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Keywords: The present work investigates the reaction kinetics of biodegradation of waxy crude oil using Bacillus subtilis YB7,
Biodegradation a thermophilic organism. Mathematical modeling of the reaction kinetics of microbial growth together with
Biosurfactant biosurfactant production and hydrocarbon substrate utilization have been attempted. Although various models,
Kinetic modeling such as Monod's, Logistic, Tessier and Contois were investigated for substrate degradation and biomass produc-
Monod's model tion, and compared with the experimental studies, none of them could accurately predict the biosurfactant
Thermodynamics
production in the presence of waxy crude oil. In this study, a new model, which is an extension of Monod's
equation, has been developed to predict the observed values of biosurfactant production along with substrate
degradation and biomass production in the presence of waxy crude oil satisfactorily. The proposed model has also
been tested with various experimental studies carried out in the literature. The proposed model is observed to
provide satisfactory model predictions when compared to other models available in literature. This shows that the
proposed model can be used to study the reaction kinetics of all types of biodegradation studies to find the op-
timum parameters for maximum possible biodegradation of hydrocarbon substrates and production of bio-
surfactant. The positive values of activation energy observed in the study indicates that the process of
biodegradation is an endothermic process. The negative values of entropy indicates that the reacting molecule
underwent an internal rearrangement to give the activated complex, without a change in the number of mole-
cules. It is believed that this study will be suitable for possible model development for biodegradation of hy-
drocarbons for oil recovery applications or bioremediation methods.
* Corresponding author.
E-mail address: jitendrasangwai@iitm.ac.in (J.S. Sangwai).
https://doi.org/10.1016/j.petrol.2017.10.056
Received 9 June 2017; Received in revised form 4 October 2017; Accepted 19 October 2017
Available online 23 October 2017
0920-4105/© 2017 Elsevier B.V. All rights reserved.
N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
Table 1
Various kinetic models used in this study.a
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N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
Table 2
Comparison of microbial growth rate with degradation of waxy crude oil and production of surfactin at 48 h of incubation.a
Temperature, C μ td, R2 S P,
The current study involves the mathematical modeling of the reaction hydrocarbon is relative to the total area of peaks. The percentage
kinetics incorporating microbial growth, biosurfactant production and degradation of waxy crude oil was evaluated by matching the area of
substrate utilization using Bacillus subtilis YB7 a thermophilic organism. the peaks acquired before and after the crude oil degradation in the
Formulation of an appropriate mathematical model serves as a guide to chromatograph as obtained from GC-MS. The collected samples were
microbial process developments with relevance to degradation. Various also analyzed for the production of biosurfactant (Cooper et al., 1981),
models have also been compared with the experimental results and the microbial count (colony forming units) (Hassanshahian et al., 2014),
new model has been developed to get the best fit with the observed and biomass dry weight (Etoumi, 2007). All the experiments were
experimental values. The developed model has been compared with the carried out in triplicates and the mean values were reported in
experimental values on biosurfactant production, substrate degradation, Figures and Tables. Error bars in the figures represent the standard
and microbial growth taken from our previous studies (Sakthipriya et al., deviation of triplicates.
2015b, 2015c) and other data available in literature. Other than kinetic
studies, thermodynamic behavior of biodegradation is necessary to check 3. Reaction kinetics
the feasibility of the process for large scale industrial applications. Such
studies are not common in the literature dealing with the biodegradation The specific growth rate (μ, h1) of the microorganism is calculated
of petroleum fractions. Hence, in this study, thermodynamic behavior of from Eq. (1).
biodegradation of hydrocarbon has also been investigated.
dX
¼ rx ¼ μX (1)
2. Biodegradation experiments dt
Table 3
First order rate constant of biodegradation of waxy crude oil using Bacillus subtilis.
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N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
Fig. 6. Plot to calculate yield coefficients for (a) biosurfactant produced per waxy crude oil utilized; (b) biomass produced per waxy crude oil utilized; (c) biosurfactant produced per
biomass produced.
