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A study on the effect of parameters on lactic acid production from whey

Article  in  Polish Journal of Chemical Technology · March 2016

DOI: 10.1515/pjct-2016-0010

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58 Pol. J. Chem. Tech.,
Polish
Vol.
Journal
18, No.
of 1,
Chemical
2016 Technology, 18, 1, 58—63, 10.1515/pjct-2016-0010

A study on the effect of parameters on lactic acid production from whey

Hamidreza Ghafouri Taleghani1, Ghasem D. Najafpour 2*, Ali Asghar Ghoreyshi 2
1
University of Mazandaran, Faculty of Chemical Engineering, Babolsar, Iran
2
Babol Noshirvani University of Technology, Faculty of Chemical Engineering, Babol, Iran
*
Corresponding author: e-mail: [email protected]

In batch fermentation of whey, selection of suitable species at desired conditions such as substrate, product concen-
trations, temperature and inoculum size were investigated. Four Lactobacillus species and one Lactococcus species
were screened for lactic acid production. Among them L. bulgaricus ATCC 11842 were selected for further studies.
The optimal growth of the selected organism for variable size of inocula was examined. The results indicated that
inoculum size had insignificant effect on the cell and lactic acid concentration. The effect of temperature was also
studied at 32, 37, 42 and 47°C. Results showed that the concentration of cell dry weight increased with increment
of temperature from 32 to 42°C. The maximum cell and lactic acid concentration was obtained at 42°C. The ef-
fect of initial substrate concentration on lactic acid production was also examined. The optimum initial lactose
concentration was found to be 90 g/l.

Keywords: lactose, lactic acid, fermentation, Lactobacillus bulgaricus, whey.

INTRODUCTION range of temperatures19. Microbial growth is governed

by the rate of chemical reaction catalyzed by enzymes
Lactic acid is the most widely occurring hydroxy car-
within the cell20.
boxylic acid found in most living organisms1. Lactic acid
The lactic acid bacteria requires substrates with high
is an important chemical used in variety of food-related
nitrogen content and it has a particular demand for
industries; however its main potential use is an inter-
vitamins B21. The nitrogen sources required for the
mediate agent for manufacturing of the biodegradable
fermentation medium are supplied in the form of yeast
polymer and poly lactic acid2, 3.
extract, cotton oil, soy flour, tryptone and peptone22.
There are two main routes for producing lactic acid;
In the current study, lactose hydrolysate from cheese
synthetic route through hydrolysis of lactonitrile and
whey was used as substrate for growth of LAB. This
microbial route through fermentation of carbohydrates
substrate supplied sufficient nutrients for some organisms.
using lactic acid bacteria (LAB)4. Production of lactic
Four Lactobacillus species and one Lactococcus species
acid by fermentation has received much attention in past
were screened for lactic acid production; among them
decade as evidenced by a number of patents and scien-
the desired species was selected for further studies. The
tific articles which has been published in recent years5, 6.
influence of temperature, inoculum size, and initial sub-
Conversion of dairy waste streams into lactic acid is
strate concentration on the cell growth and lactic acid
a process with several beneficial facts7. On one hand
production was investigated.
cheese waste poses an environmental threat and on the
other hand it represents an abundant renewable raw
material for production of several value-added products MATERIAL AND METHODS
such as lactic acid8.
There are several vital factors affecting the fermenta- Microorganism and medium
tive production of lactic acid9. The choice of substrate, The L. delbrueckii ATCC 9649, L. casei ATCC 39392,
LAB species and operating conditions are a few influ- L. bulgaricus ATCC 11842 and Lactococcus lactis ATCC
ential parameters which should be considered for lactic 11454 were obtained from Iranian Research Organization
acid production. Science and Technology (IROST). Man-Rogosa-Sharpe
Substrate for the lactic acid fermentation process can (MRS) medium was used for cultivation of bacteria. The
be chosen from a variety of carbon sources, such as MRS medium consists of yeast extract, 5 g; meat extract,
glucose, xylose, sucrose and lactose10–13. The choice of 5 g; peptone, 10 g; K2HPO4, 2 g; diammonium citrate,
substrate depends upon its availability, cost and pretre- 5 g; glucose, 20 g; sodium acetate, 2 g; MgSO4 . 7H2O,
atment required for fermentation14. 0.58 g; MnSO4 . 4H2O, 0.2 g, in one liter medium. The
There are several species of bacteria that are capable media were sterilized at 121oC for 15 minutes before
to produce lactic acid from lactose such as L. bulgaricus8, inoculation.
L. plantarum15 and L. casei16, 17.
Media temperature is one of the important factors Substrate preparation
that affects the growth of microorganism18 Dong-Hoon</ Sweet cheese whey was obtained from a dairy plant
author><author>Lim, Wan-Taek</author><autho- (Kalle, Mazandaran, Iran). The whey was first filtrated in
r>Lee, Mo-Kwon</author><author>Kim, Mi-Sun</ order to separate the coagulated proteins. Then lactose
author></authors></contributors><titles><title>Ef- in the presence of dilute acid was hydrolyzed to galactose
fect of temperature on continuous fermentative lactic and glucose (1 ml HCl in 100 ml whey). After 24 h, the
acid (LA. Most species have a characteristic range of whey was neutralized with 1M NaOH solution. The pH
temperature, in which they can grow and propagate, of pretreated whey was adjusted to 6.5. A 0.3% (w/v)
but they do not grow at the same rate over the whole yeast extract was added to the whey in all fermentation
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 Pol. J. Chem. Tech., Vol. 18, No. 1, 2016 59

