenedesmus, Nannochloropsis, Chlamydomonas, Chlorella, Euglena, Phaeodactylum, Arthrospira, Dunaliella, Microcystis, and macroalgae Ulva, Palmaria, Sargassum) [76,121– 136]. The theoretical methane yield for carbohydrates, proteins, and lipids in algal biomass are 415 mL CH4/g carbohydrates, 851 mL CH4/g proteins, and 1014 mL CH4/g lipids, respectively [18]. As shown in Table 6, methane yields of microalgal biomass (24.0–417.0 mL CH4/g VS) are generally higher than those of macroalgal biomass (130.0–279.0 mL CH4/g VS), because the contents of lipids and proteins of microalgal biomass are usually higher than those of macroalgal biomass. Co-digestion of algal biomass and waste biomass (e.g., waste activated sludge, kitchen wastes, and corn straw) exhibits relatively high methane yields (234.0–462.6 mL CH4/g VS) compared with mono-digestion [125,137,138]. Some issues such as ammonia inhibition caused by protein degradation and sodium inhibition caused by inorganic salts of marine algal species should be addressed to enhance anaerobic digestion of algal biomass [18,126]. As shown in Table 6, methane yields and contents produced using algal biomass are in the ranges of 24.0–462.6 mL CH4/g VS (with common methane contents of 49.0–78.6%), which are equal to energy production rates of 1.0–18.4 kJ/g VS. Methane production rates are in the range of 0.8–67.0 mL CH4/L/h, which are equal to energy production rates of 0.03–2.7 kJ/L/h. The median energy production rate of hydrogen of algal biomass by dark fermentation (0.1–7.9 kJ/L/h) is approximately 3 times higher than that of methane by anaerobic digestion (0.03–2.7 kJ/L/h) as shown in Tables 5 and 6. The higher energy production rate of dark fermentation leads to smaller volume of reactor and shorter hydraulic retention time of operation, and results in lower economic cost and less energy input, which can make dark fermentation more attractive. However, the energy yields (0.1–3.5 kJ/g VS) of single-stage dark fermentation are lower than those of singlestage anaerobic digestion (1.0–18.4 kJ/g VS), because of the thermodynamic bottleneck of dark fermentation and loss of energy in organic residues, which constrains single-stage dark fermentation [38,45]. 4.2. Subsequent photo fermentation for hydrogen co-generation The organic residues in effluent of dark fermentation are mainly composed of SMPs (e.g., acetate, butyrate, and ethanol) in supernatant residues and undegraded biomass (e.g., lipid components) in solid residues [45]. SMPs can be converted into hydrogen and carbon dioxide by photosynthetic bacteria (PSB) during anaerobic photo fermentation [Eq. (12)] [38]. Both nitrogenase and hydrogenase are detected in PSB. However, nitrogenase is the key enzyme that catalyzes molecular hydrogen formation. Typical bacteria genera that are related with photo fermentation are Rhodobacter, Rhodopseudomonas, and Rhodospirillum [9]. Based on Eqs. (3)–(7) and (12), the overall reactions of glucose, xylose, glutamic acid, and glycerol are shown in Eqs. (13) [38], (14), (15), and (16), respectively. The stoichiometric hydrogen yield of glucose is improved from 497.8 mL H2/g glucose (4 mol H2/mol glucose) by single-stage dark fermentation to 1493.3 mL H2/g glucose (12 mol H2/mol glucose) by two-stage dark fermentation

224

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Table 7 Combination of dark fermentation, photo fermentation, and anaerobic digestion to enhance energy production from biomass Fermentation type

Substrate

Dark fermentation þphoto fermentation Dark fermentation þphoto fermentation

Glucose

Dark fermentation þphoto fermentation Dark fermentation þphoto fermentation Dark fermentation þphoto fermentation Dark fermentation þphoto fermentation Dark fermentation þphoto fermentation þanaerobic digestion Dark fermentation þphoto fermentation þanaerobic digestion Dark fermentation þphoto fermentation þanaerobic digestion Dark fermentation þphoto fermentation þanaerobic digestion Dark fermentation þphoto fermentation þanaerobic digestion Dark fermentation þanaerobic digestion Dark fermentation þanaerobic digestion Dark fermentation þanaerobic digestion Dark fermentation þanaerobic digestion Dark fermentation þanaerobic digestion a b c

Inoculum

Clostridium butyricum þRhodopseudomonas palustris Cassava starch Heat-pretreated anaerobic digestion sludgeþRhodopseudomonas palustris Cassava starch Heat-pretreated anaerobic digestion sludgeþ immobilized mixed photosynthetic bacteria Arthrospira Heat-pretreated and platensis domesticated anaerobic digestion sludgeþ mixed photosynthetic bacteria Eichhornia Heat-pretreated anaerobic crassipes (Water digestion sludgeþ immobilized hyacinth) Rhodopseudomonas palustris Heat-pretreated anaerobic Eichhornia crassipes (water digestion sludgeþ immobilized mixed photosynthetic bacteria hyacinth) Trehalose Heat-pretreated anaerobic digestion sludgeþ mixed photosynthetic bacteriaþanaerobic digestion sludge Glutamic acid Heat-pretreated anaerobic digestion sludgeþ mixed photosynthetic bacteriaþanaerobic digestion sludge Nannochloropsis Heat-pretreated anaerobic oceanica digestion sludgeþ mixed photosynthetic bacteriaþanaerobic digestion sludge Chlorella Heat-pretreated anaerobic pyrenoidosa digestion sludgeþ mixed photosynthetic bacteriaþanaerobic digestion sludge Heat-pretreated anaerobic Chlorella pyrenoidosa and digestion sludgeþ mixed photosynthetic cassava starch bacteriaþanaerobic digestion sludge Glucose Heat-pretreated anaerobic digestion sludgeþ anaerobic digestion sludge Xylose Heat-pretreated and domesticated anaerobic digestion sludgeþ anaerobic digestion sludge Lipid-extracted Heat-pretreated anaerobic Scenedesmus sp. digestion sludgeþ anaerobic digestion sludge Residues Arthrospira Heat-pretreated and maxima domesticated anaerobic digestion sludgeþ anaerobic digestion sludge Heat-pretreated anaerobic Eichhornia crassipes (water digestion sludgeþ anaerobic digestion sludge hyacinth)

Dark H2 yield (mL H2/g VS)

Energy yield of dark H2 (kJ/g VS)b

Photo H2 yield (mL H2/g VS)

Energy yield of photo H2 (kJ/g VS)b

CH4 yield (mL CH4/g VS)

Energy yield of CH4 (kJ/g VS)c

Total energy yield (kJ/g VS)

Enhancement compared with dark fermentation (time)

Reference

164.3

2.1

517.7

6.6

–

–

8.7

4.2

[38]

276.1

3.5

126.1

1.6

–

–

5.1

1.5

[80]

351.0

4.5

489.0

6.2

–

–

10.7

2.4

[74]

