Effect of pre-fermentation types on the potential of methane production and energy recovery from food waste

Renewable Energy 146 (2020) 1588e1595

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Effect of pre-fermentation types on the potential of methane production and energy recovery from food waste Kai Feng a, Huan Li a, b, *, Zhou Deng c, Qiao Wang d, Yangyang Zhang b, Chengzhi Zheng e a

Shenzhen Engineering Research Laboratory for Sludge and Food Waste Treatment and Resource Recovery, Graduate School at Shenzhen, Tsinghua University, Shenzhen, 518055, China b Key Laboratory of Microorganism Application and Risk Control of Shenzhen, Graduate School at Shenzhen, Tsinghua University, Shenzhen, 518055, China c Shenzhen Lisai Environmental Technology Co, Ltd, Shenzhen, 518055, China d Guangdong Engineering Research Center of Urban Water Cycle and Environment Safety, Graduate School at Shenzhen, Tsinghua University, Shenzhen, 518055, China e Technical Department of Rocktek, Rocktek Limited Liability Company, Wuhan, 430223, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 December 2018 Received in revised form 25 July 2019 Accepted 27 July 2019 Available online 27 July 2019

Two-phase anaerobic digestion (TPAD) is a commonly used method for recovering energy from food waste, even though the relationship between fermentation type and methane production has not to be thoroughly investigated. In this study, homolactic acid fermentation (HOLA), heterolactic acid fermentation (HELA), butyric acid fermentation (BUA), and mixed acid fermentation (MA) were used in the first phase, and the corresponding methane production levels were compared. HELA and MA resulted in the maximum methane yields of 290 and 287 ml per gram chemical oxygen demand (COD), respectively, but they were not significantly higher than the yield of 279 ml/g COD from single-phase anaerobic digestion (SPAD). During methanogenesis, BUA led to the fastest hydrolysis and methane production rates, followed by MA and HELA. In spite of the similar potential for methane production and energy recovery, TPAD using either BUA, MA, or HELA as the fermentation phase exhibited at least 50% greater methane production efficiency than SPAD. Overall, HELA and MA were found to be the best choices in terms of treatment efficiency and energy recovery. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Anaerobic digestion Fermentation Food waste Lactic acid Methane Volatile fatty acid

1. Introduction Food waste is the main component of municipal solid waste (MSW), and its treatment and utilization have attracted much attention due to its abundant nutrients and high biodegradable organic content. These characteristics suggest that food waste is both a potential threat to the environment and a potential source for bioenergy recovery. Recently, more than 100 food waste treatment facilities have been built or are under construction in China in an attempt to enhance MSW classification and resource recycling. In these plants, anaerobic digestion is the most common process, followed by composting for fertilizer manufacturing, thermal drying for feed processing, cultivating insects or worms for protein feed, and so on. Compared with other technical options, anaerobic digestion is a widely-used approach that can simultaneously

* Corresponding author. Room 2113, Building of Energy and Environment, Tsinghua Campus, University Town, Shenzhen, China. E-mail address: [email protected] (H. Li). https://doi.org/10.1016/j.renene.2019.07.127 0960-1481/© 2019 Elsevier Ltd. All rights reserved.

recover energy and resources. Food waste can be bioconverted to biogas through anaerobic digestion, and biogas can be further processed into natural gas or burned directly to output thermal energy and electricity [1]. In addition, the digested residuals can be utilized as an organic fertilizer with abundant nitrogen, phosphorus, and micronutrients. The various energy products and the possible land utilization of residuals make anaerobic digestion of food waste a flexible technical option that exhibits a high degree of adaptability in different areas, thus connecting a broad market. For the anaerobic digestion of food waste, there are two basic technical processes: single-phase anaerobic digestion (SPAD) and two-phase anaerobic digestion (TPAD) [2e4]. SPAD is operated in one digester, in which acidogenesis and methanogenesis coexist and the pH should be maintained at a neutral level. Despite the simplicity of the system, SPAD sometimes suffers from excessive acidification due to the accumulation of volatile fatty acids (VFAs) under high organic loading rates (OLRs). Hence, moderate OLRs and pH control are inevitable in SPAD. To improve the efficiency of anaerobic digestion, TPAD is an alternative option. Compared to

