Journal of the Taiwan Institute of Chemical Engineers 60 (2016) 119–123

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Journal of the Taiwan Institute of Chemical Engineers

journal homepage: www.elsevier.com/locate/jtice

Performance of fed-batch acetone–butanol–ethanol (ABE) fermentation

coupled with the integrated in situ extraction-gas stripping process and
the fractional condensation
Kuan-Ming Lu a, Yu-Sheng Chiang a, Yin-Rong Wang a, Rei-Yu Chein b, Si-Yu Li a,∗
a
Department of Chemical Engineering, National Chung Hsing University, Taichung 402, Taiwan
b
Department of Mechanical Engineering, National Chung Hsing University, Taichung 402, Taiwan

a r t i c l e i n f o a b s t r a c t

Article history: In this study, fed-batch acetone–butanol–ethanol (ABE) fermentation was coupled with the integrated in situ
Received 28 June 2015 extraction-gas stripping process. The total glucose consumptions were 255 and 310 g/L at the gas flow rates
Revised 19 October 2015
of 0.5 and 1.0 liter per minute (lpm), respectively. The ABE productivity and yield were 0.65 g/L/h and 0.43 g-
Accepted 26 October 2015
solvent/g-glucose at the gas flow rates of 0.5 lpm. When the gas flow rates increased from 0.5 to 1.0 lpm,
Available online 28 November 2015
the ABE productivity and yield became 0.69 g/L/h and 0.48 g-solvent/g-glucose, respectively. The fractional
Keywords: condensation was operated by using two different cold traps where temperatures for the first and second one
Clostridium acetobutylicum were 2 and −196°C, respectively. It was found that 71–81 and 64–73% of total stripped water was condensed
Fed-batch acetone–butanol–ethanol (ABE) in the 2 °C cold trap at gas flow rates of 0.5 and 1.0 lpm, respectively. Therefore, high ABE concentrations of
fermentation 360–460 g/L were found in the second cold trap. The overall separation factor for butanol was calculated to
Integrated extraction-gas stripping be up to 34 where the raffinate solution is the fermentation broth and the extract solution is the condensate
Fractional condensation
in the −196 °C cold trap.
© 2015 Taiwan Institute of Chemical Engineers. Published by Elsevier B.V. All rights reserved.

1. Introduction
Butanol is a carbon neutral, low polluting, and sustainable fuel
alternatives [1–3]. It can be fermentatively produced by acetone–
butanol–ethanol (ABE) fermentation where Clostridium species are
microbial catalysts that are responsible for it [4–6]. Batch, fed-batch,
and chemo-stat reactors are three common type processes for run-
ning ABE fermentation [7–11]. Among these methods, fed-batch fer-
mentation has attracted attentions because the continuous feeding of
fresh medium dilutes the butanol toxicity while provides more glu-
cose for fermentation [8,12]. Performance of fed-batch ABE fermen-
tation can be further enhanced by incorporating in situ product re-
moval (ISPR) technique, such as adsorption [13], pervaporation [14],
gas stripping [15], and liquid–liquid extraction [16,17].
A novel integrated extraction-gas stripping ISPR technique has
been developed in our previous study [18]. One advantage of the in-
tegrated in situ extraction-gas stripping process is that since butanol
in the oleyl alcohol (O.A.) phase is continuously removed by nitro-
gen stripping, only small amount of oleyl alcohol is needed without
the concern of butanol saturation during ABE fermentation. The other
advantage is that since butanol is stripped from the non-volatile O.A.
phase instead of aqueous fermentation broth, the selectivity toward
butanol during gas stripping is significantly elevated and has been
shown to be comparable to pervaporation [18]. This method can ef-
fectively improve performance of batch ABE fermentation where the
glucose consumption of 121 ± 2 g/L was achieved in a single batch
[18]. Accompanied with the high glucose consumption were the sig-
nificant increase in butanol productivity and yield by 112 and 56%,
respectively. In this study, fed-batch fermentation combined with
the integrated in situ extraction-gas stripping technique is developed
in this study and performance of this novel fed-batch fermentation
process is presented. Meanwhile, the fractional condensation is cou-
pled aiming to further elevate the purity of recovered butanol. During
which, separation factor and solvent removal rates were discussed in
this study.
2. Materials and methods
2.1. Bacterial strain and medium