98.5a

1.3

256.2

3.3

–

–

4.5

3.6

[104]

73.5

0.9

522.6

6.7

–

–

7.6

8.1

[44]

112.3

1.4

639.3

8.2

–

–

9.6

6.7

[72]

396.2

5.1

335.1

4.3

116.9

4.6

14.0

2.8

[78]

–

–

292.0

3.7

102.7

4.1

7.8

–

[59]

39.0

0.5

144.9

1.9

161.3

6.4

8.7

17.6

[45]

75.6

1.0

122.7

1.6

186.2

7.4

9.9

10.3

[11]

276.2

3.5

388.0

5.0

126.0

5.0

13.5

3.8

[14]

342.2

4.4

–

–

265.1

10.5

14.9

3.4

[77]

190.6

2.4

–

–

216.5

8.6

11.0

4.5

[83]

46.0

0.6

–

–

393.6 15.6

16.2

27.6

[109]

82.8

1.1

–

–

115.3

4.6

5.6

5.3

[113]

51.7

0.7

–

–

143.4

5.7

6.4

9.6

[73]

Components of algae dry biomass is assumed to be composed of 95% VS and 5% ash. Higher heating value of hydrogen (286 kJ/mol) is used in calculation of energy yield for dark fermentation and photo fermentation. Higher heating value of hydrogen (889 kJ/mol) is used in calculation of energy yield for anaerobic digestion.

and photo fermentation, the stoichiometric hydrogen yield of xylose is improved from 497.8 mL H2/g xylose (10/3 mol H2/mol xylose) to 1493.3 mL H2/g xylose (10 mol H2/mol xylose), the

stoichiometric hydrogen yield of glutamic acid is improved from 0 to 1371.4 mL H2/g glutamic acid (9 mol H2/mol glutamic acid), and the stoichiometric hydrogen yield of glycerol is improved from

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

730.4 mL H2/g glycerol (3 mol H2/mol glycerol) to 1704.3 mL/g glycerol (7 mol H2/mol glycerol). CH3 COOH þ 2H2 O-2CO2 þ 4H2

ð12Þ

C6 H12 O6 þ 6H2 O-6CO2 þ 12H2

ð13Þ

C5 H10 O5 þ 5H2 O-5CO2 þ 10H2

ð14Þ

C5 H9 NO4 þ 6H2 O-5CO2 þ NH3 þ 9H2

ð15Þ

C3 H8 O3 þ 3H2 O-3CO2 þ 7H2

ð16Þ

Studies reported that PSB can directly use SMPs in supernatant of dark fermentation for efficient photo hydrogen production using glucose, cassava, water hyacinth with low, or no protein content as substrates in dark fermentation (Table 7). However, when algal biomass with high protein content is used as the substrate, ammonium [formed from ammonia under an acidic condition as shown in Eq. (17)] is produced in excess in the supernatant under dark fermentation, which seriously inhibits the activity of the key enzyme (i.e., nitrogenase) of PSB responsible for hydrogen production [139]. Cheng et al. found that hydrogen yield is near zero during photo fermentation using supernatant of dark fermentation from A. platensis because of ammonium inhibition. Zeolite can efficiently remove ammonium by selective ion exchange with little influence on SMPs in supernatant of dark fermentation. After zeolite treatment, SMPs can be used in PSB efficiently for photo hydrogen production, and the overall hydrogen yield from A. platensis is enhanced from 98.5 mL H2/g VS by single-stage dark fermentation to 354.7 mL H2/g VS by two-stage dark fermentation and photo fermentation [104]. NH3 þ H þ -NH4 þ

ð17Þ

4.3. Subsequent anaerobic digestion for methane co-generation High-molecular weight residues in effluent of dark fermentation (such as biomass residues and LCFAs) can hardly be used by PSB during photo fermentation. Such residues can be used by MPB for methane production to enhance total energy yield from algal biomass by subsequent anaerobic digestion [11,43,45,140]. As shown in Table 7, the overall hydrogen and methane yields by three-stage dark fermentation, photo fermentation, and anaerobic digestion are 183.9 mL H2/g VS and 161.3 mL CH4/g VS for N. oceanica, 198.3 mL H2/g VS and 186.2 mL CH4/g VS for C. pyrenoidosa, 664.2 mL H2/g VS and 126.0 mL CH4/g VS for mixed C. pyrenoidosa and cassava starch, which correspond to 3.8–17.6 time increases in total energy yields (8.7–13.5 kJ/g VS) compare with those in single-stage dark fermentation [11,14,45]. Effluent of dark fermentation can be used directly to cogenerate methane by MPB by subsequent anaerobic digestion, which is also a cost-effective method to improve energy yield from algal biomass. The overall yields of hydrogen and methane by two-stage dark fermentation and anaerobic digestion are 82.8 mL H2/g VS and 115.3 mL CH4/g VS for A. maxima, 46.0 mL H2/g VS and 393.6 mL CH4/g VS for lipid-extracted Scenedesmus sp. residues, which correspond to 5.3–27.6 time increases in total energy yields (5.6–16.2 kJ/g VS) compared with single-stage dark fermentation [109,113]. A few studies have been carried out to analyze the mass balance of the two-stage dark fermentation and anaerobic digestion [141–143]. Monlau et al. reported 10.7–13.8%, 23.9–28.3%, and 49.4–58.4% of the substrates (based on the mass percentage of VS) are converted to gas fuels (hydrogen and methane), carbon dioxide, and digestate (sludge), respectively [141]. The digestate can be used as a valuable fertilizer, because of the improved availability of nitrogen and significant short-term fertilization

225

effect [144]. Jung et al. used L. japonica as a substrate to produce fermentative hydrogen and methane. They reported that the 7.1%, 73.8% and 10.6% of the substrates (based on COD) are converted to hydrogen, methane, and residue sludge, respectively [142]. Giordano et al. suggested that 2.9–22.8% and 18.9–88.5% of the substrates (based on COD) are fermented to hydrogen and methane, respectively [143]. 4.4. Dark fermentation as a platform for the production of biofuels and biochemicals Alternatively, effluent of dark fermentation, which is rich in VFAs, has the potential to be used (1) for direct electricity generation in microbial fuel cells [145], (2) as substrates for biodiesel production by microalgae and yeasts [146,147], (3) as substrates for polyhydroxyalkanoate production [148], (4) as additional carbon sources for wastewater denitrification [149,150], and (5) for the production of various chemicals, such as alcohols, aldehydes, and esters [39,151]. 4.5. Impurities in biogas The raw biogas may comprise various impurities, such as abundant carbon dioxide (e.g., 25–50%), and small amounts of hydrogen sulfide, ammonia, water, nitrogen, oxygen, carbon monoxide, siloxanes, halogenated hydrocarbons, and organic sulfur molecules, which are dependent on the substrate compositions and process operation. A cleaning process (to remove trace components harmful to the natural gas grid and engine) and upgrading process (to remove carbon dioxide to improve the heating value) are required to meet the standard for grid injection or use as transport fuel [152]. However, if the biogas is directly used for combustion or combined heat and power generation, carbon dioxide, nitrogen, and oxygen may be retained in the biogas. The biogas cleaning and upgrading processes are mature. They have been commercialized in many countries, such as Germany and Sweden [153].