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SPAD, TPAD is often regarded as a preferable method for the treatment of easily biodegradable food waste due to its greater stability and higher working efficiency [5,6]. TPAD uses two reactors in sequence, and physically separates hydrolysis and the acidogenesis phase (fermentation reactor) from the methanogenesis phase (methane reactor) physically [7,8]. Thus, fermentative bacteria and methanogens can be cultivated in their respective optimal environmental conditions. Generally, a wide pH range of 4.0e8.5 is suitable for fermentative bacteria, while a narrow pH range of 6.8e8.0 favors methanogens [9]. Conventional TPAD processes usually adopt pH 5.0e6.0 as the fermentation condition so as to maximize the generation of VFAs [10,11], and adopt a pH level of approximately 7.5 as the methanogenesis condition in order to stimulate the activity of methanogens [12]. Voelklein et al. [13] reported that a fermentation reactor at pH 5.5 produced VFAs of 5.01e14.62 g/L with an ORL of 6e15 g VS/(L$d), and the subsequent methane production reached 67.7e76.4% (371.1e419.0 ml/g VS added) of the theoretical yield. In comparison to this TPAD, only 57.6e59.6% of the theoretical yield was obtained in the SPAD. Massanet-Nicolau et al. [7] obtained an acetic acid concentration of 3671 mg/L and a butyric acid concentration of 2640 mg/L during fermentation at pH levels higher than 5.5. The fermentation effluent was then used to produce methane with a yield of 359 ml/g VS added. Compared with the value of 261 ml/g VS added in the SPAD, the TPAD with the same overall solid retention time achieved an increase of 37% in methane production. During TPAD, fermentation products play a crucial role in the overall system, since they can affect the efficiency of methane production. Beyond VFAs, there are other fermentation products that can be added to methanogenic reactors. These products can be obtained under different fermentation conditions, such as pH. The pH value can alter the structure of the microbial community in fermentation reactors and consequently change fermentation types, such as lactic acid fermentation, ethanol fermentation, propionic acid fermentation, butyric acid fermentation, mixed acid fermentation, and so on [14,15]. Most of the existing studies on TPAD, however, have adopted either butyric acid fermentation or mixed acid fermentation at pH values higher than 5.0, with either butyric or acetic acid as the main intermediate products [10,16]. Although these conditions have been verified to be effective for subsequent methane production, there are still some possibilities involving fermentation type alteration that may further improve TPAD processes. For example, yeast has been added to food waste in order to achieve ethanol fermentation, which increased the buffering capacity of methane reactor [17]. Furthermore, the conversion from lactate to acetate requires less Gibbs free energy than the conversion from ethanol and other VFAs to acetate [18]. Hence, lactic acid is theoretically beneficial for methane production, although it is also possible that it will be converted to propionic acid when the hydrogen content is high. In addition, the process of lactic acid fermentation produces no hydrogen, and can be carried out at pH values below 4.5 [10,19]. Wu et al. [3] found that no lactic acid was detected in their methanogenic reactor in spite of the considerable amount of lactic acid that accumulated in their acidogenic reactor. Thus, lactic acid fermentation could be a lowcost step in TPAD, since maintaining a high pH consumes alkalis during fermentation. There have been very few studies concerning the effects of various fermentation types on the methane production of TPAD. In the limited research available, Wang et al. [5] investigated the effects of VFA concentration on methane yield, and Chen et al. [15] compared methane production performance following ethanol type fermentation, butyric acid fermentation, and mixed acid fermentation. To date, methane production following lactic acid fermentation, including homofermentation and

