A novel, repeated fed-batch, ethanol production system with extremely long term stability achieved by fully recycling fermented supernatants

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1 Biotechnology Letters 25: , Kluwer Academic Publishers. Printed in the Netherlands A novel, repeated fed-batch, ethanol production system with extremely long term stability achieved by fully recycling fermented supernatants Xin Lu, Yongfei Li, Zuoying Duan, Zhongping Shi & Zhonggui Mao The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Southern Yangtze University, Wuxi , P.R. China Author for correspondence (Fax: ; zpshi@sytu.edu.cn) Received 11 July 2003; Revisions requested 24 July 2003; Revisions received 1 September 2003; Accepted 2 September 2003 Key words: ethanol production, minimum wastewater discharge, repeated fed-batch, Saccharomyces, soluble inhibitors, supernatant recycle Abstract Using Saccharomyces cerevisiae, a novel, repeated fed-batch ethanol production system from corn flour by fully recycling fermented supernatants is demonstrated. With recovery of ethanol by evaporation coupled with consecutive removal of the insoluble and soluble inhibitory substances accumulated, either completely or partially by filtration, the concentrations of the soluble inhibitors in the system could be maintained at their equilibria. As a result, a sustained high concentration of ethanol (up to 15% v/v) and significant pollution control performance were obtained. Introduction Fermentation is a water-intensive process with much of the effluent water having a high BOD. It is therefore desirable to minimize the discharge of the waste stream from the fermentation process. For these reasons, recycling the process effluent can be economically beneficial (Hsiao & Glatz 1995). In situ ethanol recovery and complete recycling of the used medium during continuous fermentation by Saccharomyces cerevisiae to produce ethanol has been studied (Converti et al. 1991): the final concentrations of soluble, non-fermentable oligosaccharides and ions (Ca 2+,Mg 2+,Mn 2+,Fe 2+,andZn 2+ ) in the broth increased times compared with those at the beginning of the fermentation and reached the inhibitory levels after 40 d of continuous used-medium recycling. Further, the accumulation of the non-fermentable oligosaccharides and ions is also inhibitory to the ethanol fermentation so that the stable ethanol production completely stopped. To overcome this problem, the method of installing enzymatic hydrolysis and ion removal stages in the process to eliminate the inhibition has been proposed (Converti et al. 1991). However, the complicated features of the process made it difficult to put into practical use. In other studies, methods of recycling distillery waste either using ultrafiltration (Kim et al. 1997, Teramoto et al. 1993) or recycling as much as 75% of spent broth (Hsiao et al. 1994) were applied to alcohol fermentation processes and batch yeast fermentation. In the first case, Kim et al. (1997) showed that direct recycle of stillage without ultrafiltration adversely effected on both the fermentation time and alcohol yield as recycling was repeated, while the process with ultrafiltration could ensure a stable ethanol production over 8 recycles (a total of 26 d) without significant performance [ethanol productivity and concentration (about 9% v/v)] reduction. It is of great interest to know both theoretically and experimentally whether and how a fermentation system associated with full utilization of the used medium could be operated infinitely. In this study, we focused on investigating full utilization of the used supernatants to the repeated fed-batch ethanol fermentation, aiming at constructing an effective and simple ethanol production system with extremely long term stability and a minimum wastewater discharge, while maintaining ethanol concentration in the effluent stream

