Fungal pretreatment of rice straw with Pleurotus ostreatus and Trichoderma reesei to enhance methane production under solid-state anaerobic digestion

Applied Energy 180 (2016) 661–671

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Fungal pretreatment of rice straw with Pleurotus ostreatus and Trichoderma reesei to enhance methane production under solid-state anaerobic digestion Ahmed M. Mustafa a,c, Tjalfe G. Poulsen b, Kuichuan Sheng a,⇑ a b c

College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China Department of Civil Engineering, Xi’an Jiaotong-Liverpool University, Suzhou 215123, China Department of Agricultural Engineering, Faculty of Agriculture, Suez Canal University, Ismailia 41522, Egypt

h i g h l i g h t s
Solid state anaerobic digestion of fungal treated rice straw for biogas production.
Fungal pretreatment caused 33% of lignin loss led to methane yield increased by 120%.
Moisture content and incubation time significantly affected the lignin degradation.
Methane yield increased linearly with selectivity value in fungal pretreatment.

a r t i c l e

i n f o

Article history: Received 13 May 2016 Received in revised form 24 July 2016 Accepted 31 July 2016 Available online 11 August 2016 Keywords: Rice straw Fungal pretreatment Lignin removal Solid-state anaerobic digestion Moisture content Incubation time

a b s t r a c t Rice straw was subjected to fungal pretreatment using Pleurotus ostreatus and Trichoderma reesei to improve its biodegradability and methane production via solid-state anaerobic digestion (SS-AD). Effects of moisture content (65%, 75% and 85%), and incubation time (10, 20 and 30 d) on lignin, cellulose, and hemicellulose degradation during fungal pretreatment and methane yield during anaerobic digestion were assessed via comparison to untreated rice straw. Pretreatment with P. ostreatus was most effective at 75% moisture content and 20 d incubation resulting in 33.4% lignin removal and a lignin/cellulose removal ratio (selectivity) of 4.2. In comparison Trichoderma reesei was most effective at 75% moisture content and 20 d incubation resulting in 23.6% lignin removal and a lignin/cellulose removal ratio (selectivity) of 2.88. The corresponding methane yields were 263 and 214 L/kg volatile solids (VS), which were 120% and 78.3% higher than for the untreated rice straw, respectively. Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction In 2014, the world energy consumption was 12928.4 Mtoe (541.3 EJ), of which oil, natural gas coal, nuclear energy, hydroelectricity and other renewable energy consumption were 32.6%, 23.7%, 30.0%, 4.4%, 6.8% and 2.4%, respectively [1]. Fossil fuel consumption accounted for 86.3% of the world energy consumption, whereas renewable energy consumption accounted for 9.2%. At present world energy consumption is growing by 2% per year. Consumption of fossil fuels is recognized as the main cause of global warming and climate change with associated adverse environmental effects as a result. The strong dependency on fossil fuels further carries the risk of significant changes in energy costs due to varia⇑ Corresponding author. E-mail address: [email protected] (K. Sheng). http://dx.doi.org/10.1016/j.apenergy.2016.07.135 0306-2619/Ó 2016 Elsevier Ltd. All rights reserved.

tions in fossil fuel prices, which in turn may result in economic and political challenges [2]. Therefore, alternative energy sources with low greenhouse gas emissions and more stable prices should be developed, to meet the growing energy demand, reduce greenhouse gas emissions and secure more stable energy prices [3]. Lignocellulosic biomass, is one of the world’s largest sources of biomass-based renewable energy with an annual production of 200 billion tons, but is at present underutilized [4]. Lignocellulosic biomass is known to be one of the best sources for inexpensive production of carbohydrates, and has been used to produce biofuels such as biogas and bioethanol using anaerobic treatment [4,5]. Rice straw is the most abundant lignocellulosic biomass in China with an annual production ranging between 180 and 270 million tons [6]. Rice straw contains 32–47% cellulose, 19–27% hemicellulose and 5–24% lignin [7]. Cellulose (the main component of rice straw) can be hydrolyzed into glucose which may be readily con-

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verted into biogas or bioethanol. The presence of lignin and hemicellulose reduces the rate of hydrolysis especially under anaerobic conditions, resulting in lower rice straw conversion efficiency [8]. To reduce the difficulty of lignocellulosic biomass decomposition, different methods of pretreatment such as physical (particle size reduction), thermal (application of high temperature and pressure), chemical (application of strong acids or bases) and biological (application of microorganisms to decompose lignin and lignocellulose) have been widely studied and applied in recent years [9–12]. These methods can alter the chemical composition and physical structure of lignocellulosic materials, breaking the linkage between polysaccharides and lignin and consequently making cellulose and hemicelluloses more accessible to hydrolytic enzymes [13]. Biological pretreatment is more environmentally safe compared to other methods as it consumes less energy and chemicals. It is further carried out under moderate environmental conditions (temperature, pressure and pH), reducing production of potentially inhibiting compounds which could affect anaerobic digestion negatively [10]. Two groups of fungi; ascomycetes (represented by Trichoderma reesei) and basidiomycetes, white rot fungi (represented by Pleurotus ostreatus), were studied because of their ability to degrade the polymers of lignocellulose material. Some ascomycetes are known to degrade cellulose and hemicellulose, but have little ability to degrade lignin while white rot fungi can degrade cellulose, hemicellulose and lignin at equal rates [14,15]. Biological pretreatment using fungi is one of the most effective and extensively applied methods for lignocellulosic biomass conversion [16]. Taniguchi et al. [17] pretreated rice straw with four different strains of white-rot fungi (Trametes versicolor, Phanerochaete chrysosporium, P. ostreatus, and Ceriporiopsis subvermispora). P. ostreatus was found the most successful fungus as it was able to selectively decompose the lignin fraction but not the holocellulose component. To achieve good fungal pretreatment (selective lignin removal) efficiency, knowledge about the factors affecting fungal growth and metabolism (moisture content, feedstock particle size, oxygen concentration, and incubation time) is critical, [16]. Moisture content is critical in nutrient transfer during fungal pretreatment, thus sufficient moisture is required for healthy fungus growth and ligninolytic activity [18,19]. Optimum moisture content for fungal growth varies with fungus strain and type of biomass [20]. However, previous studies suggests that P. ostreatus degrades lignin well for moisture contents ranging from 60% to 85% by weight [21]. Also incubation time is important and optimal incubation time varies with biomass composition and fungus strain. Requirements for long incubation time, due to low lignin removal rates, is one of the main obstacles for the application of fungal pretreatment on a large scale [16,22]. Therefore, optimization of moisture content and incubation time in combination during fungal pretreatment is necessary to maximize lignin removal efficiency. There is, however, a lack of research and knowledge on fungal pre-treatment of rice straw and the authors are not aware of any studies that have investigated the interactive effects of moisture content and incubation time and their combined influence on lignin removal efficiency during fungal pretreatment of rice straw and its effect on subsequent methane production. The objectives of this study were therefore to: (1) investigate the effect of fungus type, moisture content and incubation time on degradation of dry matter, cellulose, hemicellulose, and lignin during fungal pretreatment of rice straw; (2) evaluate the effect of fungal pretreatment on the biogas and methane yield of rice straw; (3) evaluate the relationship between methane yield and lignin degradation and lignin selectivity value (lignin degradation/cellulose degradation).

