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J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX

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1 Modified ADM1 for modeling free ammonia inhibition in

2 anaerobic acidogenic fermentation with high-solid sludge

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Jie Bai, He Liu⁎, Bo Yin, Huijun Ma, Xinchun Chen

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4 School of Environmental and Civil Engineering, Jiangnan University, Wuxi 214122, China. E–mail: wxbaijie@163.com

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87 AR TIC LE I NFO ABSTR ACT

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14 Article history: Anaerobic acidogenic fermentation with high-solid sludge is a promising method for

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15 Received 17 December 2015 volatile fatty acid (VFA) production to realize resource recovery. In this study, to model
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16 Revised 3 March 2016 inhibition by free ammonia in high-solid sludge fermentation, the anaerobic digestion
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17 Accepted 7 March 2016 model No. 1 (ADM1) was modified to simulate the VFA generation in batch, semi-
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18 Available online xxxx continuous and full scale sludge. The ADM1 was operated on the platform AQUASIM 2.0.
19 Three kinds of inhibition forms, e.g., simple inhibition, Monod and non-inhibition forms,
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20 Keywords: were integrated into the ADM1 and tested with the real experimental data for batch and
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21 High-solid sludge semi-continuous fermentation, respectively. The improved particle swarm optimization
34 ADM1
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22 technique was used for kinetic parameter estimation using the software MATLAB 7.0. In the
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23 Semi-continuous modified ADM1, the Ks of acetate is 0.025, the km,ac is 12.51, and the KI_NH3 is 0.02,
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24 Full scale respectively. The results showed that the simple inhibition model could simulate the VFA
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25 Free ammonia inhibition generation accurately while the Monod model was the better inhibition kinetics form in
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26 semi-continuous fermentation at pH 10.0. Finally, the modified ADM1 could successfully
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27 describe the VFA generation and ammonia accumulation in a 30 m3 full-scale sludge

28 fermentation reactor, indicating that the developed model can be applicable in high-solid
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29 sludge anaerobic fermentation.

30 © 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences.
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31 Published by Elsevier B.V.

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42
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43 Introduction fermented with the total solid (TS) concentration between 4% 56
and 6% (400–600 g TS/L), which requires a large volume for the 57
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45 The amount of waste activated sludge (WAS) has increased digester and low efficiency (Hansen et al., 1998). Recently, 58
46 significantly due to the rapid growth of wastewater treatment high-solid anaerobic fermentation, with the TS content over 59
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47 during the past few decades, which imposes a big burden 8% or even as high as 15% of the sludge feedstock, is becoming 60
48 on the environment. It is well known that anaerobic fermen- more prevalent due to its merits such as higher loading, 61
49 tation is an effective method to resolve WAS by reduction smaller reactor volume, lower energy consumption and so on 62
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50
Q4 of its volume and generation of valuable products (Appels (Dai et al., 2014). 63
51 et al., 2011). Among the valuable products, volatile fatty Ammonia is produced by the biological degradation of 64
52 acids (VFAs) attract intensive interest because of their wide nitrogenous matter, mostly in the form of proteins and urea 65
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53 range of applications such as in the fields of bioenergy, (Kayhanian, 1999). In high-solid fermentation, there will be a 66
54 bioplastics and biological nutrient removal from wastewater high concentration of ammonia in the fermentation liquid, 67
55 (Lee et al., 2014). In traditional anaerobic digestion, the WAS is which will inhibit the anaerobic fermentative microorganisms 68

⁎ Corresponding author. E-mail: liuhe@jiangnan.edu.cn (He Liu).

http://dx.doi.org/10.1016/j.jes.2016.03.004
1001-0742/© 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 2 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