2 1820 at a high level to reduce the cost of the downstream process. Materials and method Microorganism Saccharomyces cerevisiae Y002, screened and isolated in this laboratory, was used throughout this study. This strain has a strong fermentative capability and is resistant to high ethanol and sugar concentrations. Saccharification of corn flour Corn flour (raw starch content about 62% w/w) was mixed 1:3 (w/w) with water at 70 C, adding 14 units g 1 corn of the heat resistant α-amylase ( units ml 1, Genencor Biotech Co., Wuxi, P.R. China), and then heated at 95 C for 18 min. The hydrolyzed solution was then cooled down to 60 C, and then 150 units g 1 corn of glucoamylase ( units ml 1, Genencor Biotech Co., Wuxi, P.R. China) was added to convert the majority of the remaining oligosaccharides into reductive sugars (glucose). The saccharification process continued at 60 Cfor9h. The amounts of α-amylase and glucoamylase, as well as their acting time were determined and optimized by experiments. Fermentation medium The seed yeast was grown in a shaker at 28 Cand 100 rpm for 18 h in liquid medium containing 5% (w/v) soluble saccharified sugars (containing reductive sugar and some oligosaccharides) and 0.85% (w/v) yeast extract. The fermentation medium consists of 15% (w/v) soluble saccharified sugars, 0.25% (w/v) urea, 0.06% (w/v) KH 2 PO 4, 0.06% (w/v) MgSO 4,and a Ca salts complex of 4.1 mg l 1 (containing 2 mg CaCl 2 l 1 and 2.1 mg CaCO 3 l 1 ). Fed-batch ethanol fermentation The fed-batch operation was implemented in a 2 l flask with the initial working volume of 0.75 l, containing 15% (w/v) sugar, 8% (v/v) inoculums, and the above mentioned fermentation medium. Feeding medium 375 ml, consisting of sugars 35% (w/v), urea 1.73 g l 1,KH 2 PO 4 0.6gl 1,MgSO 4 0.6gl 1,and the above mentioned Ca salts complex 4.1 mg l 1,was added into the flask twice in equal amount at 12 h and 24 h, to make up the final working volume 1.5 l. The fermentation was carried out at 34 C for 60 h. Repeated fed-batch ethanol fermentation with fully recycling of the used supernatants The scheme of the repeated fed-batch ethanol fermentation with fully recycling of the used supernatants is shown in Figure 1. When one operation run finished, the fermentation broth was filtrated to remove the yeast cells, and then the supernatants were transferred into an evaporation unit for heating to strip the ethanol. The supernatants collected at the bottom of the evaporator, were then cooled down and then used for hydrolysis and saccharification of newly added corn flours for the next fermentation run. Amounts of α- amylase and glucoamylase for the hydrolysis and saccharification, as well as the relevant conditions were as per those described before. The insoluble substances unfriendly to the fermentation (insoluble polysaccharides, solid proteins, etc.) produced in the hydrolysis and saccharification liquid were removed by another filtration unit. The newly filtrated sugar syrup was mixed with the other fermentation medium components: 0.25% (w/v) urea, 0.06% (w/v) KH 2 PO 4, 0.06% (w/v) MgSO 4, and a Ca salts complex of 4.1 mg l 1. Then, they were transferred into the fermentation flask again. Seed inocula (8% v/v) were added to obtain a 0.75 l initial working volume to start a new fermentation run. Feeding medium 375 ml described before (also dissolved and saccharified by the used supernatants), was added into the flask twice at 12 h and 24 h. The fed-batch fermentation was carried out at 34 C for 60 h. In the repeated fed-batch fermentation process, parts of the fermentation broth are used as the seed for the next fermentation run. However, in our case, the fermentative activity of the yeast cells at the end of each run was very weak as they had been subject to high ethanol concentration for a long time, thus the alternative fresh seed inocula addition method was used throughout the experiments. Evaporation When fermentation finished, the fermented broth was transferred into a glass evaporator where the broth was vigorously mixed and heated to 98 C for 11 min to effectively evaporate the ethanol. The removed ethanol was then recovered by condensation.

