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Immobilisation of microbial cells for fermentation has
been developed to eliminate inhibition caused by high
concentration of substrate and product, also to uncouple the
hydraulic retention time and the cellular retention time.
Immobilisation of cells to a solid matrix is an alternative
means of high biomass retention. Alginate is widely used in
food, pharmaceutical; textile and paper products. The use of
alginate is for thickening, stabilising, gel and film forming [6].Recent works on ethanol production in an immobilised cell
reactor showed that production of ethanol using Zymomonas
mobilis and S. cerevisiae was increased significantly [13,14].
The Qp can be also improved by increasing the concentra-
tion of viable biomass in the reactor. In this approach many
researches studied cultures at high cell density. The best
performance was obtained using continuous systems with cell
recycling [15e17]. Membrane filtration is most frequently used
to increase the concentration of viable biomass in the reactor.
We musttake intoaccount the characteristics of the membrane
(material, porosity, size and number of pores, charge of
surface), the nature and composition of species present in the
solution and the operating conditions (applied pressure, thesolution concentration, temperature, pH and ionic strength).
The aim of this work was to study the alcoholic fermen-
tation of sugar cane molasses by using CSTR, ICR and MBR
technologies. In order to findthe better alternative with higher
ethanol productivity, the reactors performances were inves-
tigated at different loading rates.
2. Materials and methods
2.1. Yeasts and molasses sources
Sugarcane (Saccharum officinarum) cultivars employed in thiswork were harvested in the central province of Santiago
(Cuba) on 2008. Molasses, from which fermentation medium
were prepared, were obtained from the STS Company of
Tunis. They have the following composition: dry matter
(72.2%), total sugars (48.5%), ash content (6.7%) and pH of 7.9.
The feedstock solution was boiled for 5 min, centrifuged and
filtered for pre-treatment and clarification. In the clarification
step, a part of the coloured material and unknown toxic
substances frequently included in the molasses were sepa-
rated or inactivated and the molasses were diluted with
distilled water to give a total sugar concentration of 100 g L1.
pH was adjusted to 5 with 10% sulphuric acid concentration.
Medium used for bioreactors feeding consisted of yeastextract (10 g L1), peptone (5 g L1), NH4Cl (2 g L1), KH2PO4,
MgSO4 H2O (0.5 g L1), sugars (100 g L1) and 200 mg L1Na-
thioglyconate as the reducing agent at pH 5 [18]. The culture
medium was sterilized at 121 C for 15 min. The initial
oxidation reduction potential (ORP) of the medium was nearly
250 mV indicating the anaerobic conditions.
The different fermentations have been achieved using
fresh commercial baker’s yeast S. cerevisiae (Tunisian Society
of Yeasts). The yeast strain viability was determined using
methylene blue staining technique. It was cultivated using an
incubator shaker under sterile conditions at pH 5, 30 C and
150 revolutions min1. Pure cultures grown under anaerobic
conditions were used forinoculation of experimentalreactors.
2.2. Laboratory reactors configurations and operating
conditions
Three types of reactors were used to carry out the continuous
fermentation at 30 C (CSTR: Fig. 1, ICR: Fig. 2 and MBR: Fig. 3).
The fermentation in the CSTR was conducted in a 1 L Bio-
lafit fermentor using a pre-culture of 200 mL seeded in
a medium with a sugar concentration of 50 g L1. An aeratedbatch phase for 48 h was provided to produce a sufficient
concentration of biomass of 18 g L1. At the end of the batch
phase, the continuous culture was conducted in anaerobic
conditions to ensure the fermentation. The CSTR was fed with
a sugar concentration of 100 g L1. Different dilution rates
were tested. A D of 0.12 h1 (run 1) was applied during the first
246 h of monitoring, a D of 0.25 h1 (run 2) was applied from
time 246 h to time 415 h and a D of 0.5 h1 (run 3) was applied
during the last 85 h of work.