69 in the digester and consequently limit the VFA production. water. Pre-treatment of sludge by thermal alkaline treatment 126
70 Among the four types of anaerobic microorganisms, the was conducted as follows: the pH of the sludge was adjusted 127
71 methanogens are the least tolerant to ammonia inhibition. to 11.0 using 20 mol/L NaOH solution from an initial pH of 7.0, 128
72 There is conflicting information in the literature about the and then stirred for 2 hr at 90°C (Liu et al., 2012). The process 129
73
Q6 sensitivity of aceticlastic and hydrogenotrophic methanogens. of the acclimation and re-reactivation of seeding sludge was 130
74 The fermentative and acidogenic populations in granular followed as per the previous literature (Wang et al., 2013). 131
75 sludge were hardly affected by the free ammonia (FA) (Chen The characteristics of the fermentation sludge and seeding 132
76 et al., 2008). sludge are shown in Table 1. In order to fit the application in 133
77 Because alkaline fermentation has been widely demon- the model, the organic matter is converted to COD with the 134
78 strated as the optimal condition for the production of VFAs equivalent coefficient. 135
79 from sludge (Yuan et al., 2006), a high pH value further
80 promotes the generation of FA, and this may lead to a stronger 1.2. Fermentation experiments 136

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81 inhibition of VFA fermentation. However, there is less
82 information about the mathematic modeling regarding the The batch and semi-continuous fermentation of sludge were 137

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83 inhibition impacts of high NH3 on VFA generation from sludge carried out in a 30 L anaerobic reactor (GUJS-30C, Zhengjiang 138
84 by anaerobic fermentation, which limits the scale-up of East Co., China). 18.9 L pre-treated sludge and 2.1 L seeding 139

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85 anaerobic digesters and industrial application. sludge were pumped into the reactor for anaerobic fermenta- 140
86 The anaerobic digestion model No. 1 (ADM1) proposed in tion. During the fermentation, the pH of the sludge will 141
87 2002 is a structural model used to establish a common deviate from the target because of the VFA generation, so the 142

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88 platform for modeling anaerobic digestion processes and for pH should be maintained at 11.0 by periodic adjustment. The 143
89 further model development and validation studies (Batstone pH of the sludge was adjusted to pH 11.0 every 48 hr by using 144

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90 et al., 2002). The ADM1 has become a widely used application 20 mol/L NaOH when it was lower than 11.0 or 12 mol/L HCl 145
91 tool for modeling anaerobic digestion. By using the model, solution when it exceeded 11.0, respectively. Nitrogen gas was 146
92 anaerobic processes can be simulated and predicted in a sparged into the reactor for 10 min to remove the oxygen from
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93 variety of operating conditions. Many studies based on the the headspace after sampling and pH adjustment. The 148
94 original ADM1 have been applied to describe the whole temperature was kept at 37 ± 1°C. 149
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Q7 process and results (Batstone, 2006; Rodriguez et al., 2006; In the semi-continuous experiment, a 21.0 L sludge mix- 150
96 Girault et al., 2012). However, in the conventional ADM1 ture was pumped into the anaerobic reactor, and the other 151
97 152
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structure, inhibition by FA only considered the inhibitor operation conditions were the same as those in batch
98 concentration and the inhibitor parameter (Batstone et al., fermentation. After reaching the stable stage, the fermenta- 153
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99 2002). Since the hydrophobic ammonia molecule may diffuse tion was converted to a semi-continuous experiment. 4.2 L 154
100 passively into the cell, causing proton imbalance and/or fermented sludge was discharged and 4.2 L fresh pre-treated 155
101 potassium deficiency in acidogenic microorganisms, the sludge was pumped into the reactor every 2 days, so the 156
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102 inhibition by ammonia with high concentration should be sludge retention time was 10 days. Samples were taken every 157
103 re-considered and integrated into the ADM1 to elaborate the 2 days for analysis. 158
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104 model structure. Therefore, it is necessary to compare and The full scale sludge fermentation was conducted in 159
105 integrate proper kinetiac forms to simulate the inhibition due Shuofang Wastewater Treatment Plant, Wuxi, China. During 160
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106 to FA in WAS fermentation systems for VFA production. the fermentation, 21 m3 pre-treated sludge (TS = 8%) and 161
107 Several algorithms have been used to estimate the parame- 0.2 m3 seeding sludge were pumped into the fermentation 162
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108 ters for simulating the biochemical reactions (Ni et al., 2011). reactor. The methods of sludge pretreatment and seeding 163
109 Particle swarm optimization (PSO) is a novel evolutionary sludge acclimation were the same as the methods used in the 164
110 algorithm which has many advantages over the other laboratory experiment. The whole fermentation was divided 165
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111
Q8 algorithms in some aspects (Kennedy, 2010). However, few into a start-up period (days 0–18) and stable operation period 166
112 papers have applied PSO in ADM1 for parameter estimation. (days19–48). The start-up period was batch fermentation and 167
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113 The objective of this study is to develop a modified ADM1