C. acetobutylicum ATCC824 was used as the bacterial strain for fed-

batch ABE fermentation. The spore stock preparation, spore germina-
∗
Corresponding author. Tel.: +886 42284 0510x509. tion, and pre-culture preparation were conducted as previously de-
E-mail address: syli@dragon.nchu.edu.tw (S.-Y. Li). scribed [11].

http://dx.doi.org/10.1016/j.jtice.2015.10.044
1876-1070/© 2015 Taiwan Institute of Chemical Engineers. Published by Elsevier B.V. All rights reserved.
120 K.-M. Lu et al. / Journal of the Taiwan Institute of Chemical Engineers 60 (2016) 119–123
Fig. 1. Schematic of integrated in situ extraction-gas stripping process for fed-batch ABE fermentation. The implementation of the fractional condensation is presented.
2.2. Fed-batch ABE fermentation with the integrated in situ
extraction-gas stripping process and the fractional condensation
Fed-batch ABE fermentation was achieved by firstly aseptically
transferring 9 mL of C. acetobutylicum pre-culture solution to 300 mL
of fresh Luria Broth (LB) medium containing 80 g/L glucose, 0.008 g/L
CaCl2 , 0.1 g/L FeSO4 ·7H2 O, and 0.6 g/L MgSO4 ·7H2 O. A 500 mL serum
bottle was used as a reactor for ABE fermentation. 40 mL fresh Luria
Broth containing 600 g/L glucose, 0.008 g/L CaCl2 , 0.1 g/L FeSO4 ·7H2 O,
and 0.6 g/L MgSO4 ·7H2 O were fed into the reactor when the glucose
concentration was below 10 g/L. Fermentation was conducted in a
rotary shaker at 37 °C and 150 rpm.
The schematic of fed-batch ABE fermentation coupled with the in-
tegrated in situ extraction-gas stripping process was shown in Fig. 1.
The 500 mL serum bottle held 300 mL of fresh medium and 100 mL
of oleyl alcohol (80 –85%, Alfa Aesar® ). Gas stripping of butanol was
initiated at the fermentation time of 48 h. The nitrogen gas from the
cylinder was delivered at a flow rate of 0.5 or 1.0 liter per minute
(lpm) into the O.A. layer for butanol gas stripping where the nitrogen
gas was sterilized using a 0.2 μm syringe filter (Millipore). The bub-
bling of nitrogen gas was achieved through a single 18-G syringe nee-
dle. Upon the initiation of gas stripping, the rotary speed decreased
from 150 to 100 rpm.
As shown in Fig. 1, the fractional condensation was achieved by
using two cold traps in series. The first cold trap was maintained at
2 °C (50% water and 50% ethylene glycol) and the second cold trap
was maintained at −196 °C with liquid nitrogen. The sampling of the
condensate was on the 24 h basis.
Fig. 2. Profile of the biomass and glucose concentration of fed-batch ABE fermentation with the gas stripping rate of (a) 0.5 lpm, (b)1.0 lpm.
2.3. Analytical methods
The biomass concentration and the glucose concentration were
respectively determined by the spectrophotometry and the dinitros-
alicylic acid (DNS) method as described earlier [19]. The concentra-
tions of acetone, butanol, ethanol, acetate, and butyrate were quanti-
fied by gas chromatography (GC) (Hewlett Packard HP 5890 Series II)
as described earlier [19].
3. Results and discussion
3.1. Performance of fed-batch ABE fermentation coupled with the
integrated in situ extraction-gas stripping process
Performance of fed-batch ABE fermentation coupled with the in-
tegrated in situ extraction-gas stripping process has been conducted
where flow rates of 0.5 and 1.0 lpm were tested. It can be seen in
Fig. 2a that when the gas flow rate of 0.5 lpm was applied in the ex-
traction phase, the biomass concentration reached above 25 g/L and
whole fed-batch fermentation time reached 168 h with the total glu-
cose consumption of 255 g/L. The profile of the biomass and glucose
concentrations reflects a fact that the prolonged fermentation results
from the relief of butanol toxicity. Furthermore, since each supple-
ment of fresh medium was achieved with 13% dilution rate, the fed-
batch mode itself has little contribution to the dilution of butanol.
It is therefore concluded that the relief of butanol toxicity is mainly
achieved by the effective function of the integrated in situ extraction-
gas stripping process. Fig. 2b showed that when the gas flow rate was
 K.-M. Lu et al. / Journal of the Taiwan Institute of Chemical Engineers 60 (2016) 119–123
Fig. 3. Ratio of the butanol concentration in the O.A. phase to that in the aqueous
phase. The enclosed region between 3.2 and 4.3 represents the typical partition coeffi-
cient of butanol in O.A. and aqueous phases.
elevated from 0.5 lpm to 1.0 lpm, the total glucose consumption fur-
ther improved. The total glucose consumption increased from 255 to
310 g/L and the total fermentation time increased to 216 h. It is be-
lieved that the improved glucose consumption can be attributed to a
faster butanol removal rate when the gas flow rate is increased from
0.5 to 1.0 lpm.
3.2. Performance of in situ butanol extraction