The fermentation set-up of the ICR was comprised of
a Biorad column packed with beads of immobilised cells. The
immobilisation of S. cerevisiae was performed by the enriched
cells cultured media harvested at the exponential growthphase. The fixed cell loaded ICR was carried out at initial stage
of operation and the cell were entrapped by calcium alginate
(2%) [6,8]. The fermentation in the ICR has been done over
a period of 225 h. Ds were adapted to 0.12, 0.25 and 0.5 h 1,
respectively.
The MBR system (YUASA Membrane Systems: ED-03SPH) is
composed of two reactors: the fermentation tank and
a membrane tank (1 L each) maintained in anaerobic condi-
tions. A recirculation of flux was maintained between the
fermentation tank and the membrane tank with a high flow
rate to maintain similar conditions in both tanks in terms of
mixed liquor total suspended solids. Then, the dilution rate
was calculated using the 2 L total volume of the fermentor andthe membrane unit. The filtrationunit consisted of an external
filtration module with a nominal cut-off filter of 0.4 mm and
a filtration surface of 0.014 m2. The maximum allowable
pressuredropoverthefilterwas4bars.Thestart-upoftheMBR
culture wasprovidedfrom theoutletof theCSTR with an initial
biomass concentration of 8 g L1 and a pH of 4.8. The
fermentation tank was loaded with an initial sugar concen-
tration of 100 g L1. The system was operated 245 h without
cleaning resulting in a membrane flux of 21.4e35.7 L h1 m1.
There has been a decrease in the permeate flow over time
Feed Tank Pump Fermenter Pump
CO2
Product Tank
Fig. 1 e Schematic of the laboratory scale continuously
stirred tank reactor.
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which corresponded to the membrane fouling. Consequently
thedilutionrate initiallyset at0.5 h1 fallduringthefirst90hof
working to stabiliseat 0.31 h1. Allthe experiments occurred in
triplicate and the relative standard deviations among the
results did not exceed 5%.
2.3. Technical analysis
Kinetic of fermentations was monitored by measuring the
concentration of biomass, total reduced sugars (TRS) and
ethanol during the time. The samples were centrifuged
(10,000 g) and the biomass concentration wasdetermined by
measuring the optic density (OD) of diluted sample at 600 nm
using a standard curve of absorbance against dry cell mass
(TSS: total suspended solids). The TRS concentration was
measured by using the phenol acid method [19]. The samples
were analysed in triplicates and results were reproducible. pH
and ORP were measured using a pH metre (WTW).
Ethanol production was analysed by high performance
liquid chromatography on an Agilent Model 1200 series
liquid chromatograph equipped with four solvent pumps,a programmable multi-wavelength detector and a data
module. The mobile phase was 1 mol m3 H2SO4. Aliquots of
20 mL were injected into a silica column (ZORBAX C18)
(150 mm 3.9 mm) at ambient temperature. The flow rate of
the mobile phase was 0.3mL min1 and the analysis was done
under isocratic mode (no composition change of the solvent).
Quantification of ethanol was done by using standard ethanol.
Samples were diluted with ultra pure water and filtered with
millipore membranes (0.22 mm pore size).
2.4. Statistical analysis
In order to determine whether the observed differences
between reactors performances were significantly different,
data were subjected to the analysis of variance by ANOVA
tests ( p < 0.05) [20].
3. Results and discussion
3.1. Performances of the CSTR
The alcoholic fermentation provided in the CSTR has been
achieved by varying the D from 0.12 h1 to 0.5 h1.
Fig. 4 shows the variation of total sugar and ethanolconcentrations. During the first run (D ¼ 0.12 h1) the
concentration of residual sugar was stabilised at an average
value of 18.3 g L1 equal to a substrate conversion yield (Ys) of
81.7%. This condition permitted to succeed to an average
ethanol concentration of 27.9 g L1 and a yield ethanol for
substrate (YP/S) of 0.34 g g 1. Average Qp of 3.34 g L1 h1 has
been determined.
Feed Tank Pump
Valve
Pump
Valve
Product Tank
I m m o b i l i s e d C e l l R e a
c t o r
Fig. 2 e Schematic of the laboratory scale immobilised cell
reactor.