114 model to better characterize the FA inhibition and simulate
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the VFA accumulation in anaerobic fermentation with both

Table 1 – The characteristics of the pretreated sludge t1:1
116 experimental and modeling approaches. Furthermore, the
liquid. t1:2
117 modified ADM1 was also used to simulate the VFA production t1:3
Q1
Parameters Value Input values of model t1:4
118 in a semi-continuous digester and 30 m3 full-scale sludge
(mg/L) (kg COD/m3)
119 fermentation reactor.
Total COD 36,982.58 36.98 t1:5
Soluble COD 30,884.62 30.86 t1:6
Total COD (seeding sludge) 31,381.54 31.38 t1:7
121
120 1. Materials and methods
Proteins 9341.67 21.52 t1:8
Carbohydrates 2240.01 3.45 t1:9
122 1.1. Sludge characteristics and pre-treatment method Lipids 952.07 2.77 t1:10
Total nitrogen 2089.75 ―― t1:11
123 The WAS used in the study was dewatered sludge obtained Ammonia nitrogen 1217.88 ―― t1:12
124 from the Taihu Xincheng Wastewater Treatment Plant, Wuxi,
“――”No unit conversion. t1:13
t1:14
125 China. The sludge was diluted to TS of 75 g/L with distilled

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 3

168 the stable operation period was semi-continuous fermenta- listed in Appendix A Tables S3–S4. Typically, inhibition such 213
169 tion. In the start-up period, the fermentation was batch mode, as that due to long-chain fatty acids was classified as toxic, 214
170 so the VFAs will eventually accumulate to a plateau. After while ammonia inhibition was considered as non-competitive 215
171 the VFAs stopped increasing, the fermentation was switched inhibition. A simple inhibition form was proposed by 216
172 into semi-continuous fermentation mode. During the semi- Lehninger and given in Eq. (1) (Granger and Lehninger, 1982). 217
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173 continuous fermentation, 2.1 m3 fresh sludge was pumped
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174 into the reactor each day after the same volume of sludge was I¼  ð1Þ
1 þ SI KI
175 pumped out from the reactor. The VFAs will maintain stability
176 if the fermentation is operated well. Based on this operation 219
218
In the above form, non-competitive inhibition was only 220
177 mode, when the fluctuation of VFA yield was less than 10%– influenced by the concentration of inhibitors and the influ- 221
178 15% of the average yield, the fermentation was considered to ence of substrate concentration was ignored. Also, studies 222
179 be in stable status. During the fermentation, the VFAs, total have reported that the Monod kinetics form can also be used 223

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180 nitrogen and ammonia nitrogen were measured every day. to describe the inhibition process. This is shown in Eq. (2) 224
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181 The fermentation temperature was controlled at 35 ± 2°C, 225

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(Sprott and Patel, 1986).
182 with stirring rate of 48 r/min and pH at 10.0–11.0. During the
183 operation, sludge samples were taken every day or two days km;i XS
rj ¼    ð2Þ

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184 for analysis. KS;i þ S 1 þ KI SI

185 1.3. Analytical methods The two forms of inhibition equations and definition of 226
227
228

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parameters are listed in Appendix A Table S1. 229
186 Before the VFA assay, the sludge samples were centrifuged The determination coefficient (R2) values were used to 230