5. Efficient hydrogen fermentation from algal biomass 5.1. Hydrogen fermentation of algal biomass at optimized components Although combined dark fermentation and photo fermentation can theoretically enhance hydrogen yield and reduce energy waste in effluent of dark fermentation, this method have some challenges when algal biomass is used as substrate. Firstly, protein content in algal biomass is too high for dark fermentation, leading to low dark hydrogen yield and excess ammonium, which inhibits subsequent photo fermentation [59]. Optimization of growth conditions (e.g., nitrogen starving and sodium stress) to accumulate carbohydrates of algal biomass and co-fermentation of algal biomass and waste biomass rich in carbohydrates can solve this problem [14,46,66]. Secondly, extracellular LCFAs from lipids cannot be used in dark fermentation or in photo fermentation [9,43,63,140]. Furthermore, LCFAs exhibit inhibitory effect on hydrogen fermentation [154]. Therefore, removal of LCFAs before hydrogen fermentation is desired. Combined lipid extraction and hydrogen fermentation is a solution to this issue, because LCFAs in lipids are extracted and used to produce biodiesel, and residual glycerol is readily used for efficient hydrogen fermentation [62]. We propose a method for efficient conversion of algal biomass to hydrogen. This method comprises pretreatment, dark fermentation, and photo fermentation (Fig. 5). In the first step, algal biomass (or mixed biomass) at appropriate C/N ratio is pretreated

226

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

Fig. 5. Flowchart of efficient conversion from algal biomass to hydrogen. Table 8 Comparison of dark fermentation, photo fermentation, and anaerobic digestion Elements

Dark fermentation

Photo fermentation

Anaerobic digestion

Main substrates Main products Gas biofuel yield Gross energy yield of gas biofuela Volumetric energy production rate of gas biofuel Light requirement Continuous operation Operation cost pH adjustment Technology

Carbohydrates, proteins, and glycerol Hydrogen, volatile fatty acids, and carbon dioxide 4 mol H2/mol glucose Low (6.4 kJ/g glucose) High No Easy Medium Necessary Pilot

Sugars and volatile fatty acids Hydrogen and carbon dioxide 12 mol H2/mol glucose High (19.1 kJ/g glucose) Low Yes Hard High Optional Pilot

Organic materials Methane and carbon dioxide 3 mol CH4/mol glucose High (14.8 kJ/g glucose) Medium No Easy Low Optional Mature

a

Higher heating values of hydrogen (286 kJ/mol) and methane (889 kJ/mol) are used in calculation of gross energy yield.

with an efficient methods to convert high-molecular weight polymers to low-molecular weight monomers. Monosaccharides and amino acids are obtained by hydrolysis of carbohydrates and proteins, respectively, and glycerol is obtained by transesterification of lipids [45,62]. In the second stage, monomers are fermented by HPB to produce hydrogen, SMPs (e.g., acetate, butyrate, and ethanol), and ammonia, which is further converted to ammonium in acidic condition [114]. Zeolite treatment is recommended if ammonium concentration reaches the inhibitory level of photo fermentation [104]. In the third stage, SMPs are fermented by PSB to produce hydrogen [11]. In general, the fermentable biomass can be totally converted to hydrogen, carbon dioxide, and ammonia [Eq. (18)].   b 3 Ca Hb Nc Od þ ð2a  dÞH2 O-aCO2 þcNH3 þ 2a þ  c  d H2 ð18Þ 2 2 5.2. Challenges of fermentative hydrogen production for large-scale applications Table 8 presents a brief comparison of dark fermentation, photo fermentation, and anaerobic digestion. Anaerobic digestion is a mature technology with a low operation cost. It has been widely used for large-scale biogas production in European and Asian countries [155,156]. There are a few demonstration projects on biogas production from waste algal biomass. A 2500 m3 anaerobic digester has been built to treat waste biomass from microalgal bloom in Taihu Lake, Wuxi, China. The harvested microalgal biomass is co-digested with swine manure to produce biogas, which can further power a 400 kW electricity generator. A pilot project in Sweden has been established to harvest drifting filamentous macroalgae from shorelines in Baltic Sea. The harvested macroalgal biomass may be used for biogas production [157].

In contrast, hydrogen fermentation has not been commercialized [158]. In dark fermentation, the additional alkali to maintain the optimal pH during dark fermentation may significantly increase the operation cost and reduce the economic feasibility [159]. The recirculation of effluents of subsequent anaerobic digestion and/or photo fermentation can effectively reduce the external alkali requirement [142]. In photo fermentation, the light supply is a major constraint for its application. The development of novel technology for effective illumination and light distribution is an important strategy to improve photo hydrogen production. Furthermore, hydrogen fermentation may also be affected by the accumulation of end-products and shift of bacterial community and metabolic pathway [40]. More studies on metabolic/genetic engineering and process engineering are necessary to improve the efficiency and stability of hydrogen fermentation. 5.3. Potential of fermentative hydrogen production from algal biomass in China According to Statistical Review of World Energy 2013, China is the largest energy consumer, accounting for 21.9% of the world's total primary energy demand in 2012. The total consumption of oil and natural gas of China is 613.2 million ton oil equivalent (2.575  1016 kJ). If petroleum and natural gas are totally replaced by hydrogen (higher heating value: 286 kJ/mol), then the total volume of hydrogen demand is 2.017  1015 L. If hydrogen is produced from algal biomass by the combined dark fermentation and photo fermentation method [the stoichiometric hydrogen yield of fermentable components is assumed to be 1537.9 mL H2/ g VS (L H2/kg VS) based on the median stoichiometric values of glucose, xylose, glutamic acid, and glycerol (1371.4–1704.3 mL H2/ g VS) as shown in Section 4.2] and 30% of stoichiometric hydrogen yield can be obtained by current technology, then the total algal

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biomass demand is 4.372  109 t VS. Considering the annual productivity of algal biomass (26,300 t DW/km2), in which 75% of components is assumed to be fermentable components, the total area required for algae cultivation is 2.216  105 km2, equal to 2.3% of total land area or 7.4% total sea area of China. Given the stoichiometric potential of hydrogen production from algal biomass (100% stoichiometric hydrogen yield of algal biomass is achieved), and then total area requirement decreases to 0.7% of land area or 2.2% of sea area. This type of energy harvesting from algal biomass could be very beneficial to the Chinese energy situation. However, this potential is a theoretical value, and does not consider the energy demand of algal biogas fermentation, such as harvesting, transport, storage (e.g., ensiling), biogas production, biogas upgrading, and digestate handing. The energy analysis for whole process of hydrogen fermentation (combined dark and photo fermentation) from algal biomass has been rarely reported. A recent study by Risen et al. indicated the whole process of biogas production from waste macroalgae in the Baltic Sea consumes 30– 40% of energy content in biogas [157]. More studies on mass, energy and economical balances of the whole process should be carried out in the future.