experiments except when the effect of nitrogen source

was examined. Deprotonated and hydrolyzed whey was
prepared as suitable medium for fermentation. The
initial lactic acid concentration in the cheese whey was
less than 2 g/l.

Analytical methods
Substrates and products were analyzed by HPLC
(Shimadzu-Japan) equipped with a Shim-pack CLC-ODS
column. The column, maintained at 75°C, was eluted with
4 mM H2SO4 at a flow rate of 0.4 ml/min for 20 min.
The retention time of lactic acid under these conditions
was 18 min. The samples were centrifuged at 5000 rpm
for 5 minutes and then filtered through 0.2 μm paper
filter (Whatman). To obtain the desired peak height,
10 μl of clear sample solution was injected to HPLC. Figure 1. Cell growth profiles for the selected microorganisms
Growth rates were monitored by measuring optical
density (the absorbance at 620 nm) using a Unico 2100
spectrophotometer. The dry cell weight was measured
using a pre-developed calibration curve.

Fermentation
The bacteria were cultured in 100 ml MRS medium in
250-ml Erlenmeyer flasks. The medium temperature was
adjusted according to the proposed temperature for the
optimum growth of the respective organism, i.e., 30°C
for the Lactococci strains, 32°C for L. casei and 37°C for
L. delbrueckii. For each strain, several parallel fermenta-
tions were carried out with different conditions to obtain
the highest cell growth. The fermentations were carried
out in vessels with 500 ml volume and controlled at the
optimal growth temperature for the respective organism.
The vessels were sealed with a rubber cap with ports to Figure 2. Utilization of lactose as substrate by the selected mi-
allow insertion of a sampling device. Stirring at approxi- croorganisms
mately 180 rpm was applied using an incubator shaker.
up to 80% of lactose. However, only 35% of lactose was
consumed even after 72 hours by L. delbrueckii. The
RESULTS AND DISCUSSION
fermentations were considered completed when substrate
was depleted or the lactic acid production was ceased.
Microorganism The lactic acid production using different strains is
The growth of several LAB and their lactic acid pro- illustrated in Figure 3. All of the four organisms pro-
duction ability was investigated in some batch fermen- duced lactic acid. L. bulgaricus exhibited the highest
tation experiments. Four microorganisms, L. delbrueckii, lactic acid concentration and L. delbrueckii produced
L. casei, L. delbrueckii and Lactococcus lactis were used the lowest amount of lactic acid. The fermentation with
for the fermentative production of lactic acid from L. delbrueckii was stopped after 72 hours of incubation
whey. These bacteria are very important for the dairy since small amount of lactic acid was produced. The
industry because of their use in milk fermentation to maximum lactic acid concentration of 23.3 and 21.5 g/l
convert substrate to lactic acid for product preservation.
Therefore, it is important to determine the performance
of each species. Each experimental test was repeated in
various conditions and the best results were reported.
Figure 1 shows the cell concentration in batch fer-
mentation process using whey as carbon source. Results
indicated that all strains were able to ferment lactose
except L. delbrueckii. Figure 1 also shows that L. bulga-
ricus and L. Casei had the highest cell concentrations.
The exponential phase, defined as the time with maxi-
mal lactic acid production, was around 36 h and ended
at about 48 h in all fermentations. There was a strong
relationship between the cell concentration and substrate
consumption.
Figure 2 demonstrates the utilization of lactose of whey
as substrate. As it was expected, L. bulgaricus can utilize
Figure 3. Lactic acid production by the selected organisms
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60 Pol. J. Chem. Tech., Vol. 18, No. 1, 2016