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187 10 min at 10,000 r/min at room temperature and the super- evaluate the accuracy of the model simulation and experi- 231
188 natants were used for VFA measurement. The VFAs were mental data of different forms of FA inhibition. If the model is 232
189 measured by a gas chromatograph (GC-2010, Shimadzu Co., more accurate, the R2 is closer to 1, indicating the simulated
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190 Japan) equipped with an auto injector (AOC-20i, Shimadzu data are in agreement with the actual data. 234
191 Co., Japan). The liquid sample was pretreated by filtration
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192 through a 0.45 μm filter membrane (Liu et al., 2011). A flame 1.5. Parameter estimation 235
193 ionization detector was used and the column was a fused
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194 silica capillary (PEG-20 M, 30 m × 0.32 mm × 0.51 m, China); During the parameter optimization, ADM1 takes the specific 236
195 4-methyl-valeric acid was added as an internal standard and parameters km,i, and Ks,j as variables. The difference between 237
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196 the samples were acidified by 3 mol/L phosphoric acid. The the true and simulated values was taken as the objective 238
197 initial temperature of the GC column was 80°C and was held function. Then, we minimized the objective function to 239
198 for 3 min, then increased by 15°C/min to a final temperature improve the accuracy of simulation. 240
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199 of 210°C, and then held for 2 min. Among the available algorithms, PSO is a widely used 241
algorithm for global space search in several algorithms that 242
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200 1.4. Model modification and inhibition functions are used in estimating. For parameter estimation, an im- 243
proved PSO method was used for ADM1 optimization (Bai 244
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201 The ADM1 model contains the disintegration, hydrolysis, et al., 2015). The estimation was conducted using the platform 245
202 acidogenesis and methanogenesis process in the WAS anaer- of MATLAB 7.0. The Monod maximum uptake rate parameters 246
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203 obic fermentation. Due to the strong inhibition caused by the km , i and Monod half saturation constant Ks,j in the modified 247
204 FA released from the high-solid sludge, the inhibition due to ADM1 model were estimated with the experimental data 248
205 FA on VFA generation was considered in the modified ADM1 using the PSO algorithm. With the estimation based on the 249
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206 model. Modifications of the main inhibition form in the model improved κ-PSO, the optimal values of the parameters are 250
207 are listed in Appendix A Table S2. The ADM1 was simulated by shown in Appendix A Fig. S1. As shown in Fig. S1A, B and C, 251
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208 AQUASIM 2.0 in this study. The stoichiometric coefficients after 500 iterations by κ-PSO, the Ks of acetate is 0.025, the 252
209 were calculated from the concentrations of the substrate km,ac is 12.51, and the KI-NH3 is 0.02, respectively. 253
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210 components in Table 2. The values of other coefficients used

211 in modeling are from Batstone et al. (2002). Additional
212 parameters and the initial state in the model calculation are 2. Results and discussion 255
254

2.1. Modeling simulation in batch fermentation 256

t2:1 Table 2 – Stoichiometric coefficients for ADM1.
t2:3
t2:2
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t2:4 Symbol Definition Values A high concentration of FA is one of inhibiting factors in the 257
fermentation of high-solid WAS for VFA generation. To 258
t2:5 fsi_XC Fraction of soluble inert from components 0.085
t2:6 fxi_XC Fraction of insoluble inert from components 0.165 evaluate the simulation by the modified ADM1 that integrated 259
t2:7 fch_XC Fraction of particulate carbohydrates from 0.091 simple inhibition, Monod inhibition or non-inhibition forms 260
components of high FA inhibition, the model was first tested with the 261
t2:8 fpr_XC Fraction of particulate proteins from 0.581 experimental data in the batch fermentation. The experimen- 262
components tal data for acetate, propionate, butyrate and valerate accu- 263
t2:9 fli_XC Fraction of particulate lipids from components 0.075
mulation and the simulation results are shown in Fig. 1. 264

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 4 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