6. Conclusion Stoichiometric hydrogen yields by dark fermentation depend on the contents of monosaccharides and glycerol in algal biomass. Dark hydrogen yields of algal biomass can be remarkably enhanced to 50–70% of theoretical values by efficient pretreatments (e.g., steam heating with dilute acid and ultrasonication) at optimized biomass C/N ratios (e.g., 15–25) using domesticated HPB as the inoculum. Subsequent photo fermentation and anaerobic digestion can significantly enhance the total energy yield to 16.2 kJ/g VS. Potential algal feedstock for industrial fermentative hydrogen production could be obtained from (1) naturally grown waste algal biomass (e.g., algal bloom), (2) algal biomass grown in waste water or flue gas from thermal power plant, and (3) residual algal biomass after lipid and valuable component extraction. Furthermore, wet biomass of microalgae is recommended for future study in continuous systems.

Acknowledgments This study is supported by the National Natural Science Foundation-China (51176163), National High Technology R&D Program-China (2012AA050101), International Sci. & Tech. Cooperation Program-China (2012DFG61770), Zhejiang Provincial Natural Science Foundation-China (LR14E060002), Program for New Century Excellent Talents in University-China (NCET-11–0446), Specialized Research Fund for the Doctoral Program of Higher Education-China (20110101110021), Science and Technology Project of Guangxi Province-China (1346011-1). The authors wish to thank the reviewers for their insightful comments on this paper. References [1] Demirbas A. Progress and recent trends in biofuels. Prog Energy Combust Sci 2007;33:1–18. [2] John RP, Anisha GS, Nampoothiri KM, Pandey A. Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 2011;102: 186–93. [3] Verhelst S, Wallner T. Hydrogen-fueled internal combustion engines. Prog Energy Combust Sci 2009;35:490–527. [4] Cai G, Jin B, Monis P, Saint C. Metabolic flux network and analysis of fermentative hydrogen production. Biotechnol Adv 2011;29:375–87. [5] Navarro RM, Sanchez-Sanchez MC, Alvarez-Galvan MC, del Valle F, Fierro JLG. Hydrogen production from renewable sources: biomass and photocatalytic opportunities. Energy Environ Sci 2009;2:35–54.

227

[6] Bahadar A, Khan MB. Progress in energy from microalgae: a review. Renew Sustain Energy Rev 2013;27:128–48. [7] Holladay JD, Hu J, King DL, Wang Y. An overview of hydrogen production technologies. Catal Today 2009;139:244–60. [8] Liao Q, Wang Y-J, Wang Y-Z, Zhu X, Tian X, Li J. Formation and hydrogen production of photosynthetic bacterial biofilm under various illumination conditions. Bioresour Technol 2010;101:5315–24. [9] Argun H, Kargi F. Bio-hydrogen production by different operational modes of dark and photo-fermentation: an overview. Int J Hydrog Energy 2011;36: 7443–59. [10] Cheng J, Xia A, Song W, Su H, Thou J, Cen K. Comparison between heterofermentation and autofermentation in hydrogen production from Arthrospira (Spirulina) platensis wet biomass. Int J Hydrog Energy 2012;37: 6536–44. [11] Xia A, Cheng J, Ding L, Lin R, Huang R, Zhou J, et al. Improvement of the energy conversion efficiency of Chlorella pyrenoidosa biomass by a threestage process comprising dark fermentation, photofermentation, and methanogenesis. Bioresour Technol 2013;146:436–43. [12] Akutsu Y, Li Y-Y, Harada H, Yu H-Q. Effects of temperature and substrate concentration on biological hydrogen production from starch. Int J Hydrog Energy 2009;34:2558–66. [13] Yang H, Shen J. Effect of ferrous iron concentration on anaerobic biohydrogen production from soluble starch. Int J Hydrog Energy 2006;31: 2137–46. [14] Xia A, Cheng J, Ding L, Lin R, Song W, Zhou J, et al. Enhancement of energy production efficiency from mixed biomass of Chlorella pyrenoidosa and cassava starch through combined hydrogen fermentation and methanogenesis. Appl Energy 2014;120:23–30. [15] Kiran B, Kumar R, Deshmukh D. Perspectives of microalgal biofuels as a renewable source of energy. Energy Convers Manag 2014;88:1228–44. [16] Nigam PS, Singh A. Production of liquid biofuels from renewable resources. Prog Energy Combust Sci 2011;37:52–68. [17] Jones CS, Mayfieldt SP. Algae biofuels: versatility for the future of bioenergy. Curr Opin Biotechnol 2012;23:346–51. [18] Sialve B, Bernet N, Bernard O. Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable. Biotechnol Adv 2009;27:409–16. [19] Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC. Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 2008;19:235–40. [20] Wei N, Quarterman J, Jin Y-S. Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol 2013;31:70–7. [21] Demirbas A. Use of algae as biofuel sources. Energy Convers Manag 2010;51:2738–49. [22] Becker EW. Micro-algae as a source of protein. Biotechnol Adv 2007;25: 207–10. [23] Chisti Y. Biodiesel from microalgae. Biotechnol Adv 2007;25:294–306. [24] Gai C, Zhang YYN, Chen W-T, Zhang P, Dong Y. Thermogravimetric and kinetic analysis of thermal decomposition characteristics of low-lipid microalgae. Bioresour Technol 2013;150:139–48. [25] Yu G, Zhang Y, Schideman L, Funk T, Wang Z. Distributions of carbon and nitrogen in the products from hydrothermal liquefaction of low-lipid microalgae. Energy Environ Sci 2011;4:4587–95. [26] Ziolkowska JR, Simon L. Recent developments and prospects for algae-based fuels in the US. Renew Sustain Energy Rev 2014;29:847–53. [27] Rashid N, Rehman MSU, Memon S, Rahman ZU, Lee K, Han JI. Current status, barriers and developments in biohydrogen production by microalgae. Renew Sustain Energy Rev 2013;22:571–9. [28] Miao H, Lu M, Zhao M, Huang Z, Ren H, Yan Q, et al. Enhancement of Taihu blue algae anaerobic digestion efficiency by natural storage. Bioresour Technol 2013;149:359–66. [29] Markou G, Nerantzis E. Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol Adv 2013;31:1532–42. [30] Ehimen EA, Connaughton S, Sun Z, Carrington GC. Energy recovery from lipid extracted, transesterified and glycerol codigested microalgae biomass. GCB Bioenergy 2009;1:371–81. [31] Batista AP, Moura P, Marques PASS, Ortigueira J, Alves L, Gouveia L. Scenedesmus obliquus as feedstock for biohydrogen production by Enterobacter aerogenes and Clostridium butyricum. Fuel 2014;117:537–43. [32] Park J-H, Cheon H-C, Yoon J-J, Park H-D, Kim S-H. Optimization of batch dilute-acid hydrolysis for biohydrogen production from red algal biomass. Int J Hydrog Energy 2013;38:6130–6. [33] Liu C-H, Chang C-Y, Cheng C-L, Lee D-J, Chang J-S. Fermentative hydrogen production by Clostridium butyricum CGS5 using carbohydrate-rich microalgal biomass as feedstock. Int J Hydrog Energy 2012;37:15458–64. [34] Yan Q, Wang A, Yu C, Ren N, Zhang Y, Zhang G. Enzymatic characterization of acid tolerance response (ATR) during the enhanced biohydrogen production process from Taihu cyanobacteria via anaerobic digestion. Int J Hydrog Energy 2011;36:405–10. [35] Choi J-A, Hwang J-H, Dempsey BA, Abou-Shanab RAI, Min B, Song H, et al. Enhancement of fermentative bioenergy (ethanol/hydrogen) production using ultrasonication of Scenedesmus obliquus YSW15 cultivated in swine wastewater effluent. Energy Environ Sci 2011;4:3513–20. [36] Efremenko EN, Nikolskaya AB, Lyagin IV AB, Senko OV, Makhlis TA, Stepanov NA, et al. Production of biofuels from pretreated microalgae biomass by