2. Materials and methods 2.1. Feedstock and inoculum preparation and characterization Rice straw was obtained from a farm in Haiyan, Zhejiang Province, China. It was initially air dried for one week to a moisture content of less than 10%, subsequently cut into pieces 2–3 cm in length and stored at room temperature until further use. Anaerobic sludge obtained from the effluent of a mesophilic biogas plant (with cow manure as feedstock) at Lin’an Zhengxing Farm, Hangzhou, Zhejiang Province, China was used as inoculum. Prior to sampling, the digester stirring was stopped for 1 day to increase the dry matter content in the inoculum. After sampling, the sludge was stored in an airtight container at room temperature (about 25 °C) until use. The concentrations of total solids (TS), volatile solids (VS) and ash content of untreated rice straw and inoculum were measured according to the Standard Methods [23]. Estimation of cellulose, hemicellulose and lignin contents were conducted by the detergent method [24]. Total carbon and nitrogen contents were evaluated by an elemental analyzer (EA 1112, CarloErba, Italy). All chemical analysis were conducted in triplicate. Characteristics of raw rice straw and inoculum are shown in Table 1. The surface structure of untreated rice straw was further examined employing field launch scanning electron microscope (SEM) using an SU8010 microscope (Hitachi, Japan). Before examination, sample particles were coated with gold film. The launching voltage of the electron microscope was 10.0 kV. Specific surface area of raw and pretreated rice straw was measured based on nitrogen adsorption using a static nitrogen absorption instrument (JW-BK, Beijing). Measurements were conducted in a liquid nitrogen environment at 196 °C for ten different nitrogen adsorption pressure intervals using about 0.8 g dried sample. The BrunauerEmmett Teller (BET) adsorption isotherm was used to approximate the data and calculate specific surface area. 2.2. Fungus preparation Two types of fungi were used in this study, the white-rot fungus P. ostreatus (DSM 11191) and Trichoderma reesei (QM9414). The fungi were obtained from the Department of Food Science and Nutrition and the Department of Plant Protection, Zhejiang University, Hangzhou, China, respectively. It was cultured on potato dextrose agar (PDA) plates in an incubator at 28 °C for 8 days. Four pieces of agar medium (about 5 mm in diameter) with fungus mycelium were placed in one 125 mL Erlenmeyer flask containing 25 mL of potato dextrose liquid medium. The flask was subsequently closed with a cotton stopper and incubated for 8 days at 28 °C with agitation. The fungus was separated from the liquid medium by centrifuging at 3000 rpm for 5 min using a Heal Force,

Table 1 Characteristics of rice straw and inoculum. Parameters

Rice straw

Inoculum

TS (%, w.b.) VS (%, w.b.) VS/TS (%) Total carbon (%, d.b.) Total nitrogen (%, d.b.) C/N pH Cellulose (%, d.b.) Hemicellulose (%, d.b.) Lignin (%, d.b.) Ash content (%, d.b.)

89.9 ± 0.2 80.6 ± 0.2 89.7 ± 0.1 41.4 ± 0.3 1.3 ± 0.4 31.8 ± 0.4 ND 37.8 ± 0.2 29.6 ± 0.7 14.8 ± 0.4 10.3 ± 0.5

12.1 ± 0.1 6.4 ± 0.1 52.9 ± 0.1 30.1 ± 0.3 2.2 ± 0.5 13.7 ± 0.6 7.85 ± 0.1 ND ND ND 47.1 ± 0.2

Note: w.b., wet base; d.b., dry base; ND, not determined. Data are mean values ± standard error of three replicates.

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Neofuge 15R centrifuge followed by re-suspension in 25 mL of sterilized deionized water. This suspension was subsequently used as inoculum for fungal pretreatment.

fungal pretreatment were calculated as follow [25,26] (Eqs. (1)– (6)):

Dry matter loss ¼ ððTSinitial  TSfinal Þ=TSInitial Þ 100;

ð1Þ

Lignin removal ¼ ððL0  La Þ=L0 Þ 100;

ð2Þ

Solid Recovery SR ¼ ðDa =D0 Þ 100;

ð3Þ

Cellulose retention ¼ ðC a =C 0 Þ 100;

ð4Þ

Hemicellulose retention ¼ ðHa =H0 Þ 100;

ð5Þ

Lignin retention ¼ ðLa =L0 Þ 100:

ð6Þ

2.3. Fungal pretreatment 100 g of rice straw particles were placed into thirty-six 1 L Erlenmeyer flasks, moisturized with deionized water and sterilized at 121 °C for 30 min to prevent microbial growth. During sterilization flasks were closed using cotton stoppers and aluminum foil to reduce moisture loss. After cooling to room temperature, 25 mL of fungus suspension was added to each flask. Initial moisturizing was done such that the final moisture content including inoculum was 65%, 75%, and 85% by weight (12 flasks for each moisture content). Two additional autoclaved flasks containing only rice straw and deionized water at 75% moisture content (no inoculation) were set up as controls; all flasks were closed with cotton plugs. Fungal pretreatment was performed in an incubator at 28 °C for incubation times of 10, 20 and 30 days for all three moisture contents. All experiments were carried out in duplicate. After incubation, the pretreated rice straw samples were divided into two groups, the first was washed with deionized water and dried at 100 °C for 24 h, the second was air dried by necessity to reach TS 20% without washing to investigate the effect of washing on the methane yield. Pretreated rice straw characteristics (including SEM examination) were measured using the same methods as discussed in Section 2.1. Remaining pretreated rice straw samples were then stored in polythene bags until further use. Dry matter loss, biomass component degradation (lignin, cellulose and hemicellulose), solid recovery SR, cellulose retention, hemicellulose retention and selectivity value of rice straw after

where Da, Ca, Ha, La are, dry weight, cellulose, hemicellulose, and lignin fractions (%) of rice straw after fungal pretreatment, respectively, while D0, C0, H0, L0 are the corresponding fractions (%) of original rice straw. Results of the calculations are shown in Table 2. 2.4. Solid-state anaerobic digestion of pretreated rice straw The batch system was composed of a 500-mL glass reactor, a 2-L glass bottle for gas collection which was filled with diluted hydrochloric acid solution (pH < 3 to avoid CO2 dissolution) and a 500-mL liquid collection beaker. Biogas production was measured using the water displacement method where biogas generated in the reactor moves to the gas collection bottle where it replaces acid solution, which in turn is collected in the liquid collection beaker. Thirty-eight groups each containing duplicate SS-AD reactors were set up. Eighteen groups corresponding to all possible combinations of fungus (P. ostreatus, T. reesei), moisture content (65%, 75%, and 85%) and incubation time (10, 20, and 30 d), were fed with

Table 2 Changes in chemical composition and digestion properties of rice straw for different pretreatments. Experimental factors

Methane yieldb

Methane contenta

DT90b

MC (%)

IT (d)

(L/Kg Vs)

(%)

(%)

20

120 (14.1) 127 (11.3)

63.7 (1.50) 62.4 (0.42)

73.3 (3.93) 71.1 (3.14)

10 20 30

208 (9.91) 237 (15.6) 251 (22.6)

66.4 (0.25) 68.3 (0.71) 69.4 (0.15)

75

10 20 30

199 (19.8) 263 (12.7) 232 (21.2)

85

10 20 30

Surface area b

Composition of treated samples Retention a (%)

(m2/g)

SR

Lignin

CEL

HCEL

– 0.32 (0.07)

2.83 (0.11) 2.86 (0.08)

100 99.1 (0.42)

– 98.7 (0.47)

– 95.9 (0.56)

– 97.3 (0.43)

66.7 (1.57) 60.0 (0.79) 53.3 (1.57)

3.05 (0.03) 3.76 (0.91) 4.24 (0.47)

3.08 (0.14) 3.27 (0.06) 4.39 (0.02)

93.6 (0.66) 90.9 (1.13) 88.8 (1.35)

82.3 (4.41) 74.6 (2.11) 67.8 (1.40)

94.2 (1.50) 92.9 (2.44) 92.3 (1.12)

87.8 (2.91) 84.1 (3.02) 81.1 (2.32)

117 (13.7) 134 (21.3) 167 (17.2)

67.4 (0.36) 71.6 (1.23) 69.3 (0.80)

60.0 (3.93) 46.7 (2.36) 57.8 (0.79)

3.08 (0.61) 4.30 (0.70) 3.68 (1.07)

2.98 (0.07) 4.50 (0.05) 4.02 (0.04)

92.7 (0.95) 89.0 (0.91) 86.8 (1.18)

80.5 (2.67) 66.6 (1.41) 64.7 (1.01)

93.4 (2.67) 92.1 (1.56) 89.7 (3.20)

85.8 (1.88) 83.1 (1.90) 76.3 (1.72)

116 (18.2) 195 (16.7) 129 (19.8)

186 (26.9) 161 (35.4) 152 (39.6)

67.1 (0.85) 65.8 (1.21) 64.8 (0.87)

60.0 (2.36) 62.2 (5.50) 64.4 (4.71)

2.57 (0.18) 2.19 (0.16) 1.94 (0.24)

3.11 (0.32) 3.19 (0.13) 3.29 (0.23)

94.0 (0.75) 91.9 (1.07) 90.9 (1.16)

79.2 (0.97) 76.4 (3.95) 75.3 (0.91)

91.8 (1.05) 89.1 (2.55) 86.9 (2.11)

95.6 (1.06) 91.2 (2.36) 89.9 (3.03)

106 (11.4) 92 (17.8) 85 (10.8)

10 20 30

131 (9.90) 184 (15.6) 169 (7.07)

67.2 (0.36) 67.7 (0.93) 64.7 (0.75)

71.1 (2.20) 60.7 (0.94) 68.9 (1.26)

1.67 (0.81) 2.02 (1.51) 1.84 (1.22)

3.05 (0.47) 3.66 (0.34) 3.59 (0.18)

94.3 (2.21) 92.5 (1.23) 90.7 (1.36)

88.5 (1.94) 84.8 (1.61) 83.1 (3.60)

93.1 (2.40) 92.5 (1.06) 90.8 (2.96)

86.8 (2.76) 82.8 (1.21) 78.0 (2.31)

75 (22.3) 102 (24.9) 97 (18.9)

75

10 20 30

148 (11.3) 214 (8.49) 190 (14.1)

63.5 (1.40) 67.7 (0.57) 62.5 (1.30)

62.2 (1.41) 66.7 (1.89) 66.7 (1.57)

1.67 (1.19) 2.88 (0.55) 2.35 (1.44)

3.17 (0.27) 3.97 (0.81) 3.86 (0.13)

93.3 (1.72) 90.5 (1.03) 89.4 (1.05)

87.3 (2.62) 76.4 (0.98) 77.0 (3.05)

92.4 (2.20) 91.8 (1.78) 90.2 (2.12)