was obtained with L. bulgaricus and L. Casei, respecti- probable occurrence of lag phase. Furthermore, the
vely. The results proved that L. bulgaricus is the most effect of inoculum size on L. bulgaricus has not been
potent strain for lactic acid production. Therefore, further reported in any previous study. In this work, the growth
investigations on lactic acid production were performed of L. bulgaricus using inoculum sizes ranging between
with this strain. The yield of lactic acid based on total 1–15% was examined. The results indicated that inoculum
sugar was 70–80% for three strains whereas the yield size had no significant effect on the cell concentration
for L. delbrueckii was much lower than other species. as the size of inoculums exceeded certain percentages.
The highest cell concentration of 4.6 g/l was obtained
Growth kinetics with inoculum size of 10% (see Fig. 4). In addition,
Kinetic models are being widely used for better inoculum size could have an effect on the duration of
understanding of the microorganism growth. Several the lag phase. It was expected that duration of the lag
growth-related kinetic models were tested in this study. phase decrease with an increase in inoculum size but
However, among them logistic model was capable of when inoculum size was increased to above 5%, the
predicting the growth curve of Lactobacilli bacteria and lag phase decreased. A long lag phase is undesirable
was well fitted with experimental data. Logistic model is because it is time consuming and the medium is used to
a suitable model for prediction of lag, exponential and maintain a viable culture prior to the growth. Therefore,
stationary phases of growth curve. The specific growth 5% inoculum was performed better than 10% because
rate predicted by this model is presented by the follo- the lag phase for 10% inoculum was a little longer than
wing equation: 5%. Effect of inoculum size on lactic acid concentration
is given in Table 2.
(1) Table 2. Effect of inoculum size on lactic acid concentration

Where μmax is the maximum specific growth rate (h–1)

and xmax is the maximum cell dry weight concentration
(g/l). This equation is known as the Riccati equation,
which can be easily integrated to give the logistic equation:

(2)