228

[37]

[38]

[39]

[40]

[41]

[42] [43] [44]

[45]

[46]

[47] [48]

[49]

[50]

[51] [52]

[53] [54] [55]

[56]

[57]

[58]

[59]

[60]

[61]

[62] [63]

[64]

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

anaerobic fermentation with immobilized Clostridium acetobutylicum cells. Bioresour Technol 2012;114:342–8. Ferreira AF, Ortigueira J, Alves L, Gouveia L, Moura P, Silva CM. Energy requirement and CO2 emissions of bioH2 production from microalgal biomass. Biomass Bioenergy 2013;49:249–59. Su H, Cheng J, Zhou J, Song W, Cen K. Combination of dark- and photofermentation to enhance hydrogen production and energy conversion efficiency. Int J Hydrog Energy 2009;34:8846–53. Motte J-C, Sambusiti C, Dumas C, Barakat A. Combination of dry dark fermentation and mechanical pretreatment for lignocellulosic deconstruction: an innovative strategy for biofuels and volatile fatty acids recovery. Appl Energy 2015;147:67–73. Hay JXW, Wu TY, Juan JC, Jahim JM. Biohydrogen production through photo fermentation or dark fermentation using waste as a substrate: overview, economics, and future prospects of hydrogen usage. Biofuels Bioprod Biorefining 2013;7:334–52. Maru BT, Bielen AAM, Constanti M, Medina F, Kengen SWM. Glycerol fermentation to hydrogen by Thermotoga maritima: proposed pathway and bioenergetic considerations. Int J Hydrog Energy 2013;38:5563–72. Pawar SS, van Niel EWJ. Thermophilic biohydrogen production: how far are we? Appl Microbiol Biotechnol 2013;97:7999–8009. Wellinger A, Murphy JD, Baxter D. The Biogas Handbook: Science, Production and Applications. Woodhead Publishing; 2013. Su H, Cheng J, Zhou J, Song W, Cen K. Hydrogen production from water hyacinth through dark- and photo- fermentation. Int J Hydrog Energy 2010;35:8929–37. Xia A, Cheng J, Lin R, Lu H, Zhou J, Cen K. Comparison in dark hydrogen fermentation followed by photo hydrogen fermentation and methanogenesis between protein and carbohydrate compositions in Nannochloropsis oceanica biomass. Bioresour Technol 2013;138:204–13. Carrieri D, Momot D, Brasg IA, Ananyev G, Lenz O, Bryant DA, et al. Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl Environ Microbiol 2010;76:6455–62. Klaehn S, Hagemann M. Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 2011;13:551–62. Nguyen T-AD, Kim K-R, Nguyen M-T, Kim MS, Kim D, Sim SJ. Enhancement of fermentative hydrogen production from green algal biomass of Thermotoga neapolitana by various pretreatment methods. Int J Hydrog Energy 2010;35: 13035–40. Temudo MF, Poldermans R, Kleerebezem R, van Loosdrecht MCM. Glycerol fermentation by (open) mixed cultures: a chemostat study. Biotechnol Bioeng 2008;100:1088–98. Cooksley CM, Zhang Y, Wang H, Redl S, Winzer K, Minton NP. Targeted mutagenesis of the Clostridium acetobutylicum acetone-butanol-ethanol fermentation pathway. Metab Eng 2012;14:630–41. Lee H-S, Salerno MB, Rittmann BE. Thermodynamic evaluation on H2 production in glucose fermentation. Environ Sci Technol 2008;42:2401–7. Song W, Cheng J, Zhao J, Carrieri D, Zhang C, Zhou J, et al. Improvement of hydrogen production by over-expression of a hydrogen-promoting protein gene in Enterobacter cloacae. Int J Hydrog Energy 2011;36:6609–15. Jung KA, Lim S-R, Kim Y, Park JM. Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 2013;135:182–90. Chen C-Y, Zhao X-Q, Yen H-W, Ho S-H, Cheng C-L, Lee D-J, et al. Microalgaebased carbohydrates for biofuel production. Biochem Eng J 2013;78:1–10. Jung K-W, Kim D-H, Shin H-S. Fermentative hydrogen production from Laminaria japonica and optimization of thermal pretreatment conditions. Bioresour Technol 2011;102:2745–50. Markou G, Angelidaki I, Georgakakis D. Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biotechnol 2012;96:631–45. Temudo MF, Mato T, Kleerebezem R, van Loosdrecht MCM. Xylose anaerobic conversion by open-mixed cultures. Appl Microbiol Biotechnol 2009;82: 231–9. Lay C-H, Sen B, Chen C-C, Wu J-H, Lee S-C, Lin C-Y. Co-fermentation of water hyacinth and beverage wastewater in powder and pellet form for hydrogen production. Bioresour Technol 2013;135:610–5. Xia A, Cheng J, Lin R, Liu J, Zhou J, Cen K. Sequential generation of hydrogen and methane from glutamic acid through combined photo-fermentation and methanogenesis. Bioresour Technol 2013;131:146–51. Kobayashi T, Xu K-Q, Li Y-Y, Inamori Y. Evaluation of hydrogen and methane production from municipal solid wastes with different compositions of fat, protein, cellulosic materials and the other carbohydrates. Int J Hydrog Energy 2012;37:15711–8. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008;54:621–39. Mata TM, Martins AA, Caetano NS. Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 2010;14:217–32. Oh ST, Martin AD. Long chain fatty acids degradation in anaerobic digester: thermodynamic equilibrium consideration. Process Biochem. 2010;45: 335–45. Seifert K, Waligorska M, Wojtowski M, Laniecki M. Hydrogen generation from glycerol in batch fermentation process. Int J Hydrog Energy 2009;34: 3671–8.