Circulation
Tank
Feed Tank Feed Pump Fermenter Circulation
PumpCirculation
Pump Membrane
Permeate Tank
(Permeate)(Concentration)
P
P
CO2
(V)
(V)
(V)(V)
Fig. 3 e
Schematic of the laboratory scale membrane bioreactor (P [ pressure measurement and V [ valve).
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In the second run, the increase of the D to 0.25 h1 caused
a disruption of the system balance which resulted in a signif-
icant drop in the residual sugar concentration, accompanied
by an increase in the alcohol concentration. The important
input of substrate excited the fermentation metabolism of
cells to produce high quantity of ethanol which reached
a maximum concentration of 40.9 g L1. This result showed
the coupling between biomass and ethanol productionsbecause the biomass concentration has risen in this phase to
reach a maximum value of 9 g L1. At the end of this run
ethanol and residual sugar concentrations were stabilised at
an average values of 21.6 g L1 and 31.1 g L1, respectively,
equal to a Ys yield of 68.9%. The YP/S yield decreased to
0.31 g g 1 and the Qp increased to 5.4 g L1 h1 by the appli-
cationofa D of0.25h1. In fact,the Qp depends on the ethanol
concentration and the dilution rate that has been increased.
The highest Qpof 6.8 g L1 h1 for theCSTRwas observedat
a D of 0.5 h1 (run 3). Applying a high D caused a progressive
decrease in the concentration of ethanol to achieve an average
value of 11.6 g L1, accompanied by an increase in the
concentration of TRSs (51.5 g L1). Then, the Ys fell to 48.5%corresponding to an YP/S of 0.24 g g 1. At high D, the assimi-
lation declined and a significant part of sugars was washed
out. This result showed that cells fail to produce high quantity
of ethanol at high D due to the wash out of cells at high flow
rate. The same Qp in order of 5.98 g L1 h1 with a high YP/S
yield of 0.47 g g 1 were obtained by Purwadi and Taherzadeh
[9] in a continuous fermentation of glucose by applying
a dilution ratio of 0.86 h1. However, using hydrolysed ligno-
celluloses wood after an acid pre-treatment has led to a high
Qp in the order of 20 g L1 h1 by conducting a continuous
fermentation reactor in a volume equal to 0.45 L, with a D of 0.3 h1 [21].
At run 1 (D ¼ 0.12 h1), the biomass concentration dropped
considerably from 18 g L1 to 4.8 g L1 after passing through
fluctuations (Fig. 4). This decrease corresponds to a transi-
tional state of cells adaptation characterised by a very
important wash out of cells out side the reactor. The stabili-
sation of biomass concentration was reached after 75 h of
operation of the system. The increase in the D from 0.12 to
0.25 h1 caused an acceleration of cell multiplication to ach-
ieve a biomass concentration of 9 g L1, followed by a fall, then
stabilised. The fall of the biomass concentration was caused
by the important flow rate that created a significant wash out
of cells. After 108 h of operation under this condition thebiomass stabilised and reached steady state at a concentra-
tion of 4.9 g L1. The second change of the D (run3) led to
a further reduction in the biomass concentration to be
0
2
4
6
8
10
12
14
16
18
20
0 50 100 150 200 250 300 350 400 450 500
Time (h)
B i o m a s s c o n c e n t r a
t i o n
( g L - 1 )
0
0,5
1
1,5
2
2,5
3
3,5
4
4,5
5
5,5
6
p H
a n d D
( h - 1 )
0
10
20
30
40
50
60
0 50 100 150 200 250 300 350 400 450 500
Time (h)
T R S a n d e t h a n
o l c o n c e n t r a t i o n s
( g
L - 1 )
0
0,1
0,2
0,3
0,4
0,5
0,6
D
( h - 1 )
a
b
Fig. 4 e Evolution of (a): total reducing sugar (TRS) ( > ), ethanol ( B ), (b): biomass ( > ) and pH ( B ) during CSTR fermentation of
sugar cane molasses under different Ds ( D ).