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heterofermentation, in comparison to other types of TPAD has yet to be investigated. In this study, different fermentation types, including homolactic acid fermentation, heterolactic acid fermentation, butyric acid fermentation, and mixed acid fermentation, were compared in terms of their subsequent performance during bioconversion to methane. Their methane production was then further compared with that from SPAD without prepositive anaerobic fermentation. Finally, the potential of energy recovery from different fermentation types followed by methanogenesis was examined. Our findings should provide a clear way to optimize TPAD through the selection of fermentation type. 2. Materials and methods 2.1. Inoculum and substrates During the digestion experiments of fermentation products, the inoculum was the digested sludge discharged from a laboratory anaerobic digester, which was operated at 35 ± 1
C, with food waste and dewatered sludge as the feedstock. Before use in the experiments, the inoculum was pre-incubated for three days in order to exhaust residual organic matter. The inoculum had a total solids (TS) concentration of 45 g/L, volatile solids (VS) content of 23 g/L, total chemical oxygen demand (TCOD) of 32880 ± 264 mg/L, soluble chemical oxygen demand (SCOD) of 3376 ± 28 mg/L, total soluble ammonia nitrogen (TAN) of 2983 ± 12 mg/L, and total alkalinity (TA) of 12854 ± 132 mg/L. These values indicates good quality of inoculum [20], such as sufficient TA suppling appropriate abiotic factor [21]. The substrates were the fermentation effluents from four continuous stirred tank reactors (RTK-CSTR, Rocktek, China), which used simulated food waste as the feedstock. Each reactor was equipped with an online pH monitor and an automatic feeding system of NaOH and HCl solution. Thus, the system could be kept at a particular pH value with an accuracy of 0.1. The food waste was composed of 36% vegetables (37% cabbage, 33% potato, 12% carrot, 16% onion, and 2% garlic), 34% rice, 8% meat, 6% noodle, 5% egg, 4% tofu, 4% edible oil, and 3% condiments (13% salt, 30% soy sauce, 4% pepper, 8% monosodium glutamate, 30% thick broad-bean sauce, and 15% oyster sauce). The food waste was first cooked for 30 min in an auto rice cooker, and then crushed using a garbage disposal. The TS content of the food waste was 5%, its VS/TS ratio was 95%, its TCOD was 58470 ± 916 mg/L, its SCOD was 10563 ± 610 mg/L, and its C/N ratio was 21. The four reactors were operated in semicontinuous mode at 35 ± 1
C, i.e., they were fed and drawn off once a day, and the discharged effluent was used for methane production. The solid retention time (SRT) of these fermentation reactors was kept at 4 days, and the corresponding OLR was 11.8 g VS/(L$d). 2.2. Methane production tests The biochemical methane production (BMP) tests were carried out in an automatic methane potential test system (AMPTS II, Bioprocess Control, Sweden) [20,22]. The effluents from different fermentation conditions and the raw food waste were used as the substrates. Each substrate was tested in triplicate. A series of 500ml glass bottles were used as the reactors. In each bottle, a certain quantity of fermentation effluent corresponded to a certain quantity of raw food waste that was fed to the fermentation reactors; the ratio of the inoculum and the raw food waste was set at 3:1, according to their VS. The total VS concentration was approximately 20 g/L in the mixture of inoculum and fermentation effluent. The working volume of each reactor was 400 ml, and all experimental trials were operated at 35 ± 1
C in a water bath. All bottles were