[65] Nakashimada Y, Rachman MA, Kakizono T, Nishio N. Hydrogen production of Enterobacter aerogenes altered by extracellular and intracellular redox states. Int J Hydrog Energy 2002;27:1399–405. [66] Aoyama K, Uemura I, Miyake J, Asada Y. Fermentative metabolism to produce hydrogen gas and organic compounds in a cyanobacterium Spirulina platensis. J Ferment Bioeng 1997;83:17–20. [67] Liu Z-Y, Wang G-C, Zhou B-C. Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 2008;99:4717–22. [68] Lv J-M, Cheng L-H, Xu X-H, Zhang L, Chen H-L. Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 2010;101:6797–804. [69] Fernandes B, Teixeira J, Dragone G, Vicente AA, Kawano S, Bisova K, et al. Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour Technol 2013;144:268–74. [70] Malik A. Environmental challenge vis a vis opportunity: the case of water hyacinth. Environ Int 2007;33:122–38. [71] Chuang Y-S, Lay C-H, Sen B, Chen C-C, Gopalakrishnan K, Wu J-H, et al. Biohydrogen and biomethane from water hyacinth (Eichhornia crassipes) fermentation: effects of substrate concentration and incubation temperature. Int J Hydrog Energy 2011;36:14195–203. [72] Cheng J, Xia A, Su H, Song W, Zhou J, Cen K. Promotion of H2 production by microwave-assisted treatment of water hyacinth with dilute H2SO4 through combined dark fermentation and photofermentation. Energy Convers Manag 2013;73:329–34. [73] Cheng J, Xie B, Zhou J, Song W, Cen K. Cogeneration of H2 and CH4 from water hyacinth by two-step anaerobic fermentation. Int J Hydrog Energy 2010;35:3029–35. [74] Cheng J, Su H, Zhou J, Song W, Cen K. Hydrogen production by mixed bacteria through dark and photo fermentation. Int J Hydrog Energy 2011;36:450–7. [75] Zhao C, Karakashev D, Lu W, Wang H, Angelidaki I. Xylose fermentation to biofuels (hydrogen and ethanol) by extreme thermophilic (70 1C) mixed culture. Int J Hydrog Energy 2010;35:3415–22. [76] Zamalloa C, Boon N, Verstraete W. Anaerobic digestibility of Scenedesmus obliquus and Phaeodactylum tricornutum under mesophilic and thermophilic conditions. Appl Energy 2012;92:733–8. [77] Xie B, Cheng J, Zhou J, Song W, Cen K. Cogeneration of hydrogen and methane from glucose to improve energy conversion efficiency. Int J Hydrog Energy 2008;33:5006–11. [78] Xia A, Cheng J, Lin R, Ding L, Zhou J, Cen K. Combination of hydrogen fermentation and methanogenesis to enhance energy conversion efficiency from trehalose. Energy 2013;55:631–7. [79] Lin CY, Cheng CH. Fermentative hydrogen production from xylose using anaerobic mixed microflora. Int J Hydrog Energy 2006;31:832–40. [80] Su H., Cheng J., Zhou J., Song W., Cen K. Improving hydrogen production from cassava starch by combination of dark and photo fermentation. Int J Hydrog Energy. 2009;34:1780-1786. [81] de Vrije T, Mars AE, Budde MAW, Lai MH, Dijkema C, de Waard sP, et al. Glycolytic pathway and hydrogen yield studies of the extreme thermophile Caldicellulosiruptor saccharolyticus. Appl Microbiol Biotechnol 2007;74:1358–67. [82] Lin C-Y, Wu C-C, Hung C-H. Temperature effects on fermentative hydrogen production from xylose using mixed anaerobic cultures. Int J Hydrog Energy 2008;33:43–50. [83] Cheng J, Song W, Xia A, Su H, Thou J, Cen K. Sequential generation of hydrogen and methane from xylose by two-stage anaerobic fermentation. Int J Hydrog Energy 2012;37:13323–9. [84] Lo Y-C, Chen X-J, Huang C-Y, Yuan Y-J, Chang J-S. Dark fermentative hydrogen production with crude glycerol from biodiesel industry using indigenous hydrogen-producing bacteria. Int J Hydrog Energy 2013;38:15815–22. [85] Varrone C, Rosa S, Fiocchetti F, Giussani B, Izzo G, Massini G, et al. Enrichment of activated sludge for enhanced hydrogen production from crude glycerol. Int J Hydrog Energy 2013;38:1319–31. [86] Reungsang A, Sittijunda S, Angelidaki I. Simultaneous production of hydrogen and ethanol from waste glycerol by Enterobacter aerogenes KKU-S1. Int J Hydrog Energy 2013;38:1813–25. [87] Reungsang A, Sittijunda S, O-thong S. Bio-hydrogen production from glycerol by immobilized Enterobacter aerogenes ATCC 13048 on heat-treated UASB granules as affected by organic loading rate. Int J Hydrog Energy 2013;38: 6970–9. [88] Liu B, Christiansen K, Parnas R, Xu Z, Li B. Optimizing the production of hydrogen and 1,3-propanediol in anaerobic fermentation of biodiesel glycerol. Int J Hydrog Energy 2013;38:3196–205. [89] Ren N, Guo W, Liu B, Cao G, Ding J. Biological hydrogen production by dark fermentation: challenges and prospects towards scaled-up production. Curr Opin Biotechnol 2011;22:365–70. [90] Wang J, Wan W. Factors influencing fermentative hydrogen production: a review. Int J Hydrog Energy 2009;34:799–811. [91] Gavala HN, Skiadas IV HN, Ahring BK. Biological hydrogen production in suspended and attached growth anaerobic reactor systems. Int J Hydrog Energy 2006;31:1164–75. [92] Kongjan P, Angelidaki I. Extreme thermophilic biohydrogen production from wheat straw hydrolysate using mixed culture fermentation: effect of reactor configuration. Bioresour Technol 2010;101:7789–96. [93] Subhash GV, Mohan SV. Deoiled algal cake as feedstock for dark fermentative biohydrogen production: an integrated biorefinery approach. Int J Hydrog Energy 2014;39:9573–9.