265 As shown in Fig. 1, the acetate, propionate, butyrate and acetogens and homoacetogens. (Jabłoński and Łukaszewicz, 294
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266 valerate concentrations increased from the initial value of 0 2014). Many factors will influence the activity of these 295
267 to 13.40 kg COD/m3, 0.98 kg COD/m3, 7.80 kg COD/m3 and microorganisms, which then influences the VFA generation. 296
268 1.02 kg COD/m3 on day 22, respectively. They all increased In this study, we focused on the effect of high concentrations 297
269 rapidly during days 4–6 and then maintained stability during of FA on the VFA generation and simulated the process by the 298
270 the rest of the fermentation. The generation of acetate, modified ADM1. The simulated results in Fig. 1 show that a 299
271 propionate, butyrate and valerate was simulated by AQUASIM proper FA inhibition form in the ADM 1 structure is important 300
272 2.0 with the simple inhibition, Monod and non-inhibition forms for VFA simulation. 301
273 respectively. For each modified model structure, the parame-
274 ters were estimated by the improved PSO algorithm. Through 2.2. Modeling simulation in semi-continuous fermentation 302
275 structure modification and proper parameter estimation, the
276 ADM1 model has been demonstrated to successfully simulate After the evaluation of the modified ADM1 in batch fermen- 303

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277 the VFA accumulation under FA inhibition conditions in sludge tation, it was further applied in the simulation of the VFA 304
278 fermentation for VFA production (Bai et al., 2015). profiles in semi-continuous fermentation. The experimental 305

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279 It was shown that the simple inhibition model could data and the simulation results from the modified ADM1 are 306
280 simulate the production of VFAs better than the other two plotted in Fig. 2. 307

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281 models in the batch reactor at pH 6.5 over 22 days. It can be As shown in Fig. 2a, the concentration of acetate increased 308
282 seen that the data predicted by ADM1 with the non-inhibition from 6 kg COD/m3 to 9 kg COD/m3 and remained at that 309
283 form are always much lower than the experimental data level during the whole fermentation. In Fig. 2b and d, the 310

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284 (Fig. 1). This is because a high concentration of FA not only trends of propionate and valerate concentrations during the 311
285 inhibits the acidogenic microorganisms, but also inhibits the whole semi-continuous fermentation process are similar to 312

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286 methanogens very seriously (Chen et al., 2008). In the absence those for acetate, but their concentrations (0.75 kg COD/m3 313
287 of FA inhibition in the ADM1 model, the methanogens will and 0.55 kg COD/m3, respectively) are much lower than 314
288 consume the acetate, and this causes lower predicted values acetate. The butyrate concentration also followed the change
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289 for VFA data than the real determined data. trend of acetate, and its final concentration was about 316
290 VFAs are intermediates during the anaerobic fermentation 5.5 kg COD/m3 (Fig. 2c). The production of acetate, propionate, 317
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291 of sludge, and the generation process is a series of biochem- butyrate and valerate were simulated with the simple 318
292 ical reactions driven by different functions of facultative and inhibition form, Monod and non-inhibition form, respectively. 319
293 320
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anaerobic microbes, such as fermentative bacteria, syntrophic It was shown that the Monod model can simulate the
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Fig. 1 – Modeling results (line) and the experiment results (open cycle) of volatile fatty acid production in the anaerobic batch
fermentation.

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 5

Simple inhibition form a b

Monod inhibition form
Non-inhibition form

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c d

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Fig. 2 – Modeling results (line) and the experiment results (open cycle) of VFAs production in semi-continuous fermentation. a:
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acetate; b: propionate; c: Butyrate; d: valerate. VFA: volatile fatty acid.
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321 production of VFAs better than the other two models in batch fermentation experiment. The other determination co- 340
322 semi-continuous fermentation. efficient values for propionate, butyrate and valerate showed 341
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323 Traditionally, ammonia inhibition in anaerobic fermenta- that the simple inhibition model can also simulate the 342
324 tion has been modeled based on the simple form of ammonia production of VFAs very well. However, in the semi- 343
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325 inhibition in ADM1, which was proposed by Lehniner, continuous fermentation experiment, the R2 values for the 344
326 assuming that the inhibition rates depend on inhibition simple inhibition, Monod and non-inhibition forms for 345
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327
Q12 parameters and concentrations (Granger and Lehninger, acetate are 0.9750, 0.9923 and 0.9310, respectively. The R2 346
328 1982). However, for complex substrates with high concentra- results showed that the Monod inhibition model was the 347
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329 tions of FA, more complex kinetic forms should be more proper form for simulation of FA inhibition. 348
330 applicable.
2.4. Modeling simulation in full scale fermentation 349
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331 2.3. The determination coefficient analysis