3.2. Yield coefficient The experimental values on biomass dry weight, biosurfactant pro-
duction and the amount of waxy crude oil utilization has been compared
The quantity of the biomass existing at the end of exponential growth using various kinetic models reported in the literature, such as the
phase was used to estimate the yield coefficient of biomass (YX/S) in the Monod, Tessier, Contois and logistic (Tessier, 1936; Monod, 1949;
presence of hydrocarbons. YX/S can be calculated from the Contois, 1959; Kumar et al., 2005). In addition to these models, a new
following equation. model has been developed in this work with the help of basic Monod's
model incorporating the biomass production. According to Lee (2006),
dS 1 dX
¼ (5) the microbial growth rate is directly proportional to the biomass dry
dt YX=S dt
weight during the exponential growth phase under standard nutrient
Integrating Eq. (5) with limits S0 to S, and X0 to X, gives, condition. Hence, we have incorporated biomass dry weight ‘X’ in our
model. Table 1 gives the information on various models and their pa-
X X0 rameters used in this study. The best fit of the model was identified with
YX=S ¼ (6)
S0 S the help of regression coefficient (R2). The R2 value suggests the most
suitable kinetic model and the kinetic parameters associated with
where, X0 is initial biomass concentration, (g L1); S and S0 are substrate that model.
(crude oil) concentration at any time and initial substrate concentration, The specific growth rate in Eq. (1), was replaced by different forms
(g L1). YX/S is the yield of biomass per substrate utilization, (g g1). The as given in Table 1. Table 1 also provides the equation for specific
yield coefficient for biosurfactant production (P) and crude oil utilization growth rate suggested in this work as an extension to the Monod's
(S) can be calculated according to the relationship reported by model. The modified set of equations were solved using MatLab® 2010
Hong (1989). (The math works, USA) with the help of a function ode45. The kinetic
parameters, such as μmax, KS, B, f, YX/S and YP/X were estimated by
dP dX
¼ YP=X (7) assuming the initial set of parameter values. Generally, the initial
dt dt values will be obtained from the experimental results. The sum of
Combining Eqs. (1), (5) and (7), we get: squares of the error between the predicted values and the experimental
415
N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
5 4
4
3
-1 -1
0 200 400 600 800 0 200 400 600 800
Time (h) Time (h)
4 4
3
3
2
2
1
1
(c) 0 (d)
0 -1
0 200 400 600 800 0 200 400 600 800
Time (h) Time (h)
4
3.5
3
X,S and P (g/L)
2.5
1.5
1
(e)
0.5
0
0 200 400 600 800
Time (h)
Fig. 7. Kinetic modeling, (a) Monod's model; (b) Contois model; (c) Tessier model; (d) Logistic model; (e) Present model; Circles-Experimental values; Red color-Biosurfactant production
(P); Blue color-Biomass dry weight (X); Green color-Waxy crude oil degraded (S). (For interpretation of the references to colour in this figure legend, the reader is referred to the web
version of this article.)
(R2) was determined. The set of values giving the highest R2 was pre- 4. Thermodynamic studies
dicted. In all the models, the parameters μmax, KS, YP/X and YX/S were
taken from the experimental outcomes for preliminary guess and tuned Thermodynamic parameters, namely, enthalpy (H), entropy (S) and
to determine a satisfactory match between the experimental and pre- Gibb's free energy (G) are important to estimate the feasibility of the
dicted data. biodegradation process. The entropy of activation is calculated as (Low
et al., 1973),
Table 4
Model parameters for the rhamnolipid formation, substrate utilization and biomass growth.
*KS-Saturation constant, g L1; A-factor depending on biomass dry weight; μmax -Maximum growth rate of microorganism, h1; YP/X-Yield of the rhamnolipid on cell weight,g g1; YP/S- Yield
of rhamnolipid on substrate, g g1; YX/S- Yield of biomass on substrate, g g1.
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N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
3.5 3.5
3
(a)
3
2 2
1.5 1.5
1 1
0.5 0.5
0 0
0 10 20 30 40 50 60 0 20 40 60
Time (h) Time (h)
(c)
2.5
2
S and P (g/L)
1.5
0.5
0
0 10 20 30 40 50 60
Time (h)
Fig. 8. Model validation of substrate utilized and biosurfactant produced; (a) Present model; (b) Monod's model; (c) Tessier model; Circles-Experimental values of Nitschke and Pastore
(2006); Red color-Biosurfactant production (P); Blue color-Waxy crude oil degraded (S). (For interpretation of the references to colour in this figure legend, the reader is referred to the web
version of this article.)