84.8 (2.27) 81.4 (3.12) 76.7 (3.80)

83 (16.6) 127 (15.2) 109 (21.9)

85

10 20 30

113 (17.0) 117 (12.7) 84 (19.8)

60.4 (0.49) 62.4 (0.95) 59.8 (0.64)

73.3 (3.93) 73.3 (3.14) 75.6 (4.09)

0.53 (1.77) 0.54 (1.49) 0.37 (1.57)

3.02 (0.15) 3.51 (0.32) 3.23 (0.41)

95.2 (2.01) 92.7 (1.74) 90.5 (1.85)

93.9 (2.92) 91.9 (2.01) 92.6 (3.57)

88.6 (1.65) 84.9 (1.35) 79.9 (2.27)

90.2 (1.64) 83.8 (1.16) 79.1 (3.06)

65 (12.8) 73 (15.8) 54 (14.1)

Raw control P. ostreatus 65

T. reesei 65

Selectivity valuea

Methane yield UW b (L/Kg Vs)

MC – moisture content; IT – incubation time; SR – Solids Recovery; CEL – cellulose, HCEL – hemicellulose, DT90 - time required to reach 90% of methane yield, UW – unwashed samples after fungal pretreatment. a Data are the means of three measurements and number in parentheses are standard deviations. b Data are the means of two replicates and number in parentheses are standard deviations.

A.M. Mustafa et al. / Applied Energy 180 (2016) 661–671

V STP ¼

V T  273  ð760  pw Þ ð273 þ TÞ  760

ð7Þ

where VSTP is the volume of biogas at standard conditions (L), VT is biogas volume measured at temperature T (L), pw is water vapor pressure at temperature T (mm Hg), and T is the ambient temperature (°C). Methane yield was subsequently calculated from the biogas yield in using the measured methane concentrations. Biogas and methane yields were subsequently corrected for gas and methane production by the inoculum [28]. Data Analysis (including statistical analyses) was conducted using Microsoft Excel 2013. 3. Results and discussion 3.1. Characteristics of raw rice straw Table 1 shows the characteristics of the raw rice straw used in this study. Raw rice straw contained high contents of both total solids (89.9%) and total volatile solids (89.7% dry base). Cellulose and hemicellulose (the main carbon sources for anaerobic microorganisms) accounted for 67.4% the total dry mass, indicating that rice straw has a high potential for production of bioenergy based on anaerobic digestion. Lignin is resistant to biological transformation under anaerobic conditions [29] and a lignin content 14.8% in the rice straw has the potential to significantly inhibit digestion. The carbon/nitrogen (C/N) (31.8) was within the acceptable range for anaerobic digestion, thus nitrogen addition was not required. The difference between the sum of lignin, cellulose, hemicelluloses and ash content (10.3% dry base), can be considered as the extractives content, which was 7.5% (dry base). 3.2. Impact of fungal pretreatment on rice straw characteristics Impacts of pretreatment on removal of four specific rice straw components (dry matter, cellulose, hemicellulose and lignin) are shown in Fig. 1 and Table 2. The degradation of the four components in rice straw increased for both P. ostreatus and T. reesi treat-

Dry matter degradation (%)

40

(a)

10 d

35

20 d

30 d

30 25 20 15 10 5 0

65% MC 75% MC 85% MC 65% MC 75% MC 85% MC

Cellulose degradation (%)

40 35

(b)

10 d

20 d

30 d

30

25 20 15 10 5

0

65% MC 75% MC 85% MC 65% MC 75% MC 85% MC 40

Hemicellulose degradation (%)

washed, pretreated rice straw. Another eighteen groups corresponding to the same combinations were fed with unwashed pretreated rice straw. Two additional groups were fed with autoclaved control (no fungus inoculation) and with untreated rice straw, respectively. Feedstock/inoculum VS ratio was 1.0 (5.0 g VS of feedstock and 5.0 g VS of inoculum were fed to each reactor), selected based on initial testing. A group of blank trials containing inoculum only were set up to correct for biogas production by the inoculum. The TS content of all SS-AD reactors was adjusted to 20% by addition of deionized water and feedstock and inoculum were mixed well (manually). Reactors were then carefully examined for any leaks by visual inspection, closed tightly using rubber stoppers and screw caps (fitted with connection tubes) and flushed with argon gas for 5 min to ensure anaerobic conditions. Reactors were then incubated at 37 ± 1 °C for 45 days. Biogas production was measured daily for the first 6 days, and every 3 days thereafter. Biogas components (CH4, CO2, H2, and N2) were measured on a gas chromatograph (GC-2014, Shimadzu, Japan) equipped with a thermal conductivity detector. The temperatures of the column oven, injector port and detector were 100, 120, and 120 °C, respectively. The injection volume of the individual sample to the column was 200 lL. Argon was used as a carrier gas at a flow rate of 30 mL/min. Biogas composition was determined after 5 days of digestion, and then every 10 days thereafter and conducted in duplicate. Biogas yields were adjusted to standard conditions (0 °C, 1 atm) using Eq. (7) [27].

35

(c)

10 d

20 d

30 d

30 25 20 15 10 5 0

65% MC 75% MC 85% MC 65% MC 75% MC 85% MC 40

Lignin degradation (%)

664

35

(d)

10 d

20 d

30 d

30 25 20

15 10 5 0

65% MC 75% MC 85% MC 65% MC 75% MC 85% MC P. ostreatus

T. reesei

Control

Fig. 1. Degradation of rice straw components (a) dry matter, (b) cellulose, (c) hemicellulose and (d) lignin during 10, 20 and 30-day fungal pretreatment under different moisture contents (MC). Data are the means of three replicates.

ment (Fig. 1) compared to no treatment. For P. ostreatus treatment, maximum degradation of dry matter (13.2%), hemicellulose (23.7%) and lignin (35.3%) was observed for pretreatment at 75% moisture content and 30 d incubation time. For cellulose, maximum degradation (13.1%) was observed for 85% moisture content and 30 d incubation time. For T. reesi treatment, maximum degradation of dry matter (10.6%) and hemicellulose (23.3%) was observed for pretreatment at 75% moisture content and 30 d incubation time. For lignin, maximum degradation (23.6%) was observed for pretreatment at 75% moisture content and 20 d incubation time. For cellulose, maximum degradation (20.1%) was observed for 85% moisture content and 30 d incubation time. Loss