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2.4 g L1. The application of a high D of 0.5 h1 caused
a significant wash out of cells. The continuous increase of the
D to a value exceeding the maximum specific growth rate
(mmax) induced the phenomenon of leaching. In these condi-
tions growth does not compensate the biomass washed out
due to the increase of the flow rate. However, if the out flow of
biomass exceeds the growth yield of yeasts, the continuous
cultivation fails and the biomass is washed out. Taherzedehet al. [22] showed that the continuous fermentation of
a fermentable hydrolysate by yeast can be successful at a D of
0.1 h1, but fails at a D of 0.2 h1 or higher.
The initial pH of feed was regulated to 5.5 by adding
a diluted sulphuric acid. Fig. 4 showed that the pH decreased
slightly during the fermentation and stabilised around values
of 4.6e5. This slight decrease can be explained by the CO 2
production during the fermentation and the accumulation of
ions HCO
3 which represent the soluble form of CO2. It can be
also explained by the production of metabolites other than
ethanol (acetate, succinic acid, etc.) by the yeast during the
fermentation. S. cerevisiae have been reported to increase
ethanol production at pH 5.0 and 5.5 as opposed to pH 4.0 and4.5 and its optimum pH is from 5.0 to 5.2 [23].
3.2. Performances of the ICR
The ICR fermentation monitoring has been done over a period
of 225 h. The applied Ds were adapted to 0.12, 0.25 and 0.5 h1.
The results of the different runs are presented in Fig. 5 which
showed that the production of ethanol was steady after 18 h of
operation and maximum concentration of ethanol was
reachedduring the first 115 h of the fermentation. The average
concentration of ethanol during the stationary phase was
44.1 g L1. In fact, Qp reached during this D was 5.28 g L1 h1.
The concentration of ethanol was affected by the mediaflow rates and the residence time distribution. Following
a first increase in the D from 0.12 h1 to 0.25 h1 after 115 h of
fermentation, a reduction in the ethanol concentration was
observed and the Qp increased significantly (P < 0.05). Indeed,
with the increase of the D, yeasts fail to completely consume
sugar in the culture medium. Therefore the YP/S yield reduced
and the concentration of residual sugars become more
important (9.6 g L1). The decrease in the concentration of
ethanol could be caused by the combined effect of increasing
the medium flow rate and the loss of cell viability over time.
The maximum Qp of 10.1 g L1 h1 was obtained with a D of
0.5 h1. Goksungur and Zorlu [24] achieved a Qp very close
(10.16 g L1 h1) to that of our work by applying a D of 0.22 h1.While, Baptista et al. [8] achieved a higher Qp of 16 g L1 h1
with a D of 0.4 h1, with the same type of bioreactor but using
cells of S. cerevisiae immobilized on polyurethane cubes.
Monitoring of pH during this fermentation showed
a decrease of values from 5.5 to 4.3e5.3.This decrease was due
to the increase of dissolved CO2 in the reactor as mentioned
previously. The dissolved CO2 in the solution reacts with
water to form carbonate ions and proton Hþ. According to the
literature, the intracellular pH varies slightly for an extracel-
lular pH ranging between 4 and 7. In this range of pH, cell
viability can not be affected by the pH because its value
remained constant and greater than 4 [23].
3.3. Performances of the MBR
Fig. 6 shows a very important increase in the concentration of
biomass in the MBR from an initial value of 8 g L1 to a final
value of 41.1 g L1 after 245 h of work. This increase in the
biomass concentration was accompanied with a gradual
decrease in the permeate flux due to the membrane fouling.
The concentration of biomass at the outlet of the MBR was
very low; it is equal to 0.05 g L1. This result confirms the
proper functioning of the membrane system that can retain
all the cells inside the bioreactor. pH within and in the outlet
of the bioreactor were the same which showed that the
membrane system does not affect the pH.Fig. 6 shows an almost consumption of total sugars. The Ys
yield was close to 97.7e99.3% with a residual concentration
lower than2.5g L1. The consumed sugar was headed towards
the growth of yeasts resulting in a very important activity
and ethanol production with average concentrations of
0
10
20
30
40
50
60
0 25 50 75 100 125 150 175 200 225
Time (h)
s n o i t a r t n e
c n o c l o n a h t e d n a
S R T
( g L - 1 )
0
0,5
1
1,5
2
2,5
3
3,5
4
4,5
5
5,5
6
D
( h - 1 ) a n d p H
Fig. 5 e Evolution of total reducing sugar (TRS) ( > ), ethanol ( , ) concentrations and pH ( D ) during ICR fermentation of sugar
cane molasses under different Ds ( B ).