3 1821 Fig. 1. The scheme of the repeated fed-batch fermentation associated with fully recycling of the used supernatants. Filtration units The conventional filtration equipment used here was one plate of m in dimension, 0.25 m 2 effective filtration area, 4 plate stations, and 0.1 MPa working pressure. The cotton materials with 8 layers were used as the filtration septum. The filtration septum was changed and the old filtration cake was taken out when each cycle finished. Analytical methods Concentration of glucose was determined by the dinitrosalicylate method. The ethanol concentration was detected by GC at 50 C. Concentrations of oligosaccharides were measured by HPLC using a Waters Sugarpak Column and a refractive index detector with water as the mobile phase at 0.5 ml min 1 and 85 C. The organic by-products considered herewith, the lactic acid was measured by the same HPLC with an Agilent-1100 ZORBAX SB-C18 column equilibrated with 0.5 ml min 1 of 0.1 M K 2 HPO 4 /KH 2 PO 4, and its concentration was detected at 215 nm. The anion concentrations (H 2 PO 4 and SO2 4 ) were measured by an AS4A anion chromatography column (Dionex, USA), at room temperature with 1.7 mm NaHCO 3 /1.8 mm Na 2 CO 3 as the mobile phase. The cation concentrations (K + and Mg 2+ ) were measured by an atomic absorption spectrography with the carrier gas of air/acetylene at 6 l min 1 and1lmin 1, respectively. Results and discussion Repeated fed-batch ethanol fermentation strategy When ethanol was fermented in batch mode with 30% (w/v) initial sugar syrup, the final ethanol reached the most concentrated level of 16.5% (v/v) at 96 h. However, due to the sugar inhibitory effect at high concentration, the sugar conversion yield to ethanol was only about 75%, the ethanol productivity was low, and a large amount of residual sugar was drained out in the effluent stream. By taking the overall performance into consideration, the repeated fed-batch policy described before (with 15% w/v initial sugar) was used throughout the experiments. Ethanol production system with fully recycling of the used supernatants As shown on Figure 1, the proposed supernatants fully recycling system has two effluent streams: 1) The effluent stream of filtrated solid residuals mainly containing insoluble yeast cells and polysaccharides. Part of soluble oligosaccharides and inorganic salts ions accumulated, as well as organic acids formed during the repeated fed-batches, were also contained in those filtrated solid residuals. These filtrated residuals could be properly dried to remove water, and then used as useful feedstuff. 2) The evaporated product, ethanol with minor water and volatile organic byproducts, is the 2nd effluent stream of the system. As the filtrated supernatants could be cycled for reuse, wastewater effluents were completely eliminated, a complete closed-loop recycling ethanol production

4 1822 Fig. 2. Accumulation patterns of different inhibitory substances. Mark indicates the stage where the accumulation of the i-th inhibitory substance occurred and the relevant accumulation amount [ (g)] in each operation run, and P i refers to the supernatants across ratio (%) of the inhibitory substances. system was achieved. A total of 200 ml water, that is 2:15 (v/v, lost water/final broth volume of each fermentation run), lost in each operation run, and over 99% (w/w) of the total water loss occurred in Effluent Stream 1 (solid residues filtration). Same amount of fresh water needs to be supplemented to compensate the water loss. Mass balance model of the soluble inhibitory substances in the supernatants fully recycling system The solid yeast cells and non-fermentable polysaccharides produced in each fermentation run could be removed easily (near 100% w/w) by the filtration units. On the other hand, the soluble inhibitory substances (soluble organic acids, inorganic ions, and non-fermentable oligosaccharides) which accumulated in each run, either by the repeated nutrients feeding or by the continuous formation, could only be partially filtrated together with the solid substances. When the concentrations of the soluble inhibitory substances reached their critical inhibitory levels, they would stop the stable ethanol production (Converti et al. 1991). Thus, it is of interest to know whether those soluble substances could be maintained under certain equilibriums and non-inhibitory levels in the ethanol production system associated with fully recycling of the used supernatants. Figure 2 show the accumulation patterns of different inhibitory substances in the system, where three kinds of soluble inhibitory substances, organic byproducts, inorganic salt ions, and the non-fermentable oligosaccharides accumulated in different ways. Mark indicates the stage where the accumulation of the i-th inhibitory substance occurred and the relevant accumulation amount [ (g)] in each operation run, and P i refers to the supernatants across ratio (%, w/w) of the inhibitory substances. Here, the filtration unit represents the two filters shown on Figure 1. The mass balance of the i-th inhibitory substance in the system was based on the assumption of that, (g) andp i (%) in each operation run are constant, where P i can be expressed as P i = Amount of i-th Inhibitory Element in Filtrated Supernatant (g) Total Amount of i-th Element before Filtration (g).