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of dry matter is generally associated with degradation of cell wall components, such as cellulose, hemicellulose and lignin [25]. In comparison Zhao et al. [26] reported 12.5% dry matter loss at 60% moisture content and 30 d incubation for yard trimmings with white-rot fungus C. subvermispora while Taniguchi et al. [17] found 30% Klason lignin loss in rice straw treated with P. ostreatus at 60% moisture content for 24 d. Previous studies have reported optimum moisture content for lignin degradation and ligninolytic activity at 70–80% for most white rot fungi [16,25]. Removal of all four components during pre-treatment showed a clear increasing trend with increasing incubation time for both fungi across all three moisture contents, (Fig. 1 and Table 2) with a correlation coefficient of 0.95 on average. For treatment with P. ostreatus, removal was 69.9, 51.0, 71.5, and 59.3% higher at 30 d on average across all moisture contents, compared to 10 d incubation time for dry matter, cellulose, hemicellulose and lignin, respectively. For treatment by T. reesi, the corresponding numbers were 80.7%, 46.3%, 77.9% and 50.1%. Taniguchi et al. [17] also found that cellulose reduction and net yields of total soluble sugar and glucose from pretreated corn stover increased gradually with increasing pretreatment time for 18, 28 and 35 d of incubation at moisture contents of 75–85%. Limited effect of incubation time, however was observed at 60% moisture content [21]. Although degradation of dry matter, cellulose, hemicellulose and lignin was strongly dependent on moisture content, there were no clear trends in the relationships with exception of cellulose degradation which increased with increasing moisture content (Table 2) across all incubation times for both fungi. For the components; dry matter, hemicellulose and lignin, degradation generally seemed to have an optimum at 75% moisture content regardless of incubation time. Increasing moisture content below a specific level would increase the activity of lignin degradation enzymes [26]. However, too much water may prevent fungal growth by limiting the availability of oxygen [16,19]. Increasing degradation with moisture content may be due to absorption of water by the solids. This softens the material, decreases the inner cohesive forces, and causes swelling of the crystalline cellulose structure, increasing the accessibility to enzymes [25,30]. As shown in Fig. 1(C) and (D) hemicellulose and lignin degraded more than cellulose during treatment with P. ostreatus. This was also the case for T. reesi treatments, except at 85% moisture content where cellulose showed the highest degradation. It also can be observed that, more than 90% of the cellulose was retained under most pretreatment conditions (Table 2) for both fungi. The results indicate that P. ostreatus and to some degree also T. reesi selectively degraded hemicellulose and lignin as compared to cellulose. The low degradation of cellulose by especially P. ostreatus is overall positive, because cellulose is considered the main substrate for anaerobic microorganisms in SS-AD to produce biogas [31].

Selectivity defined by Wan and Li [21] as the ratio between lignin removal and cellulose removal, is a key parameter for characterizing the selective lignin-degrading capability of fungi. As shown in Table 2 the highest values of selectivity were 4.3 for P. ostreatus and 2.9 for T. reesi. These values were observed at 75% moisture content for 20 d incubation time for both fungi. This is supported by Wan and Li [21] who found that the maximum ethanol yield from corn stover pretreated by C. subvermispora was achieved at 75% moisture content and 5 mm particle size with a selectivity value of 6.4 and a lignin loss of 29.5%. In comparison, the lowest values of selectivity in this study (1.9 and 0.37) was obtained at 85% moisture content for 30-days incubation time, respectively. Selectivity generally decreased with increasing moisture content regardless of incubation time (average coefficient of correlation = 0.66) although this tendency was somewhat weaker than in case of degradation and incubation time (average coefficient of correlation = 0.95). For P. ostreatus treatment it is further seen that the maximum value of selectivity is observed at decreasing incubation times for increasing values of moisture content (Table 2). The significance of different combinations of moisture content and incubation time for removal of cellulose, hemicellulose and lignin compared to the control was assessed using the MannWhitney U test [32] due to the relatively small number of individual samples for each combination. The results of this test showed that degradation of cellulose, hemicellulose and lignin by P. ostreatus as well as the selectivity value was significantly (p < 0.05) higher than for the control for all nine combinations of moisture content and incubation time. This was also the case for T. reesei except for 85% moisture content. A two-way ANOVA was carried out for both fungi (Table 3) to assess whether the effects of moisture content, incubation time and their interaction on the degradation of cellulose hemicellulose, lignin and selectivity value were significant. The results showed that both moisture content and incubation time generally had significant effect on the degradation of cellulose, hemicellulose and lignin for both fungi, although moisture content had no significant effect on lignin degradation for T. reesi treatments. Interactive effects between moisture content and incubation time, however, were only significant for lignin degradation with P. ostreatus. Similar observations were also done by Wan and Li [21] found that significant interactive effects between moisture content and incubation time on lignin degradation in corn stover by C. subvermispora. Changes in moisture content had significant impact on selectivity while incubation time was unimportant. In comparison [33] found that fungal pretreatment of cornstalk by T. reesei at 77% moisture content resulted in selective degradation of cellulose (23.3–28.8%) and hemicellulose (22.4–24.0%) as compared to lignin (9.2–16.0%), and selectivity value ranging between 0.3 and 0.7 for incubation time between 4 and 8 days. In this study, selectivity

Table 3 Significance of the moisture content (MC), incubation times (IT) and the interaction effect (MC  IT) for several parameters (2-way ANOVA p < 0.05). Parameter

CELLa HCELLa Lignina Selectivity valuea Biogas yieldb Methane yieldb Methane content%a DT90b

P. ostreatus

T. reesei

p-Value MC

p-Value IT

p-Value interaction

p-Value MC

p-Value IT

p-Value interaction

0.005 <0.001 <0.001 <0.001 0.004 0.002 <0.001 0.007

0.004 <0.001 <0.001 0.431 0.536 0.318 0.002 0.025

0.524 0.314 0.002 0.043 0.300 0.132 <0.001 0.005

0.001 <0.001 0.051 0.002 0.004 0.015 0.161 0.285

<0.001 0.033 0.001 <0.001 0.001 <0.001 0.002 0.005

0.063 0.803 0.342 0.010 0.274 0.115 0.836 0.138

MC – moisture content; IT – incubation time; CEL – cellulose; HCEL – hemicellulose. Bold numbers mean significant (p < 0.05). a Data calculated from three replicates. b Data calculated from two replicates.