The efficiency of butanol extraction can be evaluated by calculat-
ing the ratio of the butanol concentration in the O.A. phase to that in
the aqueous phase, see Fig. 3. It can be seen that when butanol was
produced after 40 h, the ratio rose up consistently and then fluctuated
in a range between 3.0 and 5.0 till the end of fed-batch ABE fermenta-
tion (at 0.5 lpm). Since the partition coefficient of butanol in the O.A.
and water phases has been reported to be 3.2 –4.3 (see [18] for dis-
cussion), it can be concluded that the butanol partitioning between
the aqueous and the O.A. phases was at near-equilibrium. Note that
profile of the butanol concentrations in the aqueous and O.A. phases
throughout fed-batch ABE fermentation were presented in Fig. S1.
Also noted is that the mass transfer of butanol during extraction oc-
curred in the interface of two layers where the shaking of the reactor
at 100 rpm resulted in a swaying interface. This trend remained valid
when the gas flow rate increased to 1.0 lpm. Note that at flow rate of
1.0 lpm, the ratio went below 3 after 168 h. This may be attributed to
the cell debris that causes the noticeable mass transfer resistance for
butanol extraction. Given the similar ratio of butanol partition at flow
rates of 0.5 and 1.0 lpm, two conclusions can be made from the result
of lower butanol concentrations in both aqueous and O.A. phases at
the flow rate of 1.0 lpm. First, the butanol toxicity can be effectively
tackled by increasing the gas flow rate where butanol is removed out
Fig. 4. Performance of the fractional condensation. The solvent concentration in the condensate of (a) the first cold trap at 2 °C and (b) the second cold trap at −196 °C when the
gas stripping flow rate of 0.5 lpm was applied. Gas stripping was initiated at fermentation time of 48 h.
121
of the reactor with a faster rate. This indicates the effectiveness of
the integrated in situ extraction-gas stripping process. Second, while
the butanol stripping rate is significantly increased, the relatively in-
significant difference in ratios of butanol partition between flow rates
of 0.5 and 1.0 lpm indicates that the extraction is not the rate limiting
step in the regime developed in this study. This is consistent with our
previous study [18].
Oleyl alcohol is known for its low selectivity towards acetone
and ethanol as previously reported in our study and others [18,20]
and this happens to other biocompatible extracting solvents such as
mesitylene or glyceryl tributyrate. The accumulation of acetone and
ethanol in the fermentation broth is not as detrimental as that of bu-
tanol does. Besides, the separation of acetone and ethanol from the
fermentation broth is much easier. On the other hand, up to 88% of
total produced butanol was removed during fed-batch ABE fermenta-
tion by the integrated in situ extraction-gas stripping process (given
the total glucose consumption, butanol yield, and butanol concen-
tration in the fermentation broth). The efficient butanol removal re-
sults in high performance ABE fermentation. In the perspective of
downstream purification process for obtaining high purity solvents
for commercial sale, the fermentation beer along with the purified
butanol solution in the other side of the integrated in situ extraction-
gas stripping process can be subject to a novel distillation processes
proposed by Kraemer et al. [16]. Though the complexity is added to
fermentation process when the integrated in situ extraction-gas strip-
ping process is coupled, it could be paid off by high performance ABE
fermentation while 88% butanol is simultaneously recovered in a high
purity.
3.3. Performance of gas stripping coupled with the fractional
condensation for butanol separation
To further improve the solvent purity in the condensate, the frac-
tional condensation was introduced in this study where tempera-
tures of the first and second traps were controlled at 2 and −196°C,
respectively. It can be seen in Fig. 4a and b that when the gas flow
rate of 0.5 lpm was applied, the ABE and butanol concentrations in
the first condensate were 37 –42 and 29–32 g/L in the fermenta-
tion time span of 48 to168 h. The ABE and butanol concentrations
in the second condensate were 360 –460 and 200–250 g/L, respec-
tively. Similar trends for the solvent purities in the first and second
condensates were observed when the gas flow rate increased to from
0.5 to 1.0 lpm, see Figs. S2a and S2b.
It can be seen in Figs. S3a and S3b that while the total butanol re-
moval rate was 0.07 –0.12 g-butanol/h, butanol removal rates for the
first and second cold trap were 0.02 and 0.05 –0.11 g-butanol/h, re-
spectively. Given the butanol removal rates for each cold trap, it can
122 K.-M. Lu et al. / Journal of the Taiwan Institute of Chemical Engineers 60 (2016) 119–123