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41.4e46.5 g L1. The high consumption of sugars and
production of ethanol are independent to the loading flow
rate. They are the result of the high concentration of biomass
in the bioreactor, which provided an important YP/S with
a constant rate, even during the change of flow. The stabili-sation of biomass concentration in the MBR can be explained
by the fact that the high concentration of ethanol becomes
a limiting factor for the multiplication of cells and induced the
yeast metabolism for the alcoholic fermentation.
During the MBR system monitoring results showed two
phases characterised by two levels of Qp. The first Qp corre-
sponds to a D of 0.31e0.5 h1 during the first 90 h which was
about 12.83e19.2 g/L h. The second phase was characterised
by a Qp of 14.4 g L1 h1 which corresponds to a D of 0.31 h1.
After the membrane fouling, the Qp decreased significantly
( p < 0.05). The decrease of the Qp can be avoided by studying
the membrane behaviour during the operation to learn the
moment when it must be regenerated by flow reversal or
chemical cleaning.
The intensification of ethanol production from hydrolysed
wood in a membrane bioreactor was studied by Lee et al. [15].
They obtained a similar Qp of 16.9 g L1 h1 with ethanol
concentration of 76.9 g L1 and a YP/S of 0.43 g g 1. However,higher Qp has been also obtained byBen Chaabene et al. [17] in
a two stage MBR. They mentioned an important Qp in the
order of 41 g L1 h1 and an ethanol concentration of 80 g L1.
Escobar et al. [25] have implemented a membrane bioreactor
of 7000 L. They obtained a Qp of 3.4 g L1 h1 with ethanol
concentrations ranged between 80 and 90 g L1. However, the
authors mentioned some problems of membrane fouling with
biomass concentrations above 100 g L1. They also observed
a drop in the cell viability due to the stress caused by the
pump.
3.4. Comparison of reactors performances
A comparison between performances of bioreactors used for
the ethanol production has been made.
Table 1 summarizes the results obtained with different
configurations of reactors. The average ethanol concentra-
tions decreased by increasing the D however, productivities
increased. The Qp depends not only to the ethanol concen-
tration but also to the D hence the interest in working with
high D exceeding the mmax. This was achievable only by
working with the MBR which provided high cell densities
within the reactor.
Data showed that ethanol concentration and Qp during the
fermentation of sugar cane molasses in the ICR are higher
than those obtained with the CSTR. In addition, YP/S yields aremore important in the ICR. This was mainly caused by the
immobilisation of cells in the reactor which slowed cell
proliferation and promotes the metabolism to the alcoholic
fermentation. Subsequently, yeasts consumed the substrate
in advantage to produce ethanol.
The fermentation of molasses through the MBR bioreactor
improved the Qp, the concentration of ethanol and the YP/S
yield. In fact, Qp achieved in this reactor was three times
higher than that in the CSTR and it was two times higher than
that in the ICR. The Ys yield showed very high levels
0
5
10
15
20
25
30
35
40
45
0 30 60 90 120 150 180 210 240
Time (h)
B i o m
a s s c o n c e n t r a t i o n ( g L - 1 )
a n d
p e r m e a t e f l u x ( L h - 1 m
- 2 )
0
10
20
30
40
50
60
0 30 60 90 120 150 180 210 240
Time (h)
E t h a n o l c o n c e n t r a t i o n ( g L - 1 )
0
1
2
3
4
5
6
7
8
p H
a n d T R S ( g L - 1 )
a
b
Fig. 6 e Evolution of (a): biomass concentration ( > ),
permeate flux rate ( , ), (b): total reducing sugar (TRS) ( > ),
ethanol concentrations ( D ) and pH ( , ) during MBR
fermentation of sugar cane molasses.