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flushed with nitrogen gas for 1 min to remove oxygen from the headspace and maintain an anaerobic environment. The stirring speed was fixed at 60 rpm. The carbon dioxide in the biogas was absorbed by NaOH (3.0 mol/L), and the purified methane flow was recorded with gas tippers based on a water displacement mechanism. The measured methane volume was adjusted to the volume at standard status (273.15 K and 101.33 kPa). Three blank trials containing only the inoculum were used to test the methane production from residual biodegradable organic matter in the inoculum. The BMP test results were expressed in ml CH4/g COD added, where COD is the value of raw food waste. Three positive controls were carried out using microcrystalline cellulose (MC) as the substrate, and the methane production reached to 354.7 ml CH4/g MC, indicating the good quality of the inoculum. 2.3. Analytical methods TS, VS, and TA were determined according to standard methods [22]. Elementary composition of food waste was determined using an elemental analyzer (vario EL cube, Elementar, Hanau, Germany). In order to determine the soluble parameters, samples were first centrifuged at 5800 g for 60 min, and the supernatant was then filtered by membranes with a mesh size of 0.45 mm to obtain the filtrate. The total ammonia nitrogen (TAN) and soluble chemical oxygen demand (SCOD) were detected via the salicylic acid method and the potassium dichromate method, respectively, using a spectrophotometer (DR3900, Hach, USA). The pH was measured using a digital meter (PHS-3C, INESA, China) with a pH detector (501, INESA, China). Ethanol and VFAs (acetic acid, propionic acid, butyric acid, and valeric acid) were measured using a gas chromatograph (GC-2014, Shimadzu, Japan) equipped with a capillary column (Inertcap wax 30 m  0.25 mm  0.25 mm) and a flame ionization detector. The lactic acid was determined using a highperformance liquid chromatograph (Prominence UFLC, Shimadzu, Japan) equipped with an InertSustain® C18 column (5 mm, 25 cm  4.6 mm) and an ultraviolet (206 nm) detector, while 85% 20 mmol/L KH2PO4 and 15% methanol were used as eluent at a rate of 0.7 ml/min. The gas generated from fermentation was measured using a gas flow meter (RTK-SGMC, Rocktek, China) and collected using gas bags, and its composition was analyzed using a gas chromatograph (MGC-7850S, Jing He, China) equipped with a thermal conductivity detector. 2.4. Statistical analysis Means and standard deviations were calculated based on triplicate tests, and significance analyses were adopted in the comparison using Microsoft Excel. In order to quantitatively analyze the effect of fermentation types on methane production, methane production was simulated using the first-order model [23], the modified Gompertz model [1], and the Cone model [17], as

following Equations (1)e(3), respectively. P ¼ Pmax$[1 e exp(-k$t)]

(1)

P ¼ Pmax$exp{-exp[Rmax$e$(l-t)/Pmaxþ1]}

(2)

P ¼ Pmax /[1þ(k$t)n]

(3)

where, P is the cumulative methane production based on the COD added at time t, ml/g; Pmax is the possible maximum methane production based on the COD added in a cycle, ml/g; k is the hydrolysis rate constant, 1/d, R max is the maximum methane production rate based on the COD added, ml/(g$d); l is the lag-phase time, d; e is exp(1); and n is the shape factor. The values of Pmax, Rmax, l, k and n were calculated using nonlinear fitting based on the least square method.

3. Results and discussion 3.1. Fermentation types under different pH values In our previous work [24], different fermentation types were achieved through pH control (i.e., 3.2, 4.0, 4.2, 4.5, 4.7, 5.0, and 6.0) in continuous fermentation reactors. In this study, these reactors were operated continuously under different pH values, and the fermentation effluents from these reactors were collected for BMP tests. The characteristics of the fermentation effluents used for methane production are listed in Table 1, and the distribution of fermentation products are shown in Fig. 1. Based on the composition of the fermentation products, fermentation types were defined as homolactic acid fermentation (HOLA), heterolactic acid fermentation (HELA), butyric acid fermentation (BUA), or mixed acid fermentation (MA). As shown in Table 1, lactic acid was the primary product, with a content by mass greater than 80% for the pH range of 3.2e4.2. This type of fermentation was designated HOLA. High-throughput sequencing results indicated that Lactobacillus was the superior bacterium under this pH condition [24], and lactic acid was its sole product from glucose. When the pH increased to 4.5, the abundance of Bifidobacterium increased significantly. This bacterium could convert 1 mol of glucose into 1 mol of lactic acid and 3/2 mol of acetic acid. Thus, the fermentation type transformed to HELA, with a significant increase of acetic acid in the fermentation products. In addition, Lactobacillus can convert 1 mol of glucose to 1 mol lactic acid, 1 mol ethanol, and 1 mol CO2 through HELA fermentation, although this conversion did not appear in this study. BUA with maximum hydrogen yield and MA with maximum VFA production occurred at pH 4.7e5.0 and pH 6.0, respectively.

Table 1 Characteristics of fermentation effluents.