Table 1
Performance of fed-batch ABE fermentation coupled with the integrated in situ extraction-gas stripping process and the fractional condensation.

Total glucose Normalized butanol

Flow rate consumption Fermentation removal ratea Overall separation
(lpm) (g/L) time (h) Titer (g/L) Productivity (g/L/h) Yield (g/g-glucose) (g/L/h) factor for butanolb

Butanol ABE Butanol ABE Butanol ABE

0.5 255 168 63.8 109.4 0.38 0.65 0.25 0.43 0.23–0.40 28–34
1.0 310 216 82.2 148.1 0.38 0.69 0.27 0.48 0.23–0.53 27–33
a
:The normalized butanol removal rate is defined as the normalization of overall butanol removal rate by the volume of the fermentation broth of 0.3 L.
b
:The overall separation factor for butanol is calculated where the raffinate solution is the fermentation broth and the extract solution is the condensate in the −196°C
cold trap.

where x is the weight fraction of butanol in the raffinate solution and

Fig. 5. Separation factor for butanol during the extraction, fractional condensation,
and overall processes using the gas flow rate of 0.5 lpm. The overall separation factor
is calculated using the fermentation broth and the −196°C condensate as the raffinate
and the extract solutions, respectively. Gas stripping was initiated at fermentation time
of 48 h.
be calculated that up to 83% of total butanol stripped off from the O.A.
phase was accumulated in the second condensate. At the same time,
when the gas flow rate of 1.0 lpm was applied, an arguably higher
percentage of up to 88% of total stripped butanol was found in the
second condensate. Together with water removal rates in the first and
second condensates (data not shown), it can be calculated that 71 –
81 and 64–73% of total stripped water was condensed in the 2 °C cold
trap at gas flow rates of 0.5 and 1.0 lpm, respectively. This presum-
ably indicates that butanol is much easily dissolved in nitrogen gas
than water does, especially volatile solvents of acetone and ethanol
in the nitrogen gas stream may help the dissolution of butanol in the
nitrogen gas. Therefore butanol can be readily brought to the second
cold trap by the flow of nitrogen gas. Total ABE removal rates (at both
0.5 and 1.0 lpm) for the first and second condensates were shown in
Figs. S3c and S3d.
The fractional condensation has been widely used in the separa-
tion of gas mixture while achieving gas liquefaction. Since it is effi-
cient and competitive, numerous patents have been issued relating
this technique. Meanwhile, the fractional condensation has been ap-
plied for the recovery of biomass pyrolysis vapors [21]. In our pre-
vious study, performance of the integrated extraction-gas stripping
process has provided one of record-high solvent purities where the
ABE and butanol concentrations in the condensate were 166–204 and
93–113 g/L, respectively [18]. In this study, the coupling of the 2 °C
cold trap, which exhibits efficient ability for trapping water, further
promotes the final ABE and butanol concentrations around two folds.
The separation efficiency of the integrated extraction-gas strip-
ping process as well as the fractional condensation has also been eval-
uated by the separation factor for butanol. The separation factor for
butanol is defined as follows:
x/(1 − x)
Separation factor =
y/(1 − y)