5 1823 Fig. 3. Ratio of the concentrations of the i-th inhibitory substance at different repeated fed-batch cycles versus its equilibrium concentration under different supernatants across ratio P i (constant and V ) the simulation result using the model summarized in Table 1., P i = 82%;, P i = 70%;, P i = 90%. Fig. 4. The concentration of lactic acid at different repeated fed-batch cycles., Lactic acid. The above assumption is true for the repeated fedbatch fermentation cases as the initial and the final states (in terms of fermentation volume, feeding rate, time, concentrations of cells and ethanol, etc.) do not change much cycle by cycle. The mass balance model describing the change and accumulation pattern of the i-th inhibitory substance in each operation cycle is formulated in Table 1, where V represents the final working volume of each fed-batch run (1.5 l). As P i < 1, the concentration of the i-th inhibitory substance tends to reach an equilibrium level, and the accumulated and effluent amounts of the i-th inhibitory substance in each cycle tend to coincide with each other, when the repeated fed-batch cycle number n is approaching infinite ( ). As shown on Figure 3, under the condition of constant and V, the cycle numbers required for approaching the equilibrium level depend on supernatants across ratio P i, and the smaller the P i,the less cycle numbers for approaching the equilibrium are needed. P i largely depends on the characteristics of the filters septum, the filtrate, and the inhibitory substance itself. In general, P i for soluble inhibitors is reported relatively high and at about 82% (Chen 1999). The inhibitory substances are partially removed from the supernatants into the wet filtrated cake, mainly consisting of the solid non-fermentable polysaccharides and yeast cells. For example, if P i = 82%, it would take about 10 cycles to reach 90% of the equilibrium concentration (Figure 3). From the model described by Table 1, we can also see that the equilibrium concentration depends on the accumulation Fig. 5. The concentrations of the soluble inorganic ions at different repeated fed-batch cycles., K + ion;, Mg 2+ ion;, SO 2 4 ion;,h 2 PO 4 ion. amount in each cycle and the supernatants across ratio P i. The bigger the and P i, the higher equilibrium concentration could be reached. If no filtration action (P i 100%) is adopted, the soluble inhibitory substances would accumulated severely and the final concentrations could be very high without approaching an equilibrium. This coincides with the reported experimental results (Converti et al. 1991). Accumulation of the soluble inhibitory substances during the repeated fed-batch ethanol fermentation To see the accumulation of the inhibitory substances and its effect on the performance of the repeated fed-batch ethanol fermentation, the concentrations of organic by-products (the non-volatile lactic acid was considered here), the anions (H 2 PO 4 and SO2 4 ), the cations (K + and Mg 2+ ), and the soluble oligosacchar-

6 1824 Table 1. The change and accumulation patterns of the i-th inhibitory substance in different operation cycles. Cycle Concentration in Amount Amount drained out no. broth at the end of accumulated/produced at in effluent at the end each run (g l 1 ) the end of each run (g) of each run (g) The case of soluble organic by-products & inorganic salt ions 1 /V 0 2 S 1 (1 + P i )/V (1 P i ) 3 (1 + P i + Pi 2)/V (1 Pi 2) 1 P n S i n i (1 P i )V (1 P n 1 i ) N (1 P i )V The case of soluble unfermentable oligosaccharides 1 P i /V (1 P i ) 2 P i (1 + P i )/V (1 Pi 2) 3 P i (1 + P i + Pi 2)/V (1 Pi 3) 1 P n P i n i (1 P i )V N P i (1 P i )V (1 P n i ) ides at the end of each operation run were measured. Figure 4 shows that no severe accumulation of lactic acid occurred, and the lactate concentration could reach a low equilibrium level after about 5 operation cycles. Figure 5 shows that all ions approached their equilibrium concentrations but continued to increase very slowly after about 5 6 operation runs. No significant ion accumulation would occur provided that the necessary nutrients including the anions and cations were properly fed and assimilated (by yeast cells) during each operation run. As shown in Figure 6, the inhibitory oligosaccharides (tri-saccharides and tetra-saccharides) reached quickly and then remained at their equilibrium concentrations after about 3 operation runs. Lactic acid, H 2 PO 4, SO2 4, K+, Mg 2+ and the oligosaccharides are considered herewith as the typical soluble inhibitory substances in the closed-loop supernatants fully recycling system. The change and accumulation patterns of the other soluble inhibitors unmeasured should be similar to those of the substances measured. With the increase of recycle number, the concentrations of those unmeasured substances are also expected to reach and then remain at their equilibrium levels in the same ways as the substances measured did. In addition, it should be noted that as and Fig. 6. The concentrations of the soluble oligosaccharides at different repeated fed-batch cycles., Trisaccharides;, tetrasaccharides. P i could not actually be measured, the concentrations of those inhibitory substances could not be calculated from the model to compare with the measured values. However, the main purpose of formulating and using this model, is to estimate whether and how such a fermentation system could be operated for extremely long term, and actually the estimated results agreed with the experimental facts well.