Fermentation types Lactic acid (mg/L) Ethanol (mg/L) Acetic acid (mg/L) Propionic acid (mg/L) Butyric acid (mg/L) Valeric acid (mg/L) TCOD (mg/L) SCOD (mg/L) TAN (mg/L)

pH 3.2

pH 4.0

pH 4.2

pH 4.5

pH 4.7

pH 5.0

pH 6.0

HOLA 5890 ± 352 439 ± 7 251 ± 7 10 ± 3 4±1 8±7 52391 ± 1689 14160 ± 839 89 ± 8

HOLA 13639 ± 527 1371 ± 27 477 ± 31 303 ± 10 677 ± 13 123 ± 2 52411 ± 536 26268 ± 673 86 ± 10

HOLA 13254 ± 824 1348 ± 3 481 ± 26 294 ± 11 466 ± 2 204 ± 7 56375 ± 715 24826 ± 301 82 ± 15

HELA 13261 ± 577 677 ± 22 4741 ± 58 969 ± 18 2469 ± 20 621 ± 14 59901 ± 553 33274 ± 99 35 ± 8

BUA 206 ± 30 1203 ± 77 3262 ± 12 656 ± 14 8033 ± 94 1043 ± 4 52883 ± 236 30268 ± 148 38 ± 9

BUA 354 ± 46 1008 ± 91 3869 ± 79 50 ± 1 4469 ± 9 66 ± 26 56352 ± 979 28064 ± 201 33 ± 4

MA ND 408 ± 27 2494 ± 36 1607 ± 13 5437 ± 21 4152 ± 10 66058 ± 1418 32563 ± 411 20 ± 6

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Fig. 1. Distribution of fermentation products for different fermentation types (HOLA: homolactic acid fermentation; HELA: heterolactic acid fermentation; BUA: butyric acid fermentation; MA: mixed acid fermentation) corresponding to different pH values.

Fig. 2. Cumulative (a) and daily (b) methane production using different substrates (pH values indicate the fermentation condition; fermentation effluents were used for methane production; FW indicates that food waste was directly used as the substrate).

3.2. Theoretical and experimental methane production The chemical formula of the food waste was derived from elemental analyses, which could be used to calculate theoretical methane production (TMP) through stoichiometric equations. Equation (4) indicates the moles of oxygen required to oxidize 1 mol of food waste, and Equation (5) calculates the moles of CH4 generated from 1 mol of food waste. The methane production can be expressed as either ml/g VS added or ml/g COD added. The TMP based on the COD was 350 ml/g, and the TMP based on the VS of food waste should be 496 ml/g. However, the TS and VS of fermentation effluents were difficult to measure owing to the volatilization of VFAs and ethanol. Hence, the COD was used as the basis for comparison [25], and the unit was expressed as ml CH4/g COD added (ml/g for short). The conversion rate of food waste (CVR) can be calculated through Equation (6). C24.82H44.56O16.08N þ 27.17 O2 / 24.82 CO2 þ 20.78 H2O þ 1 NH3(4) C24.82H44.56O16.08N þ H2O / 13.585 CH4 þ 11.235 CO2 þ 1 NH3 (5) CVR ¼ BMP/TMP

(6)

The fermentation effluents corresponding to different pH

conditions were used for BMP tests, and the cumulative and daily methane production were recorded, as shown in Fig. 2. Simultaneously, a group of tests using the raw food waste as the substrate was carried out for comparison. After 19 days, the daily methane production was less than 1% of the accumulated yield in the last three consecutive days in all the groups, indicating the termination of all the tests. The specific cumulative methane yields based on COD are listed in Table 2, together with the conversion rates (CVR), as represented by BMP/TMP. The cumulative methane yields can be classified into 4 types, corresponding to the fermentation types. Methane yields of 251.7, 256.6, and 252.0 mL/g were obtained from the fermentation effluents associated with pH values of 3.2, 4.0, and 4.2, respectively. No significant difference was found between them (p > 0.1). Therefore, the average yield of HOLA should be 253.4 mL/g, and the average CVR was 72.4% (Table 2). Similarly, there was no significant difference between the results corresponding to pH 4.7 and 5.0 (p > 0.1), which belonged to the same BUA fermentation type. The maximum cumulative methane yield of 289.5 mL/g) and the highest CVR of 82.7% were achieved when the fermentation effluent at pH 4.5, i.e., under HELA fermentation, was used as the substrate. McEniry et al. [26] also reported that HELA resulted in a numerically higher specific methane yield. As stated above, HELA should have the lowest carbon loss in the form of CO2 at the fermentation stage,