417
N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
microorganisms has increased upto 10 days, and decreased thereafter. 2015b.). The effect of temperature on the rate of biodegradation of has
The maximum growth of bacteria was found to be at 50 C rather than at been studied by incubating microorganism with crude oil at various
35 and 75 C. An increase in the number of active cells increases the temperatures, such as 35, 50 and 75 C. Fig. 2 shows the chromatograms
degradation rate. This indicate the efficacy of the Bacillus subtilis YB7 for of waxy crude oil before degradation and after degradation at 35, 50 and
effectual biodegradation of hydrocarbons appropriate for oil recovery 75 C. Comparing the area under the peaks of chromatographs before and
from reservoirs, bioremediation, and flow assurance studies. after degradation, it has been observed that the maximum 96% of waxy
Bacillus subtilis is observed to produce a biosurfactant called surfactin. crude oil was degraded in 10 days, and negligible degradation was
Various researchers have observed that the Bacillus subtilis can produce observed thereafter. This result is in good agreement with the microbial
surfactin in the range of 0.025–3 g L1 at 28 to 40 C (Grishchenkov et al., growth (see Fig. 1). The crude oil degradation was 80 and 85% after 10
2000; Nitschke and Pastore, 2006; Salehizadeh and Mohammadizad, days of incubation at 75 and 35 C, respectively. This indicates that the
2009; Darvishi et al., 2011; Al-Bahry et al., 2013). We also have reported incubation temperature has pronounced impact on the degradation of
similar studies on the production of surfactin in the presence of crude oil hydrocarbons under biodegradation conditions. Fig. 3 shows the char-
as used in this investigations. Details of the biosurfactant experiments acteristic of Bacillus subtilis at the optimum temperature of 50 C. It is
used for validation here is presented elsewhere (Sakthipriya et al., 2015b, clearly understood that production of biosurfactant directly impacts
2015c). The adequacy of the biosurfactant production and the detailed crude oil degradation.
measurements were given in our previous reported study (Sakthipriya
et al., 2015c) and are not reproduced here for the sake of brevity. In the 5.2. Reaction kinetics
previous study, we have analyzed the production and characterization of
surfactin using various hydrocarbon substrates at various temperatures Fig. 4 shows the plot for growth kinetics of Bacillus subtilis at various
elaborately and observed maximum of 4 g L1 of surfactin at 50 C temperature with waxy crude oil as a carbon source. The graph was
(Sakthipriya et al., 2015c). plotted for ln (X/Xo) versus incubation time. The slope of the plot gives
The biodegraded samples of crude oil were fractionated using GC-MS, the specific growth rate of the microorganism (Eq. (2)). The comparison
and the extent of biodegradation was determined (Sakthipriya et al., of microbial growth rate with degradation of paraffin and production of
0.5 0.5
0.3 0.3
X(g/L)
X(g/L)
0.2 0.2
0.1 0.1
0 0
0 50 100 150 200 250 0 50 100 150 200 250
Time (h) Time (h)
0.4
(c)
0.3
X (g/L)
0.2
0.1
0
0 50 100 150 200 250
Time (h)
Fig. 9. Model validation of biomass produced; (a) Present model; (b) Monod's model; (c) Tessier model; Circles-Experimental values of Zhang et al. (2005).
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N. Sakthipriya et al. Journal of Petroleum Science and Engineering 160 (2018) 412–421
surfactin is given in Table 2. The specific growth rate was observed to be the model fits X and S, it did not satisfy P. The model values fitting the
0.075 ± 0 .0016, 0.084 ± 0.013 and 0.0710.071 ± 0.005 h1, respec- experimental results of stationary growth phase did not match with
tively, at 35, 50 and 75 C. The corresponding values of doubling time are observed values during exponential growth phase. Hence, in order to
9.25 ± 0.12, 8.25 ± 0.1, and 9.76 ± 0.20 h. The doubling time at 50 C is overcome this difficulty, we have proposed a model incorporating the
found to be lesser than that incubated at 30 and 75 C. term ‘X’ in the basic Monod's equation (Table 1). The proposed model
The concentrations of waxy crude oil degraded (S) has been deter- gives the best fit for biomass production (R2 ¼ 0.99) and substrate uti-
mined by gas chromatographic techniques at various time intervals. lization (R2 ¼ 0.99). The proposed model has also fitted the biosuractant
Initially, the reaction is assumed to follow the first order kinetics and the production perfectly (R2 ¼ 0.95) compared to any other model in the
graph was plotted for ln(S/So) against incubation time and it gave literature (Fig. 7e).
straight lines. The R2 values were found to be 0.9 for all the incubation The proposed model has also been compared with other experiment
temperatures, which suggests that the biodegradation of waxy crude oil values reported in the literature. The values of biosurfactant produced
follows the first order reaction. The first order rate constants were and substrate degraded were taken from the Nitschke and Pastore (2006)
calculated from the slopes of these lines and are given in Table 3. and compared with the proposed model. These data were are also
Fig. 5 shows the growth curve of Bacillus subtilis at 50 C extended compared with the prediction of Monods and Tessier model. Compared
upto the endogenous region. The values of natural logarithm of optical to other models, the one proposed in this work gives better fit (Fig. 8).