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

[94] Yang Z, Guo R, Xu X, Fan X, Li X. Enhanced hydrogen production from lipidextracted microalgal biomass residues through pretreatment. Int J Hydrog Energy 2010;35:9618–23. [95] Yang Z, Guo R, Xu X, Fan X, Li X. Thermo-alkaline pretreatment of lipidextracted microalgal biomass residues enhances hydrogen production. J Chem Technol Biotechnol 2011;86:454–60. [96] Yang Z, Guo R, Xu X, Fan X, Luo S. Fermentative hydrogen production from lipid-extracted microalgal biomass residues. Appl Energy 2011;88:3468–72. [97] Nobre BP, Villalobos F, Barragan BE, Oliveira AC, Batista AP, PASS Marques, et al. A biorefinery from Nannochloropsis sp microalga – extraction of oils and pigments. Production of biohydrogen from the leftover biomass. Bioresour Technol 2013;135:128–36. [98] Jeon B-H, Choi J-A, Kim H-C, Hwang J-H, Abou-Shanab RAI, Dempsey BA, et al. Ultrasonic disintegration of microalgal biomass and consequent improvement of bioaccessibility/bioavailability in microbial fermentation. Biotechnol Biofuels 2013:6. [99] Lakaniemi A-M, Hulatt CJ, Thomas DN, Tuovinen OH, Puhakka JA. Biogenic hydrogen and methane production from Chlorella vulgaris and Dunaliella tertiolecta biomass. Biotechnol Biofuels 2011:4. [100] Sun J, Yuan X, Shi X, Chu C, Guo R, Kong H. Fermentation of Chlorella sp for anaerobic bio-hydrogen production: influences of inoculum-substrate ratio, volatile fatty acids and NADH. Bioresour Technol 2011;102:10480–5. [101] Ho K-L, Lee D-J, Su A, Chang J-S. Biohydrogen from cellulosic feedstock: dilution-to-stimulation approach. Int J Hydrog Energy 2012;37:15582–7. [102] Yun Y-M, Jung K-W, Kim D-H, Oh Y-K, Shin H-S. Microalgal biomass as a feedstock for bio-hydrogen production. Int J Hydrog Energy 2012;37: 15533–9. [103] Ferreira AF, Marques AC, Batista AP, PASS Marques, Gouveia L, Silva CM. Biological hydrogen production by Anabaena sp – yield, energy and CO2 analysis including fermentative biomass recovery. Int J Hydrog Energy 2012;37:179–90. [104] Cheng J, Xia A, Liu Y, Lin R, Zhou J, Cen K. Combination of dark- and photofermentation to improve hydrogen production from Arthrospira platensis wet biomass with ammonium removal by zeolite. Int J Hydrog Energy 2012;37: 13330–7. [105] Yan Q, Zhao M, Miao H, Ruan W, Song R. Coupling of the hydrogen and polyhydroxyalkanoates (PHA) production through anaerobic digestion from Taihu blue algae. Bioresour Technol 2010;101:4508–12. [106] Kumar K, Roy S, Das D. Continuous mode of carbon dioxide sequestration by C. sorokiniana and subsequent use of its biomass for hydrogen production by E. cloacae IIT-BT 08. Bioresour Technol 2013;145:116–22. [107] Xia A, Cheng J, Song W, Yu C, Zhou J, Cen K. Enhancing enzymatic saccharification of water hyacinth through microwave heating with dilute acid pretreatment for biomass energy utilization. Energy 2013;61:158–66. [108] Dipasquale L, d'Ippolito G, Gallo C, Vella FM, Gambacorta A, Picariello G, et al. Hydrogen production by the thermophilic eubacterium Thermotoga neapolitana from storage polysaccharides of the CO2-fixing diatom Thalassiosira weissflogii. Int J Hydrog Energy 2012;37:12250–7. [109] Yang Z, Guo R, Xu X, Fan X, Luo S. Hydrogen and methane production from lipidextracted microalgal biomass residues. Int J Hydrog Energy 2011;36:3465–70. [110] Cho S, Park S, Seon J, Yu J, Lee T. Evaluation of thermal, ultrasonic and alkali pretreatments on mixed-microalgal biomass to enhance anaerobic methane production. Bioresour Technol 2013;143:330–6. [111] Ometto F, Quiroga G, Psenicka P, Whitton R, Jefferson B, Villa R. Impacts of microalgae pre-treatments for improved anaerobic digestion: thermal treatment, thermal hydrolysis, ultrasound and enzymatic hydrolysis. Water Res. 2014;65:350–61. [112] Passos F, Ferrer I. Microalgae conversion to biogas: thermal pretreatment contribution on net energy production. Environ Sci Technol 2014;48:7171–8. [113] Cheng J, Zhang M, Song W, Xia A, Zhou J, Cen K. Cogeneration of hydrogen and methane from Arthrospira maxima biomass with bacteria domestication and enzymatic hydrolysis. Int J Hydrog Energy 2011;36:1474–81. [114] Xia A, Cheng J, Ding L, Lin R, Song W, Zhou J, et al. Effects of changes in microbial community on the fermentative production of hydrogen and soluble metabolites from Chlorella pyrenoidosa biomass in semi-continuous operation. Energy 2014;68:982–8. [115] Chen Y, Xiao N, Zhao Y, Mu H. Enhancement of hydrogen production during waste activated sludge anaerobic fermentation by carbohydrate substrate addition and pH control. Bioresour Technol 2012;114:349–56. [116] Shi X, Jung K-W, Kim D-H, Ahn Y-T, Shin H-S. Direct fermentation of Laminaria japonica for biohydrogen production by anaerobic mixed cultures. Int J Hydrog Energy 2011;36:5857–64. [117] Park J-I, Lee J, Sim SJ, Lee J-H. Production of hydrogen from marine macroalgae biomass using anaerobic sewage sludge microflora. Biotechnol Bioprocess Eng 2009;14:307–15. [118] Park J-H, Yoon J-J, Park H-D, Kim YJ, Lim DJ, Kim S-H. Feasibility of biohydrogen production from Gelidium amansii. Int J Hydrog Energy 2011;36:13997–4003. [119] Lauwers J, Appels L, Thompson IP, Degreve J, Van Impe JE, Dewil R. Mathematical modelling of anaerobic digestion of biomass and waste: power and limitations. Prog Energy Combust Sci 2013;39:383–402. [120] Lakaniemi A-M, Tuovinen OH, Puhakka JA. Anaerobic conversion of microalgal biomass to sustainable energy carriers – a review. Bioresour Technol 2013;135:222–31. [121] Mussgnug JH, Klassen V, Schlueter A, Kruse O. Microalgae as substrates for fermentative biogas production in a combined biorefinery concept. J Biotechnol 2010;150:51–6.