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Table 2 Experimental biochemical methane potentials (BMP) of raw food waste and fermentation effluents under different pH and its ratio versus theoretical methane potential (TMP). substrate

BMP (ml CH4/g COD)

BMP/TMP (%)

Food waste HOLA pH3.2 pH4.0 pH4.2 HELA pH4.5 BUA pH4.7 pH5.0 MA pH6.0

279.0 ± 0.8

79.7

251.7 ± 19.8 256.6 ± 1.3 252.0 ± 10.4

71.9 73.3 72.0

289.5 ± 1.9

82.7

264.3 ± 4.4 263.0 ± 2.0

75.6 75.1

286.6 ± 1.5

81.9

thus leaving more carbon for methane production at the methanogenesis stage. At pH 6.0, the fermentation type shifted to MA, and accordingly the total VFA concentration reached the maximum compared with the other pH conditions. Consequently, its cumulative methane yield reached 286.6 mL/g, with a CVR of 81.9%; there was no significant difference between this result and that from HELA (p > 0.1). In the group using food waste as the substrate, the cumulative methane yield reached 279.0 mL/g, which was slightly less than the yields from the fermentation effluents at pH 4.5 and 6.0. In terms of the CVR, the different fermentation types exhibited the relative order of HELA > MA > raw food waste > BUA > HOLA. The maximum CVR was 82.7% (HELA), which was 3.0% higher than the performance of SPAD for raw food waste. These results verified that a shift in fermentation type did indeed change the performance of methane production, although the change was still limited. This phenomenon was also proved by Chen et al. [15], who reported that CVRs of 95%, 79%, and 75% were obtained for the BUA, ethanol, and MA fermentation types, respectively. In our current study, the lower CVR of BUA might be attributed to energy loss (generating H2 and CO2) during fermentation. The same result found in HOLA might be due to the secretion of bacteriocins by Lactobacillus at low pH, which could inhibit the activity of methanogens [27]. In terms of methane production rate, approximately 90% of the total methane yield from fermentation effluents was obtained in the first 4 days, and methane production ended by the 11th day. In contrast, the methane production from food waste reached 90% of the cumulative yield by the ninth day and ended by the 19th day. It was obvious that TPAD would shorten the digestion time of food waste, even if the pre-fermentation time of four days was included. During methanogenesis, lactic acid, ethanol, and VFAs are first converted to acetate and H2 by acetogenic bacteria, and subsequently, acetoclastic and hydrogenotrophic methanogens use acetate or H2/CO2 to produce methane [28]. Therefore, the flow of

Table 3 Gibbs free energies of main anaerobic biochemical reactions. Reaction Acetogenic reactions Lactate: CH3CHOHCOOH þ 2H2O / CH3COOH þ HCO 3 þ 2H2 Ethanol: CH3CH2OH þ H2O / CH3COOH þ 2H2 Propionate: CH3CH2COOH þ 2H2O / CH3COOH þ 3H2 þ CO2 Butyrate: CH3CH2CH2COOH þ 2H2O / 2CH3COOH þ 2H2 Homoacetogenesis: 4H2 þ 2CO2 / CH3COOH þ 2H2O Methanogenic reactions Acetate: CH3COOH / CH4 þ CO2 Hydrogen: 4H2 þ CO2 / CH4 þ 2H2O