Table 1 e Performances of the CSTR, ICR and MBR bioreactors used for the ethanol production at different dilution rates.
Reactors CSTR ICR MBR P
Run 1 Run 2 Run 3 Run 1 Run 2 Run 3 Run 1 Run2
Dilution rate D (h1) 0.12 0.25 0.5 0.12 0.25 0.5 0.31e0.5 0.31 e
Ethanol concentration (g L1) 27.9 1.9 21.6 1.9 11.6 1.6 44.06 1.9 32 1.1 20.2 0.6 41.4 1.8 46.5 1.5 0.0032
Productivity: Qp (g L1 h1) 3.34 0.2 5.4 0.3 6.8 0.3 5.28 0.2 8.0 0.4 10.1 0.6 12.83e19.2 14.41 0.6 0.0061
Substrate inlet (g L1) 100 100 100 100 100 100 100 100
Substrate outlet (g L1) 18.3 1.7 31.1 2.9 51.5 1.2 2.9 0.4 9.6 0.6 26.8 1 2.3 0.2 0.7 0.1 0.004
Sugar consumption: Ys (%) 81.7 2.1 68.9 2.4 48.5 1.8 97.1 3.2 90.4 4.1 73.2 3.8 97.7 2.8 99.3 2.9 0.0012
Biomass in the reactor (g L1) 4.8 0.4 4.9 0.16 2.4 0.13 e e e 8.4e26.7 26.13e41.1 e
YP/S yield (g ethanol
g substrate1)
0.34 0.01 0.31 0.01 0.24 0.01 0.45 0.02 0.35 0.01 0.27 0.01 0.42 0.02 0.46 0.01 0.0056
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exceeding 98%, especially for MBR and ICR configurations
which indicated that sugars were completely consumed by
yeast.
The experimental YP/S yield compared to the theoretical
performance is more important in both ICR and MBR reactors
than in the CSTR because the microbial activity in both cases
is more important than for theCSTR. The best YP/S of0.46gg 1
and the Ys of 99.3% were obtained with the MBR. However, inthe case of CSTR YP/S decreased as the cell concentration
within the reactor was diluted by increasing the D.
Themass balancein the systemswas calculated. The mass
substrate was converted in to ethanol, carbon dioxide,
biomass, glycerol and organic acids. The total feed mass was
calculated from the mass of sugars feeding per day. The
biomass generated may be accumulated in the reactors or
washed out in theeffluent daily.It was measured byTSS in the
CSTR and the MBR and by volume variation in the ICR. Results
showed that mass recovery from substrates ranged between
78% for the CSTR to 99% for the MBR. It is very likely that the
low mass balance in the CSTR was due to an ethanollostin the
carbon dioxide event and the secondary metabolites produc-tion like glycerol and organic acids.
4. Conclusion
Results showed that the performance of the MBR was more
advantageous than the CSTR and the ICR for anaerobic sugar
cane molasses fermentation since a higher concentration of
ethanol (41.4 g L1) and Qp (12.83e19.2 g L1 h1), with low
residual substrate content were achieved. These results
showed the interest of using the MBR to reach a high ethanol
concentration which confirmed the effectiveness of thistechnology.
Acknowledgements
The authors wish to acknowledge the Ministry of Superior
Education and Scientific Research and Technology, which has
facilitated the carried work.
Abbreviations
CSTR continuously stirred tank reactor
D dilution rate (h1)
ICR immobilised cell reactor
MBR membrane bioreactor
OD optic density
m max (mu-max) maximum specific growth rate (h1)
ORP oxidation reduction potential (mV)
Qp ethanol productivity (g L1 h1)
TRS total reduced sugars (g L1)
YP/S mass ratio between ethanol and sugar (g g 1)
WTW WTW GmbH, Weilhem, Germany
Ys substrate conversion yield (%)
r e f e r e n c e s
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