229

[122] Alzate ME, Muñoz R, Rogalla F, Fdz-Polanco F, Pérez-Elvira SI. Biochemical methane potential of microalgae biomass after lipid extraction. Chem Eng J 2014;243:405–10. [123] Hernandez D, Riano B, Coca M, Garcia-Gonzalez MC. Treatment of agroindustrial wastewater using microalgae-bacteria consortium combined with anaerobic digestion of the produced biomass. Bioresour Technol 2013;135: 598–603. [124] El-Mashad HM. Kinetics of methane production from the codigestion of switchgrass and Spirulina platensis algae. Bioresour Technol 2013;132: 305–12. [125] Zhao M-X, Ruan W-Q. Biogas performance from co-digestion of Taihu algae and kitchen wastes. Energy Convers Manag 2013;75:21–4. [126] Allen E, Browne J, Hynes S, Murphy JD. The potential of algae blooms to produce renewable gaseous fuel. Waste Manag 2013;33:2425–33. [127] Jard G, Marfaing H, Carrere H, Delgenes JP, Steyer JP, Dumas C. French Brittany macroalgae screening: composition and methane potential for potential alternative sources of energy and products. Bioresour Technol 2013;144:492–8. [128] Debowski M, Zielinski M, Grala A, Dudek M. Algae biomass as an alternative substrate in biogas production technologies – review. Renew Sustain Energy Rev 2013;27:596–604. [129] Gonzalez-Fernandez C, Sialve B, Bernet N, Steyer JP. Effect of organic loading rate on anaerobic digestion of thermally pretreated Scenedesmus sp biomass. Bioresour Technol 2013;129:219–23. [130] Park KY, Kweon J, Chantrasakdakul P, Lee K, Cha HY. Anaerobic digestion of microalgal biomass with ultrasonic disintegration. Int Biodeterior Biodegrad 2013;85:598–602. [131] Ras M, Lardon L, Bruno S, Bernet N, Steyer J-P. Experimental study on a coupled process of production and anaerobic digestion of Chlorella vulgaris. Bioresour Technol 2011;102:200–6. [132] Bruhn A, Dahl J, Nielsen HB, Nikolaisen L, Rasmussen MB, Markager S, et al. Bioenergy potential of Ulva lactuca: biomass yield, methane production and combustion. Bioresour Technol 2011;102:2595–604. [133] Keymer P, Ruffell I, Pratt S, Lant P. High pressure thermal hydrolysis as pretreatment to increase the methane yield during anaerobic digestion of microalgae. Bioresour Technol 2013;131:128–33. [134] Ehimen EA, Holm-Nielsen JB, Poulsen M, Boelsmand JE. Influence of different pre-treatment routes on the anaerobic digestion of a filamentous algae. Renew Energy 2013;50:476–80. [135] Gurung A, Van Ginkel SW, Kang W-C, Qambrani NA, Oh S-E. Evaluation of marine biomass as a source of methane in batch tests: a lab-scale study. Energy 2012;43:396–401. [136] Yen H-W, Brune DE. Anaerobic co-digestion of algal sludge and waste paper to produce methane. Bioresour Technol 2007;98:130–4. [137] Zhong W, Chi L, Luo Y, Zhang Z, Zhang Z, Wu W-M. Enhanced methane production from Taihu Lake blue algae by anaerobic co-digestion with corn straw in continuous feed digesters. Bioresour Technol 2013;134:264–70. [138] Wang M, Sahu AK, Rusten B, Park C. Anaerobic co-digestion of microalgae Chlorella sp and waste activated sludge. Bioresour Technol 2013;142:585–90. [139] Zheng GH, Wang L, Kang ZH. Feasibility of biohydrogen production from tofu wastewater with glutamine auxotrophic mutant of Rhodobacter sphaeroides. Renew Energy 2010;35:2910–3. [140] Batstone DJ, Keller J, Angelidaki I, Kalyuzhnyi SV, Pavlostathis SG, Rozzi A, et al. The IWA Anaerobic Digestion Model No 1 (ADM1). Water Sci Technol 2002;45:65–73. [141] Monlau F, Kaparaju P, Trably E, Steyer JP, Carrere H. Alkaline pretreatment to enhance one-stage CH4 and two-stage H2/CH4 production from sunflower stalks: mass, energy and economical balances. Chem Eng J 2015;260:377–85. [142] Jung K-W, Kim D-H, Shin H-S. Continuous fermentative hydrogen and methane production from Laminaria japonica using a two-stage fermentation system with recycling of methane fermented affluent. Int J Hydrog Energy 2012;37:15648–57. [143] Giordano A, Cantu C, Spagni A. Monitoring the biochemical hydrogen and methane potential of the two-stage dark-fermentative process. Bioresour Technol 2011;102:4474–9. [144] Weiland P. Biogas production: current state and perspectives. Appl Microbiol Biotechnol 2010;85:849–60. [145] Liu H, Cheng SA, Logan BE. Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environ Sci Technol 2005;39: 658–62. [146] Fontanille P, Kumar V, Christophe G, Nouaille R, Larroche C. Bioconversion of volatile fatty acids into lipids by the oleaginous yeast Yarrowia lipolytica. Bioresour Technol 2012;114:443–9. [147] Yang L, Tan X, Li D, Chu H, Zhou X, Zhang Y, et al. Nutrients removal and lipids production by Chlorella pyrenoidosa cultivation using anaerobic digested starch wastewater and alcohol wastewater. Bioresour Technol 2015;181:54–61. [148] Albuquerque MGE, Martino V, Pollet E, Averous L, Reis MAM. Mixed culture polyhydroxyalkanoate (PHA) production from volatile fatty acid (VFA)-rich streams: effect of substrate composition and feeding regime on PHA productivity, composition and properties. J Biotechnol 2011;151:66–76. [149] Elefsiniotis P, Wareham DG, Smith MO. Use of volatile fatty acids from an acid-phase digester for denitrification. J Biotechnol 2004;114:289–97. [150] Lee WS, Chua ASM, Yeoh HK, Ngoh GC. A review of the production and applications of waste-derived volatile fatty acids. Chem Eng J 2014;235: 83–99.

230

A. Xia et al. / Renewable and Sustainable Energy Reviews 51 (2015) 209–230

[151] Chang HN, Kim N-J, Kang J, Jeong CM. Biomass-derived volatile fatty acid platform for fuels and chemicals. Biotechnol Bioprocess Eng 2010;15:1–10. [152] Ryckebosch E, Drouillon M, Veruaeren H. Techniques for transformation of biogas to biomethane. Biomass Bioenergy 2011;35:1633–45. [153] Petersson A., Wellinger A. Biogas upgrading technologies – developments and innovations. IEA Bioenergy. 2009. [154] Pott RWM, Howe CJ, Dennis JS. Photofermentation of crude glycerol from biodiesel using Rhodopseudomonas palustris: comparison with organic acids and the identification of inhibitory compounds. Bioresour Technol 2013;130: 725–30. [155] Song Z, Zhang C, Yang G, Feng Y, Ren G, Han X. Comparison of biogas development from households and medium and large-scale biogas plants in rural China. Renew Sustain Energy Rev 2014;33:204–13.

[156] Borjesson P, Mattiasson B. Biogas as a resource-efficient vehicle fuel. Trends Biotechnol 2008;26:7–13. [157] Risen E, Tatarchenko O, Grondahl F, Malmstrom ME. Harvesting of drifting filamentous macroalgae in the Baltic Sea: an energy assessment. J Renew Sustain Energy 2014:6. [158] De Gioannis G, Muntoni A, Polettini A, Pomi R. A review of dark fermentative hydrogen production from biodegradable municipal waste fractions. Waste Manag 2013;33:1345–61. [159] Kraemer JT, Bagley DM. Continuous fermentative hydrogen production using a two-phase reactor system with recycle. Environ Sci Technol 2005;39: 3819–25.