Determination of growth kinetic parameters

Growth kinetics is typically categorized to either struc-
tured and unstructured models or segregated and non-
-segregated models20. In this study, the governing model
was selected to be unstructured and non-segregated in
logistic category. Data obtained in batch fermentation
were used to determine the cell growth kinetic parame-
ters. The kinetic parameters were calculated by non-linear
least square analysis. MATHLAB software was applied
to predict the logistic growth kinetic parameters for all
cultures. The defined kinetic parameters are summarized
in Table 1.
Figure 4. Effect of inoculum size on L. bulgaricus growth dur-
The high coefficient of determination (R2) shows the ing lactic acid fermentation. Experimental conditions:
high accuracy and capability of the model to interpret initial lactose concentration: 50 g/l; pH: uncontrolled,
the experimental data. According to data presented in temperature: 40°C and yeast extract: 0.3%
Table 3, L. bulgaricus has the highest specific growth
rate of 0.18 h–1. However, based on lactic acid yield data presented in
the table, the maximum concentration of lactic acid of
Table 1. Kinetic parameters of logistic model for different 24.6 g/l was obtained at inoculum size of 10%.
bacteria at different temperatures
Effect of temperature
Temperature is one of the most important factors that
influences the growth of microorganism but the effect
of temperature on lactic acid production has only been
studied in few reports9. L. bulgaricus is mesophilic bacte-
rium which grows in temperature range of 30 to 50oC24.
Effect of inoculum size
The effect of temperature on lactic acid fermentation
In industrial lactic acid fermentation process, the was investigated at 32, 37, 42 and 47°C using whey with
inoculum size range is usually between 3 to 10% (v/v) 50 g/l of lactose concentration, 0.3% of yeast extract and
of the fermentation broth volume23. 5% of inoculum. The effect of temperature on bacterial
The assumption that inoculum size has insignificant growth is depicted in Figure 5.
effect on microbial growth once growth is initiated; The results indicated that the lag phase of bacterial
however suitable size of inoculum would eliminate the growth at 32°C was longer than other temperatures, as
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 Pol. J. Chem. Tech., Vol. 18, No. 1, 2016 61

Figure 5. The effect of temperature on bacterial growth. Experi- Figure 7. Effect of temperature on lactic acid production.
mental conditions: initial lactose concentration: 50 g/l; Experimental conditions: initial lactose concentra-
pH: uncontrolled; inoculum: 5% and yeast extract: tion: 50 g/l; pH: uncontrolled; inoculum: 5% and
0.3% yeast extract: 0.3%

the bacteria needed to be adapted to the environment. temperature for the L. bulgaricus was 45°C. Audet et
The maximum concentration of cell dry weight increased al.26 and Samuel et al.27 reported that temperature of
with increase of temperature from 32 to 42oC. The 42°C is the optimal growth temperature for L. bulgaricus
maximum concentration of dry cell weight obtained at While Mozzi et al.28 reported that 37°C is the desired
42°C was 4.7 g/l. The exponential phase of the bacterial growth temperature for L. bulgaricus. These differences
growth for 32, 37, 42 and 47°C was started at about 12, may be due to the diversity of substrate, product and
4, 4 and 6 h, respectively. operating conditions.
Figure 6 shows the effect of temperature on lactose
utilization during the fermentation process. It appears Effect of initial lactose concentration
that the consumption of lactose at 42°C was faster than The effects of initial lactose concentration on cell
other temperatures. However, after 72 hours of incuba- growth, lactic acid production and lactose utilization
tion, the carbohydrate concentration profile shows the were investigated. Figure 8 shows the growth profile of
substrate is not fully utilized. L. bulgaricus in batch fermentation process using lactose
of whey as carbon source. The range of lactose concen-
tration was 30 to 120 g/l. The results indicate that the
cell dry weight concentration was related to substrate
concentration. High substrate and product concentrations
may cause growth inhibition, as the microorganisms may
be intoxicated in an undesired condition. With initial
lactose concentration of 90 g/l, maximum dry cell weight
of 5.0 g/l was obtained. When the substrate concen-
tration was increased to 120 g/l, the concentration of
biomass decreased to 3.2 g/l; this proved that substrate
inhibition existed.

Figure 6. Effect of temperature on lactose consumption. Ex-

perimental conditions: initial lactose concentration:
50 g/l; pH: uncontrolled; inoculum: 5% and yeast
extract: 0.3%

The effect of temperature on lactic acid production is

given in Figure 7. The maximum concentration of lactic
acid obtained at the temperature of 42°C was 24.3 g/l. It
can be seen that when the temperature was increased to
42°C, the lactic acid production increased. Nevertheless,
when the temperature was further increased to 47°C, the
lactic acid concentration decreased to 17.5 g/l.
The results indicated that the suitable temperature Figure 8. Effect of initial substrate concentration on cell con-
for the production of lactic acid by L. bulgaricus was centration. Experimental conditions: temperature:
42°C. According to Hofvendahl et al.25, optimal growth 42°C; pH: uncontrolled; inoculum: 5% and yeast
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62 Pol. J. Chem. Tech., Vol. 18, No. 1, 2016