DG0 (kJ/mol) 4.2 þ9.6 þ76.2 þ48.4 104.0 31.0 135.0

organic carbon at the fermentation stage (organic monomers transforming into lactic acid, ethanol, and VFAs) becomes a possible factor determining differences in the methane production rate. According to the Gibbs free energy (DG0), as shown in Table 3 [27], LA fermentation, with lactic acid as the main product or HELA with lactic acid and acetic acid as the main products, should be ready for methane production. Hence, they resulted in the fastest methane production at the initial stage. Next, the fermentation effluents from BUA and MA also exhibited more rapid methane production than the raw food waste. Hence, compared to SPAD, TPAD (even with HELA) only slightly improved the methane potential of food waste (3%), but significantly accelerated methane production. 3.3. Model analysis of methane production The parameters of kinetic models can characterize the process of methane production [29]. Three models, including the first-order kinetic, the modified Gompertz, and the Cone, were used here to fit the experimental data in the tests, as shown in Fig. 3. The simulated parameters corresponding to the different substrates are listed in Table 4. Concerning hydrolysis, in the first-order kinetic model, the rate constant k is an important indicator reflecting substrate hydrolysis. In other words, hydrolysis is viewed as the rate-limiting step, and the subsequent methane production is proportional to the hydrolyzed substrate. In general, high k values reflect rapid degradation and methane production rates, while low values indicate slower processes [30]. The k values of the fermentation effluents were found to be significantly higher than the k value of the raw food waste, indicating that pre-fermentation can effectively accelerate substrate hydrolysis and subsequent methane production. Nevertheless, the solid particles in the fermentation effluents provided around 40e70% of the total COD, and the detailed information can be found in our previous report [24]. Statistical indicators (R2) were used to evaluate the reliability of these modeling results. Overall, the hydrolysis models (the first-order kinetic model and the Cone model) were suitable for the digestion of raw food waste and the fermentation effluents at pH 3.2e4.2 because these effluents had low hydrolysis rates. In contrary, the applicability of the two models decreased for the fermentation effluents at pH 4.5e6.0 (R2 decreased from 0.9950 to 0.9367) because these effluents had high hydrolysis rates. Contrary to those models, the modified Gompertz model exhibited good adaptability to both the fermentation effluents and the raw food waste (R2 ranged from 0.9851 to 0.9983). These results indicated that methanogenesis might be the rate-limiting step during the tests. Hence, the results based on this model were further used to analyze the influence of fermentation type on methane production. For the modified Gompertz model, the lag phase (l) is an inherent biological phenomenon reflecting a delayed response of methanogens to environmental change [31]. In this phase, microorganisms adjust themselves to adapt to the new environment and initiate exponential growth [32]. Therefore, a shortened lag phase is beneficial for methane production from organic matter. In other words, methane production should be the rate-limiting step. In this study, the l values of the fermentation effluents were higher than the l value of the raw food waste, a finding that might be due to the fact that the microorganisms in the inoculum were originally cultivated in the environment in which food waste was used as the feedstock. Hence, a short adaptive time to the environment was observed in the group with raw food waste as the substrate. In addition, it was observed that the lag phase time increased along with the rise of fermentation pH. The maximum methane potential (Pmax) estimated from all the models varied with fermentation type, approaching maximum

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Fig. 3. Simulation of methane production using the first-order kinetic model, the modified Gompertz model, and the Cone model.

values at pH 4.5 and 6.0. These results were in accordance with the experimental data. Furthermore, the maximum methane production rate (Rmax) calculated using the modified Gompertz model increased noticeably after food waste fermentation. The maximum Rmax was achieved at pH 4.7, a rate that was 75.4% higher than that of the raw food waste. This result may be related to the high butyric acid concentration. Similarly, Wang et al. [33] found that the degradation rates of butyric acid were highest among VFAs in

anaerobic digestion. In addition to BUA fermentation, MA fermentation (pH 6.0) and HELA fermentation (pH 4.5) also produced effluents that could be rapidly converted to methane. 3.4. Potential of energy recovery from different fermentation effluents In this study, the TAPD system consisted of a fermentation phase