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did show a significant dependency on the interactive effect between moisture content and incubation time. Overall these results indicate that there is a significant potential for optimizing selectivity by choosing the correct combination of moisture content and incubation time. 3.3. SEM observation Fig. 2 shows SEM images of untreated, control, and pretreated rice straw with P. ostreatus for different moisture contents and incubation times. For untreated rice straw the rigid, arranged fibrils and compact structure are clearly visible. Autoclaving (control) induces a slight level of damage to the structure and causes micro cracking of the surface (Fig. 2B).

Fungal pretreatment by P. ostreatus under all conditions considered resulted in increased structural decomposition. Lignin fibers were damaged, secondary cell walls were exposed (Fig. 2C–H). This is consistent with the increasing surface area observed (Table 2). Comparing images at 10 and 30 d incubation time shows increased structural damage (increased pores size and gaps in the rice straw structure) 30-days incubation time. These results are consistent with the data in Table 2 and Fig. 1, which shows increased lignin removal at longer incubation time which will lead to increased surface area and larger pore size. Wan and Li [34] reported that an increase in pore size from 20 Å or less to 20–50 Å was noticed in fungus pretreated wood, which would allow enzymes to migrate through the cell walls during the initial stages of the degradation.

Fig. 2. SEM image of rice straw particles (a) untreated, (b) control, (c–h) pretreated with P. ostreatus, after 10-days [(c) 65%, (e) 75% and (g) 85% MC] and after 30-days [(d) 65%, (f) 75% and (h) 85% MC].

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pretreated at 75% moisture content and 20 d incubation time for P. ostreatus and T. reesei, respectively. In comparison, the lowest average methane content (59.8%) was observed for T. reesei at 85% moisture content and 30 d incubation time. Ultimate methane yield (taken after 45 d of digestion) for fungus pretreated rice straw ranged from 152 L/kg VS (85% moisture content and 30 d incubation) to 263 L/kg VS (75% moisture content and 20 d incubation) for P. ostreatus and for T. reesei, the corresponding methane yield was 84–214 L/kg VS. Fungal pretreatment improved total methane yield by 27–120% and 9–78% for P. ostreatus and T. reesei (at 65% and 75% MC), respectively, compared with raw rice straw. On the other hand, fungal pretreatment by T. reesei at 85% moisture content decreased total methane yield by 3–30% compared with raw rice straw. As shown in Table 4, the methane yield of 263 L/kg VS obtained by the fungal pretreatment was similar with those reported data obtained in methane fermentation from rice straw pretreated by extrusion, milling combined with alkali, extrusion combined with alkali, alkali, hydrothermal combined with alkali and sodium carbonate [4,35– 37]. As shown in Table 4 after extrusions pretreatment, the chemical compositions of rice straw had not changed, which is not quite the same as thermal, chemical and biological pretreatment. In comparison with the thermal, chemical and thermal–chemical pretreatment, the fungal pretreatment consumes less energy, chemicals and environmentally-friendly technique that may offer a promising option for the improvement of lignocellulosic degradation [33].

3.4. Biogas and methane yield in SS-AD of pretreated rice straw Cumulative biogas production for the eleven (not including the pure inoculum control) SS-AD groups as a function of digestion time is shown in Fig. 3 for both fungi. Ultimate biogas yield (at 45 d) for P. ostreatus pretreated rice straw ranged from 234 L/kg VS (85% moisture and 30 d incubation) to 367 L/kg VS (75% moisture content 20 d incubation) while for T. Reesei, the corresponding biogas yield was 129–299 L/kg VS. Fungal pretreatment by P. ostreatus and T. Reesei (at 65% and 75% MC) improved cumulative biogas yield by 25–96% and 6–60% respectively, compared with the raw rice straw. Furthermore the fungal pretreatment by T. reesei at 85% MC decreased cumulative biogas yield by 5–31% compared with the raw rice straw. Biogas production from the control (204 L/kg VS) was slightly higher than from untreated rice straw (187 L/kg VS), but the difference was not statistically significant at the 95% level. In comparison [25] found that 4 weeks fungal pretreatment of Agropyron elongatum ‘BAMAR’ (Tall Wheat Grass) by the fungus Flammulina velutipes, resulted in a 120% increase in biogas yield compared to the raw material. Methane content as a function of digestion time is shown in Fig. 4 and average methane contents and ultimate methane yield (L/kg VS) from raw, control and pretreated rice straw are shown in Table 2. The methane contents of all reactors stabilized after 15 days, reaching approximately 66%, indicating that all the reactors were healthy. Maximum average methane contents of approximately 72% and 68% were observed during digestion of rice straw 400

(a) Cumulative biogas yield (L/Kg VS)

350 300 250 200 150 Po 65% MC (10d) Po 65% MC (30d) Po 75% MC (20d) Po 85% MC (10d) Po 85% MC (30d) Control

100 50 0 0

5

10

15

20

25

30

Po 65% MC (20d) Po 75% MC (10d) Po 75% MC (30d) Po 85% MC (20d) RS

35

40

45

Digestion time (days)

Cumulative biogas yield (L/Kg VS)

400 350 300

Tr 65% MC (10d)

Tr 65% MC (20d)

Tr 65% MC (30d)

Tr 75% MC (10d)

Tr 75% MC (20d)

Tr 75% MC (30d)

Tr 85% MC (10d)

Tr 85% MC (20d)

Tr 85% MC (30d)

RS

(b)

Control

250 200 150 100 50 0

0

5

10

15

20

25

30

35

40

45

Digestion time (days) Fig. 3. Cumulative biogas yields as a function of time during 45-day SS-AD of untreated rice straw (RS), control and pretreated rice straw by (a) P. ostreatus and (b) T. reesei treatment at different moisture content (MC) and different incubation times, data are the means of two replicates.