The effect of initial lactose concentration on product Effect of nitrogen sources

formation is shown in Figure 9. The highest concentration The effect of nitrogen source on lactic acid production
of lactic acid which obtained at 90 g/l lactose was 32.1 by L. bugaricus was investigated using whey as substrate,
g/l. When the concentration of lactose was increased, at the temperature of 42°C and inoculum size of 5%. The
the lactic acid production decreased; that was due to results are summarized in Table 3. The results showed
inhibitions caused by the high substrate concentration. that lactic acid production increased with increasing the
At high substrate concentration of 120 g/l, the concen- concentration of supplements, specially yeast extract
tration of lactic acid dropped to 14.9 g/l that was due (Y.E.). The highest production rate was found with ad-
to existing inhibition in batch process. dition of 1% of yeast extract. However, the addition of
yeast extract during large scale fermentation is unlikely
due to the extra cost imposed to the fermentation process.
Table 3. Effect of nitrogen source, type and concentration on
lactic acid production

The yeast extract exhibited the highest yield of lactic

acid, followed by meat extract (M.E.) and peptone.
Therefore, yeast extract is the best nitrogen source for
Figure 9. Effect of initial substrate concentration on lactic acid lactic acid production using L. bulgaricus. The use of
production. Experimental conditions: temperature: yeast extract as nitrogen source not only increased the
42°C; pH: uncontrolled; inoculum: 5% and yeast
bacterial growth but also reduced the time required
extract: 0.3%
for the completion of fermentation. This could be due
to the nutritional value of yeast extract which contains
In comparison to similar works conducted by other
substances such as amino acid, peptides, vitamins, and
investigators, the reported concentration of lactic acid at
several organic acids including pyruvic and glyseric acid
controlled pH was slightly higher than the values obtained
which are needed for the L. bulgaricus growth.
in present work29, 30. When pH was uncontrolled, the
The maximum obtained cell concentration was 5.2 g/l
pH dropped to values lowers than 3. This condition was
which was achieved by 1% yeast extract. The results also
unfavorable for the growth activity of the fermentative
indicated that yeast extract alone at high concentration
lactic acid bacteria and the microorganisms were unable
gave higher lactic acid production than yeast extract and
to fully utilize the substrate.
peptone at low percentages. Furthermore, addition of
Figure 10 illustrates the utilization of various con-
peptone to yeast extract had little effect on the produc-
centrations of lactose as substrate. It appears that the
tion of lactic acid.
consumption of lactose decreased when the initial lactose
concentration was increased. In the course of fermenta-
tion, with initial lactose concentration of 30 g/l, 87% of CONCLUSIONS
the substrate was consumed. At initial lactose concentra- The cheese whey waste from dairy industry was used
tion of 120 g/l, consumption of lactose dropped to 50%. as carbon source for lactic acid production. The different
bacteria were tested for their growth behavior and lactic
acid production ability. L. bulgaricus had high perfor-
mance and then it was selected for further studies. The
effects of some parameters such as temperature, inoculum
size, substrate concentration and nitrogen source were
studied. The optimal values of tested variables for ma-
ximal lactic acid production were found to be: inoculum
size of 5%, temperature of 42°C, yeast extract of 1%
and initial lactose concentration of 90 g/l.

ACKNOWLEDGMENT
The authors are thankful to Biotechnology Research
Center, Noshirvani University of Technology, Babol,
Iran, for the facilities provided to accomplish the pre-
sent research.
Figure 10. Effect of initial substrate concentration on lactose uti-
lization. Experimental conditions: temperature: 42°C;
pH: uncontrolled; inoculum: 5% and yeast extract:
0.3% Unauthenticated
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 Pol. J. Chem. Tech., Vol. 18, No. 1, 2016 63

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