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Table 4 Parameters for the three models simulating methane production from fermentation effluents under different pH. Food waste First-order kinetic model Pmax (ml/g COD) 272.7 k (d1) 0.34 R2 0.9901 Cone model 280.6 Pmax (ml/g COD) k (d1) 0.47 n 1.69 R2 0.9930 Modified Gompertz model Pmax (ml/g COD) 265.4 62.9 Rmax (ml/g COD) l (d) 0.06 2 R 0.9851

pH3.2

pH4.0

pH4.2

pH4.5

pH4.7

pH5.0

pH6.0

251.8 0.49 0.9941

260.8 0.48 0.9822

255.1 0.39 0.9895

296.4 0.39 0.9678

270.1 0.48 0.9635

271.1 0.37 0.9482

294.5 0.36 0.9558

254.7 0.66 1.94 0.9950

260.9 0.61 2.39 0.9865

256.4 0.52 2.12 0.9966

293.9 0.48 2.78 0.9866

268.1 0.58 2.98 0.9867

266.3 0.43 3.51 0.9367

289.01 0.43 3.30 0.9930

248.3 82.2 0.09 0.9945

257.6 90.1 0.28 0.9983

250.2 70.5 0.23 0.9968

290.9 93.8 0.56 0.9976

266.4 110.3 0.56 0.9977

265.1 91.7 0.88 0.9945

287.2 98.33 0.85 0.9981

(4 days) and a methanogenesis phase. Hydrogen was the main energy output of the first stage of TPAD, while methane subsequently became the dominant energy product of the second stage. For SPAD (in which food waste was directly used as the substrate), methane was produced from beginning to end. However, hydrogen is usually not collected from TPAD processes in full-scale food waste treatment plants due to low cost-benefit ratios. In this study, the hydrogen released from the different fermentation types accounted for less than 6% of the total energy output in all cases. This result was consistent with the findings of Luo et al. [34], who studied hydrogen and methane production in TPAD and found only about 3e5% of the energy output was contributed by hydrogen. Therefore, only methane was considered in the energy potential analyses. Based on the BMP levels corresponding to the different fermentation types, the conditions of pH 4.5 (HELA) and 6.0 (MA) were selected as the TPAD fermentation phases in comparison to the SPAD of the raw food waste. Their energy outputs can be calculated based on methane production and the low heating value of methane (36 MJ/Nm3), as shown in Fig. 4. TPAD with either HELA or MA as its fermentation phase exhibited energy outputs that were only slightly higher than the output of SPAD in a complete digestion period, with values of 10.47, 10.32, and 10.04 MJ/kg COD, respectively. However, TPAD shortened the digestion period significantly due to its different metabolic pathways. During the two types of TPAD, the fermentation stage ended by the fourth day, and the subsequent methane production was completed by the 13th day. In terms of energy output, TPAD with either HELA or MA surpassed SPAD sometime between the seventh and the eighth day. In order

to reach the same level of energy output that SPAD achieved in 19 days, TPAD only required 9e10 days, even when taking fermentation time into account. In addition, TPAD with BUA fermentation also accelerated methane production significantly, although it did not ultimately achieve a higher energy output than SPAD. Therefore, TPAD should have a much higher treatment efficiency than SPAD, implying a higher load rate, which should primarily depend on a rapid methane conversion rate rather than a high conversion ratio of food waste. 4. Conclusions In this study, all fermentation types, including HOLA, HELA, BUA, and MA, were used as the first stage of two-phase anaerobic digestion (TPAD), resulting in different methane production performances. Compared with single-phase anaerobic digestion, TPAD exhibited a slightly higher methane potential when its fermentation type was HELA or MA. Meanwhile, TPAD with HELA or MA as its first stage significantly shortened the overall treatment time of food waste, thus demonstrating higher treatment efficiency. Acknowledgement Financial support for this project is obtained from the Shenzhen Science and Technology Project (grant number JCYJ20170817161931586); National Key Research and Development Program of China (grant number 2018YFC1902900); and the Development and Reform Commission of Shenzhen Municipality (urban water recycling and environment safety program). References

Fig. 4. Energy output based on methane production during two-stage anaerobic digestion (fermentation at pH 4.5 or 6.0) and single-stage anaerobic digestion of food waste.

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