7 1825 the amount of the hydrolyzed sugar utilized. The final ph at each run was stable at about 5.2, which is almost the optimum for both Saccharomyces cerevisiae Y002 growth and hydrolysis of the corn flours. Therefore, ph adjustment for hydrolysis and new medium preparation for the next run was not required, which greatly eased the operation. The unusual behavior of cycle no. 3 (Run 1) was due to a mistake in controlling the hydrolysis temperature, which caused the decreases in final ethanol concentration and production yield as well as an increase in residual sugar concentration. However, the fermentation recovered completely in the next operation run. This indicated that the closed-loop supernatants fully recycling system has good self-adapting and self-stable abilities to the outside disturbances. Conclusions Fig. 7. The concentrations of ethanol and glucose, ethanol production yield, and ph of the fermentation broth at the end of different repeated fed-batch cycles., Ethanol;, glucose;, ethanol production yield;, ph of the fermentation broth. Performance of the repeated fed-batch ethanol production system with fully recycling of the supernatants As the concentrations of all inhibitory substances were kept at the equilibriums which were considered below the corresponding inhibitory levels, a sustained ethanol production with high effluent ethanol concentration could continue for up to 30 cycles (75 d) without any decline in fermentation activities. As shown on Figure 7, the ethanol concentration, the ethanol production yield, the residual glucose concentration, and ph at the end of each operation run could be controlled stably at around 15% (v/v), 90%, 1% (w/v), and 5.2, respectively. An average ethanol productivity of 2 g l 1 h 1 could be obtained. Here, it should be noted that the ethanol production yield refers to the ratio of the actual ethanol yield to the theoretical ethanol yield (0.51 g ethanol/g glucose), which is based on the stoichiometry of the anaerobic ethanol fermentation C 6 H 12 O 6 2C 2 H 5 OH + 2CO 2 and The proposed repeated fed-batch system with fully recycling of the used supernatants for producing high concentration ethanol from corn flour is easy to operate, practical, and stable for an extremely long-term. As almost 100 percent of the aqueous effluent stream were recycled, it could ensure the minimum wastewater discharge and effectively reduce the treatment cost occurred in the downstream processes. Filtration of the insoluble yeast cells and polysaccharides ensured the complete removal of the solid inhibitors and partial removal of the soluble inhibitors, and it was indispensable in keeping the stability of the proposed system. With the soluble inhibitory substances being filtrated partially, the severe accumulation of those substances could be avoided and their concentrations be controlled at certain equilibrium levels successfully, which in turn maintained the extremely long-term stability of the production system. The proposed model could be used as a general tool, to estimate whether and how a fermentation system, such as the one associated with full utilization of the used medium, could be operated for an extremely long term. References Chen JX (1999) Closed-loop recycle technology in cleaner production. Wuxi Qinggong Daxue Xuebao 18: Converti A, Perego P, Lodi A, Fiorito G, Borghi MD, Ferraiolo G (1991) In-situ ethanol recovery and substrate recycling during continuous alcohol fermentation. Bioprocess Eng. 7: Hsiao TY, Glatz CE (1995) Water reuse in the L-lysine fermentation process. Biotechnol. Bioeng. 49:

8 1826 Hsiao TY, Glatz CE, Glatz BA (1994) Broth recycle in a yeast fermentation. Biotechnol. Bioeng. 44: Kim JS, Kim BG, Lee CH, Kim SW, Jee HS, Koh JH, Fane AG (1997) Development of clean technology in alcohol fermentation industry. J. Cleaner Prod. 5: Teramoto Y, Ueki T, Kimura K, Ueda S, Shiota S (1993) Semicontinuous ethanol fermentation with shochu distillery. J. Inst. Brew. 99:

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