According to the modified ADM1 model, the fit between the 350
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332 The R2 values for model simulation and experimental data of experimental data for acetate, propionate and butyrate 351
333 different FA inhibition forms are shown in Table 3. If a model accumulation as well as the ammonia accumulation in a 352
334 accurately predicts the experimental result, R2 should be close 30 m3 full-scale anaerobic digester and the simulation results 353
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335 to 1.0. The R2 values for the simple inhibition, Monod and are plotted in Fig. 3. The full-scale fermentation was divided 354
336 non-inhibition forms for acetate in the batch reactor at into a start-up stage (days 0–16) and semi-continuous stage 355
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337 pH 10.0 were 0.9842, 0.9558 and 0.7988, respectively. (days 17–48). 356
338 The R2 results showed that the simple inhibition model As shown in Fig. 3a, the acetate increased rapidly in the 357
339 was the proper form for simulation of FA inhibition in the start-up stage and maintained at about 4.5 kg COD/m3 in the 358

t3:1 Table 3 – The determination coefficient values (R2) of the different models.
t3:3
t3:2
t3:4 R2of VFAs Batch fermentation Semi-continuous fermentation

t3:5 Acetate Propionate Butyrate Valerate Acetate Propionate Butyrate Valerate

t3:6 Simple form 0.9842 0.9345 0.9953 0.9792 0.9750 0.9750 0.9625 0.9336
t3:7 Monod form 0.9558 0.9184 0.9664 0.9287 0.9923 0.9923 0.9948 0.9694
t3:8 Non-inhibition form 0.7988 0.7079 0.7840 0.7695 0.9310 0.9310 0.9445 0.9231

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 6 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

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Fig. 3 – Modeling results (line) and the experiment results (open cycle) of the VFAs (a) and total nitrogen (b) and ammonia
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nitrogen (c) in full scale sludge fermentation. VFA: volatile fatty acid.
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359 semi-continuous stage. Meanwhile, the change trends of The total nitrogen and ammonia nitrogen concentrations 372
360 propionate, butyrate and valerate were similar to that of and their simulation results are plotted in Fig. 3b and c. As 373
361 acetate, and their average concentrations were 0.85 kg/m3, shown in Fig. 3b, the total nitrogen increased from 0.04 mol/L 374
362 1.77 kg/m3 and 0.68 kg/m3 (calculated as COD), respectively. in the start-up stage and then maintained at 0.09 mol/L in 375
363 The experimental data were simulated with the simple the semi-continuous fermentation stage. The total nitrogen 376
364 inhibition form (in the start-up stage) and Monod inhibition starts off with a high concentration during the fermentation 377
365 form (semi-continuous stage) of the modified ADM1 model. because of the thermo/alkalinity pretreatment of the sewage 378
366 According to the simulation results, it can be seen that the sludge, which caused the release and accumulation of total 379
367 two forms of models can fit the acetate, propionate, butyrate nitrogen. It should be noted that due to the changes in 380
368 and valerate data well, indicating that the modified ADM1 influent sludge concentrations and operation conditions, the 381
369 model with the two FA inhibition forms can simulate the ammonia nitrogen concentrations fluctuated greatly in the 382
370 practical experimental data even in full-scale sludge fermen- semi-continuous fermentation stage. The ammonia nitrogen 383
371 tation for VFA production. concentrations were close to 0.01 mol/L during the whole 384