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(a)

80

Methane content (Vol. %)

75 70 65 60 55 50 Po 65% MC (10d) Po 75% MC (10d) Po 85% MC (10d) RS

45

Po 65% MC (20d) Po 75% MC (20d) Po 85% MC (20d) Control

Po 65% MC (30d) Po 75% MC (30d) Po 85% MC (30d)

40 0

5

10

15

20

25

30

35

40

45

Digestion time (days) 80

(b)

Methane content (Vol. %)

75 70 65 60 55 50

Tr 65% MC (10d) Tr 75% MC (10d) Tr 85% MC (10d) RS

45 40

0

5

10

15

20

Tr 65% MC (20d) Tr 75% MC (20d) Tr 85% MC (20d) Control

25

30

Tr 65% MC (30d) Tr 75% MC (30d) Tr 85% MC (30d)

35

40

45

Digestion time (days) Fig. 4. Methane content as a function of time during 45-day SS-AD of untreated rice straw (RS), control and pretreated rice straw by (a) P. ostreatus and (b) T. reesei at different moisture content (MC) and different incubation times, data are the means of two replicates.

Table 4 Comparison of methane production from rice straw by various pretreatment methods. Main compositions (% TS) CEL

HCEL

Lignin

37.8 30.0 30.0 30.0 30.0 38.9 38.9 70.2

29.6 29.8 29.8 29.8 29.8 24.0 24.0

14.8 6.5 6.5 6.5 6.5 5.6 5.6 18.3

Pretreatment method

Fungal Extrusion Extrusion Milling + alkali Extrusion + alkali Alkali Hydrothermal + alkali Sodium carbonate

Component degradation (% TS)

Methane yield

Reference

CEL

HCEL

Lignin

Pretreated (L/kg VS)

Untreated (L/kg VS)

Increase (%)

7.9 0 0.7b 5.6b 4.5b ND ND 14.7b

16.9 0 0.3b 15.5b 17.3b ND ND

33.4 0 0 30.0b 35.4b ND ND 49.7b

263 227.3 224c 232c 288 74.1 132.7 292

120 132c 187d 187d 187d 59.8 59.8 130

120 72.2 20c 24c 54 23.7c 121.9c 125

a

This study [35] [4] [4] [4] [36] [36] [37]

CEL – cellulose, HCEL – hemicellulose, ND – not determined. a Compared to untreated sample. b Values calculated from the reference by Eq. (2). c Values calculated from the reference. d Untreated samples were milled.

Methane production from the control (127 L/kg VS) was slightly higher than from raw rice straw (120 L/kg VS), but the difference was not statistically significant at the 95% level. Impact of moisture content and incubation time (as well as their interactive effect) on biogas yield, methane yield and methane content was analyzed using 2-way ANOVA (Table 3). For both biogas yield and methane

yield significant effects of differences in moisture content during pretreatment were observed, however interactive effects between moisture content and incubation time was not significant for both fungi, while impacts of changes in incubation time was significant for T. reesei only. For methane content, effects of changes in moisture content, incubation time as well as their interaction were all

Cumulative methane yield (L/kg VS)

A.M. Mustafa et al. / Applied Energy 180 (2016) 661–671

275 250

(a)

225 200 175 150 y = 35.969x + 96.933 R² = 0.9436

125 100 0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

4.5

Cumulative methane yield (L/kg VS)

Selectivity value 225

(b) 200 175 150 125 y = 41.118x + 89.418 R² = 0.8582

100 75 0.0

0.5

1.0

1.5

2.0

2.5

3.0

Selectivity value Fig. 5. Correlation between the cumulative methane yield and selectivity value of (a) P. ostreatus and (b) T. reesei.

significant with P. ostreatus, while for T. reesei, only effects of changes in incubation time were significant. As shown in Fig. 5 there is a relatively strong linear correlation (R2 = 0.94 and 0.86) between the selectivity value for fungal pretreatment and the ultimate methane yield for P. ostreatus and T. reesei, respectively. In comparison the corresponding correlation between relative lignin removal during pretreatment and ultimate methane yield (not shown) was relatively poor (R2 = 0.69 and 0.71, respectively). This indicates that methane yield depends not only the removal of lignin from the rice straw but also on the quantities of cellulose and hemicellulose left after pretreatment. This means that when pretreating rice straw using fungi, focus should be on maximizing the selectivity value rather than maximizing lignin removal. The SS-AD experiments conducted in this study were operated for a maximum of 45 days. Retention times of this length are usually not economical in practical biogas production as very large reactor volumes are required, and because the biogas yield does not improve much by using retention times above about 30 days for mesophilic digestion. Relative digestion time, DT90, defined as the time required to reach 90% of potential methane yield (cumulative methane yield at 45 days of digestion) divided by total digestion time (45 d), was used to characterize impact of pretreatment on digestion efficiency [38]. The DT90 values for the different treatments are shown in Table 2 and ranged from 46.7–66.7% and 62.2– 75.5% for pretreated rice straw by P. ostreatus and T. reesei, respectively, while raw rice straw and untreated control had DT90 values of 73.3% and 71.1%, respectively. Rice straw pretreated with P. ostreatus at 75% moisture content and 20 d incubation time yielded the greatest reduction in DT90 compared to raw rice straw (57.1%). For P. ostreatus, values of DT90 were further significantly smaller than the control for all nine combinations of moisture content and incubation time as tested by the Mann-Whitney U test, however, this was not the case for T. reesei. These results