y is the weight fraction of butanol in the extract solution. The defi-
nition of the separation factor applies to three separation stages in-
cluding the extraction, 2 °C condensation, and −196 °C condensation.
The overall separation factor is calculated where the raffinate solu-
tion is the fermentation broth and the extract solution is the con-
densate in the −196 °C cold trap. It can be seen in Fig. 5 that the
separation factor for the extraction process was in the range of 4.1–
5.0 at the gas flow rate of 0.5 lpm. When the gas flow rate increased
from 0.5 to 1.0 lpm, the separation factor decreased to a range of 2.4
–4.1 (Fig. S4). The noticeable decrease in the separation factor at the
gas flow rate of 1.0 is simply results from the enhanced butanol re-
moval from the O.A. phase and thus the butanol concentration in
the O.A. phase deviated from the equilibrium. Nevertheless, as dis-
cussed in Section 3.2, the extraction was not the rate limiting step
for butanol separation at both gas flow rates. The separation factors
for the 2 °C condensation were in the ranges of 0.7–1.0 and 0.9–1.6
at the flow rates of 0.5 and 1.0 lpm, respectively. The separation fac-
tor of 6.4–9.8 for the −196 °C condensation represented that the bu-
tanol concentrations in the extract solution were in the range of 150
–250 g/L. The overall separation factor for the integrated extraction-
gas stripping process coupled with the fractional condensation was
steadily maintained above 28 and could reach up to 34. Separation
performance of the integrated extraction-gas stripping ISPR tech-
nique coupled with the fractional condensation is superior to the ex-
traction (0.6–2.4) [17] and gas stripping (10–22) [[22], [23]], and is
comparable to pervaporative butanol separation [[24], [25]]. Table S1
summarized performance of the fractional condensation for butanol
separation.
Performance of fed-batch ABE fermentation coupled with the in-
tegrated in situ extraction-gas stripping process and the fractional
condensation was summarized in Table 1. Compared to our pre-
vious study where batch reactor was coupled with the integrated
extraction-gas stripping process, it was found that the butanol and
ABE productivities increased respectively from 0.28 and 0.46 to 0.38
and 0.69 g/L/h. The butanol and ABE yields increased respectively
from 0.23 and 0.37 to 0.27 and 0.48 g/g-glucose.
4. Conclusions
The integrated in situ extraction-gas stripping process has been
shown to be an effective ISPR technique for fed-batch ABE fermenta-
tion. Exceptional performance of fed-batch ABE fermentation is con-
cluded in terms of the solvent productivity and yield. While the inte-
grated in situ extraction-gas stripping process provides a high solvent
removal rate, the coupling of the fractional condensation produces
high ABE concentrations of 360–460 g/L in final products. The inte-
grated in situ extraction-gas stripping process has been demonstrated
to be an effective ISPR for fed-batch ABE fermentation. By this simple,
efficient, and easily-maintained in situ separation process, one of the
highest solvent productivity and solvent purity for fed-batch ABE fer-
mentation are reported.
 K.-M. Lu et al. / Journal of the Taiwan Institute of Chemical Engineers 60 (2016) 119–123 123

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