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 7

385 stage of fermentation. After the simulation, the curve can fit and Technology (No. 2014BAD24B03-02). We also thank 440
386 the experimental data very well. Dr. Damien Batstone for kindly providing software support. 441
387 The R2 values were also calculated to show goodness of fit
388 between the simulated data and the experimental data of
389 different VFAs, total nitrogen, and ammonia (Fig. 3) in the Appendix A. Supplementary data 443
442
390 full-scale fermentation process. The R2 values of acetate,
391 propionate, butyrate and valerate were 0.9552, 0.9678, 0.9851 Supplementary data to this article can be found online at 444
392 and 0.9871, respectively. The R2 results for total nitrogen and http://dx.doi.org/10.1016/j.jes.2016.03.004. 445
393 ammonia were 0.9896 and 0.9921, respectively. The relative
394 errors for full scale fermentation were all about 0.05,
395 suggesting that there is a reasonably good agreement between
REFERENCES 44 6
396 the model outputs and the experimental results.

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397 By using standard ADM1 variables and kinetics for the
447
398 modified FA inhibition forms calibrated based on batch Appels, L., Lauwers, J., Degrève, J., Helsen, L., Lievens, B., et al., 448

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399 fermentation, the modified ADM1 models were able to 2011. Anaerobic digestion in global bio-energy production: 449
Potential and research challenges. Renew. Sust. Energ. Rev. 15 450
400 successfully predict the reactor performance under full-scale
(9), 4295–4301. 451

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401 scenarios. Predicted acetate accumulation generally complied
Bai, J., Liu, H., Yin, B., Ma, H.J., 2015. Modeling of enhanced VFAs 452
402 with the experimental observations, with deviations attribut- production from waste activated sludge by modified ADM1 453
403 ed to less accurate predicted inhibitory processes etc. Many with improved particle swarm optimization for parameters 454

R
404 studies have investigated the impacts of FA inhibition on the estimation. Biochem. Eng. J. 103, 22–31. 455
405 VFA accumulation from waste activated sludge (Gallert et al., Batstone, D.J., 2006. Mathematical modelling of anaerobic reactors 456

P
406 1998), however, there is little information about the modifi- treating domestic wastewater: Rational criteria for model use. 457
Rev. Environ. Sci. Bioresour. Technol. 5, 57–71. 458
407 cation of ADM1 for VFA generation in the condition of high
Batstone, D.J., Keller, J., Angelidaki, I., Kalyuzhnyi, S.V., 459
408 FA-based inhibition. It has been confirmed that the alkaline Pavlostathis, S.G., Rozzi, A., Vavilin, V.A., 2002. The IWA 460
409 condition was the optimal condition for VFA accumulation in
D anaerobic digestion model no 1 (ADM 1). Water Sci. Technol. 45 461
410 sludge fermentation. (10), 65–73. 462
E
411 Finally, it is important that the data simulated by modified Chen, Y., Cheng, J.J., Creamer, K.S., 2008. Inhibition of anaerobic 463
412 ADM1 models can fit the experimental data in full-scale digestion process: A review. Bioresour. Technol. 99 (10), 464
4044–4064. 465
T

413 sludge fermentation well, indicating that the improved ADM1

Dai, X., Gai, X., Dong, B., 2014. Rheology evolution of sludge 466
414 was verified to be applicable for batch, semi-continuous and
through high-solid anaerobic digestion. Bioresour. Technol. 467
C

415 full-scale sludge fermentation systems. 174, 6–10. 468

Gallert, C., Bauer, S., Winter, J., 1998. Effect of ammonia on the 469
anaerobic degradation of protein by a mesophilic and 470
E

thermophilic biowaste population. Appl. Microbiol. Biotechnol. 471

417
416 3. Conclusions 50 (4), 495–501. 472
R

Girault, R., Bridoux, G., Nauleau, F., Poullain, C., Buffet, J., Steyer, 473
418 In this study, three kinds of FA inhibition forms, e.g., simple J.P., Béline, F., 2012. A waste characterisation procedure for 474
419 inhibition, Monod inhibition or non-inhibition forms, were ADM1 implementation based on degradation kinetics. Water 475
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420 integrated into the ADM1 model, respectively, and the Res. 46 (13), 4099–4110. 476
421 simulation results were tested with the experimental data in Granger, D.L., Lehninger, A.L., 1982. Sites of inhibition of 477
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mitochondrial electron transport in macrophage-injured 478