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indicate that fungal pretreatment can significantly reduce the required digestion time, potentially resulting in significant economic benefits. As shown in Table 3, the moisture content, incubation time and their interaction had significant effect on required digestion time DT90. In comparison [38] found that DT90 for biologically treated corn straw was 20–45% shorter than that for untreated straw. Washing of rice straw after fungal pretreatment improved biogas and methane yield as shown in Table 2. Ultimate methane yield (at 45 d) for unwashed pretreated rice straw by P. ostreatus ranged from 85 L/kg VS (85% moisture and 30 d incubation) to 195 L/kg VS (75% moisture content 20 d incubation) while for T. Reesei, the corresponding methane yield was 54–127 L/kg VS. In comparison, cumulative methane yields for unwashed, pretreated rice straw were 26–44% and 36–44% lower for P. ostreatus and T. Reesei, respectively. The reason for this difference could be that fungal pretreatment produces compounds such as furan aldehydes (by degradation of sugars), organic acids (from hemicellulose sidegroups), and aldehydes and phenols (from lignin) which may inhibit methane formation during the subsequent digestion [39]. Washing reduces the concentrations of these compounds, thereby improving methane production. In contrast, for ethanol production, washing fungal-pretreated biomass is not necessary, because no inhibitory compounds to yeast fermentation were observed during fungal pretreatment and no significant difference between the ethanol yields of washed and unwashed samples [21].

3.5. Net energy production and practical implementation The net methane energy yield from the overall pretreatment – digestion process can be estimated as the energy in the produced methane minus the energy used for sterilization of the raw rice straw. Energy consumption for sterilization was estimated based on [31] yielding 878 kJ/kg (dry basis). Resulting energy yields for the different pretreatments conditions are shown in Table 5. Total methane energy production from raw rice straw and control were 2333 and 2469 kJ/kg (dry basis) respectively, 2955–5113 kJ/kg (dry basis) for P. ostreatus pretreatments and 1633–4160 kJ/kg (dry basis) for T. reesei treatments. The highest fraction of energy consumed for sterilization was 54% for T. reesei at 85% moisture content and 20 d incubation time, 17–30% for P. ostreatus treatments, and 21–54% for T. reesei treatments, 36% for the control. Maximum net energy production for P. ostreatus and T. reesei treatments was observed at 75% moisture content and 20 d incubation time at 4235 kJ/kg (dry basis) and 3282 kJ/kg (dry basis), respectively. Based on the methane yield observed in this study, and the annual rice straw production (dry basis) of 731 million tons globally [40] and 270 million tons for China [6], potentially 173 and 64 billion m3 of methane can be produced annually Worldwide and in China, respectively. This is equivalent to a net annual energy output of 73.9 and 27.3 Mtoe Globally and in China, respectively. The increase in net energy that may be produced from rice straw via fungal pretreatment is 33.2 and 12.3 Mtoe Globally and in China respectively, as compared to digesting untreated rice straw. In full-scale applications, the long incubation time required for fungal pretreatment is a major constraint for the use of fungal pretreatment. Incubation time can be reduced somewhat by choosing a suitable microbial consortium for example white rot fungi with a high selectivity of lignin degradation over cellulose, or applying fungal pretreatment simultaneously with on-farm wet storage [16,22]. Sterilization constitutes one of the main costs for fungal pretreatment. A recent study found that full sterilization is not needed and short atmospheric steaming (15 s) was enough to allow for adequate growth of white rot fungi [41].

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Table 5 Effect of sterilization on net energy production of rice straw by SS-AD. Experimental factors Fungus type

MC (%)

P. ostreatus

Raw Control 65

75

85

T. reesei

65

75

85

Total methane energy production (kJ/kg, d.b.)

Energy for sterilization (kJ/kg, d.b)

Energy for sterilization (%)

Net methane energy production (kJ/kg, d.b.)

20 10 20 30 10 20 30 10 20 30

2333 2469 4044 4607 4879 3869 5113 4510 3616 3130 2955

0 878 878 878 878 878 878 878 878 878 878

0 36 22 19 18 23 17 19 24 28 30

2333 1591 3165 3729 4001 2991 4235 3632 2738 2252 2077

10 20 30 10 20 30 10 20 30

2547 3577 3285 2877 4160 3694 2197 2274 1633

878 878 878 878 878 878 878 878 878

34 25 27 31 21 24 40 39 54

1669 2699 2407 1999 3282 2816 1319 1396 755

IT (d)

Note: d.b., dry basis.

4. Conclusions Moisture content and incubation time significantly affected the efficiency of fungal pretreatment of rice straw by P. ostreatus and T. reesei with respect to lignin removal during pretreatment and methane yield during subsequent anaerobic digestion. Fungal pretreatment by P. ostreatus caused a significant degradation of lignin and hemicellulose, but had limited effect on cellulose. For treatment by T. reesei, values for lignin and hemicellulose removal were somewhat closer to the cellulose removal in comparison. For P. ostreatus treatment lignin removal was 33.4% with selectivity (lignin/cellulose removal ratio) of 4.30 (the optimal value) at 75% moisture content and 20 d incubation time, resulting in a 120% increase in methane yield compared to untreated rice straw. In comparison, T. reesei treatment yielded a lignin removal of 23.6% at an optimal selectivity of 2.88 at 75% moisture content and 20 d incubation time, and a 78.3% increase in methane yield. For both fungi methane yield showed a strong increasing linear relationship with selectivity value but was only weakly related to lignin degradation during fungal pretreatment. Thus, although fungal pretreatment can significantly improve methane yield from rice straw, it is very important to ensure efficient preferential lignin degradation and high selectivity during pretreatment. Acknowledgements The authors are grateful to the National Science & Technology Pillar Program of China (No. 2012BAC17B02) and the Public Projects of Zhejiang Province (No. 2015C31061) for financial support. The authors also would like to thank Mr. Allen William Bell (Department of Agricultural and Biological Engineering, University of Illinois) for proofreading and language correction. References [1] BP. Statistical Review of World Energy June 2015, 64th ed. . [2] Huang AQ, Crow ML, Heydt GT, Zheng JP, Dale SJ. The future renewable electric energy delivery and management (FREEDM) system: the energy internet. Proc IEEE 2011;99:133–48. [3] Zieminski K, Romanowska I, Kowalska M. Enzymatic pretreatment of lignocellulosic wastes to improve biogas production. Waste Manage 2012;32:1131–7.

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