422 batch, semi-continuous and full-scale sludge fermentation. In
neoplastic cells. J. Cell Biol. 95 (2), 527–535. 479
423 the modified ADM1, the KS of acetate is 0.025, the km,ac is 12.51, Hansen, K.H., Angelidaki, I., Ahring, B.K., 1998. Anaerobic 480
and the KI-NH3 is 0.02, respectively. The statistical R2 values
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424 digestion of swine manure: inhibition by ammonia. Water Res. 481

425 showed that the simple inhibition form can simulate the VFA 32 (1), 5–12. 482
426 generation better than the other two forms in a batch reactor, Jabłoński, S.J., Łukaszewicz, M., 2014. Mathematical modelling of 483
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427 while the Monod kinetics form was more appropriate to methanogenic reactor start-up: Importance of volatile fatty 484
acids degrading population. Bioresour. Technol. 174, 74–80. 485
428 simulate the VFA production in semi-continuous fermenta-
486
U

Kayhanian, M., 1999. Ammonia inhibition in high-solids

429 tion. Finally, the modified ADM1 model was successfully
biogasification: An overview and practical solutions. Environ. 487
430 developed to describe the VFA generation and ammonia Technol. 20 (4), 355–365. 488
431 accumulation in a 30 m3 full-scale sludge fermentation Kennedy, J., 2010. Particle swarm optimization. In encyclopedia of 489
432 reactor, indicating that the model developed in this study machine learning. Springer US, pp. 760–766. 490
433 was applicable for different high-solid sludge fermentation Lee, W.S., Chua, A.S.M., Yeoh, H.K., Ngoh, G.C., 2014. A review of 491
434 systems. the production and applications of waste-derived volatile fatty 492
acids. Chem. Eng. J. 235, 83–99. 493
Liu, H., Wang, J., Liu, X., Fu, B., Chen, J., Yu, H.Q., 2012. Acidogenic 494
fermentation of proteinaceous sewage sludge: Effect of pH. 495
Water Res. 46 (3), 799–807. 496
436
435 Acknowledgments
Liu, H., Wang, J., Wang, A., Chen, J., 2011. Chemical inhibitors of 497
methanogenesis and putative applications. Appl. Microbiol. 498
437 This work was supported by the Joint Innovative R&D Program Biotechnol. 89 (5), 1333–1340. 499
438 of University and Industry (No. BY2014023-03) and National Ni, B.J., Liu, H., Nie, Y.Q., Zeng, R.J., Du, G.C., Chen, J., Yu, H.Q., 2011. 500
439 Key Technology R&D Program of the Ministry of Science Coupling glucose fermentation and homoacetogenesis for 501

Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004
 8 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

502 elevated acetate production: Experimental and mathematical anaerobic acidogenic fermentation of sewage sludge. Biochem. 511
503 approaches. Biotechnol. Bioeng. 108 (2), 345–353. Eng. J. 70, 1–8. 512
504 Rodriguez, J., Lema, J., van Loosdrecht, M., Kleerebezem, R., 2006. Yuan, H., Chen, Y., Zhang, H., Jiang, S., Zhou, Q., Gu, G., 2006. 513
505 Variable stoichiometry with thermodynamic control in ADM1. Improved bioproduction of short-chain fatty acids (SCFAs) 514
506 Water Sci. Technol. 54 (4), 101–110. from excess sludge under alkaline conditions. Environ. Sci. 515
507 Sprott, G.D., Patel, G.B., 1986. Ammonia toxicity in pure cultures of Technol. 40 (6), 2025–2029. 516
508 methanogenic bacteria. Syst. Appl. Microbiol. 7 (2), 358–363. 517
509 Wang, J., Liu, H., Fu, B., Xu, K., Chen, J., 2013. Trophic link between
510 syntrophic acetogens and homoacetogens during the
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Please cite this article as: Bai, J., et al., Modified ADM1 for modeling free ammonia inhibition in anaerobic acidogenic fermentation
with high-solid sludge, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2016.03.004