density was plotted against incubation time and the value obtained The biomass values from Zhang et al. (2005) have also been compared
from the slope of the graph gives the decay coefficient. According to with many other models along with the proposed one and found that the
Kumar et al. (2005), the value of kd is independent of the initial sub- proposed model provided better match (Fig. 9).This indicate the
strate concentration. The value of the coefficient of decay rate was robustness of the proposed model in this work as compared to other
observed to be 0.00003 h1 for waxy crude oil. Decay coefficient available models. .
directly affects the growth rate. Due to this, the wash out condition
(growth cannot be sustained) will occur at low dilution rate. This will
be very important in case of continuous flow mixed reactors during 5.4. Thermodynamic behavior of biodegradation
large scale applications.
Fig. 6 shows the plots to determine yield coefficients for biosurfactant In order to make the biodegradation successful for industrial appli-
produced per waxy crude oil utilized (YP/S); biomass produced per waxy cation, thermodynamic feasibility is the major concern. Fig. 10 shows the
crude oil utilized (YX/S) and biosurfactant produced per biomass pro- variation of activation energy and pre-exponential factor during the
duced (YP/X), respectively. The amount of biomass available immediately course of degradation. It has been observed that the activation energy
at the end of exponential growth phase was used in estimating the required for the reaction increases with increase in time. The amount of
biomass produced as a result of consumption of substrate. According to energy required to initiate the degradation has almost doubled on 20th
Pirt (1975), the observed yield coefficient is calculated as, day of degradation when compared to day 1. This is because activity of
bacterial metabolism has found to be reduced over the period of time.
1 1 m During the course of incubation the microorganism will undergo the
¼ þ (15)
Y YT μ stationary growth phase and dead phase and their activity will reduce.
Hence, the energy required to activate the biodegradation process has
where, Y is the observed yield coefficient, YT is the true yield coefficient found to be increased with increase in incubation time. The positive
and m is the maintenance coefficient. In case of batch system, the growth value of Ea indicates that the degradation reaction is endothermic in
rate ‘μ’ does not vary significantly from μmax. Hence, any discrepancy nature. Table 5 gives the thermodynamic parameters for the biodegra-
arises because of the effect of maintenance requirement on the substrate dation of waxy crude oil using Bacillus subtilis. From the results, we have
utilization is neglected (Kumar et al., 2005). Thus, the observed yield observed the change in thermodynamic properties of biodegradation
coefficient is equal to the true yield coefficient. This observation is also with respect to temperature during the biodegradation process. Gibbs
supported by the negligible decay ratio. The value of YX/S in the presence free energy has also been increased with increase in temperature irre-
of waxy crude oil was observed to be 1.99 g/g, with the regression co- spective of the activity of microorganisms. Similarly, the change in
efficient (R2) of 0.98. The values of YP/X and YP/S were observed to be enthalpy of biodegradation has found to decrease with increase in in-
1.68 and 3.36 g/g, respectively, and the corresponding R2 values were cubation temperature. The negative values of ΔS showed that the for-
observed to be 0.99 and 0.96. mation of the metabolites, such as biosurfactant by Bacillus subtilis is
connected with a decrease in entropy. Also, the negative values of en-
5.3. Correlation of kinetics models tropy show that the biodegradation activated compound is highly orga-
nized compared to the initial compound. Mulla (2012) reported that
Fig. 7 shows the comparison between the experimental data with the thermodynamic compensation in any reaction occurs because of the
prediction of various kinetic models. Monod's model which forms the
foundation for many models matches only with biomass production
(R2 ¼ 0.97) and substrate degradation (R2 ¼ 0.79). Monod's equation has
fitted the experimental values of biosurfactant production only during
the initial degradation time (but not with the whole reaction time,
R2 ¼ 0.20). This observation is in-line with Lin et al. (2000), who stated
that the Monod model is applicable only during the exponential growth
phase (Fig. 7a). Contois model (see Fig. 7b) fits the observed values in all
the three plots of X, P and S with R2 of 0.81, 0.67 and 0.59, respectively.
The corresponding R2 values using Tessier model (Fig. 7c) are 0.76, 0.78
and 0.95. The values of the model parameters for the biosurfactant
production, substrate (crude oil) utilization and biomass growth are
given in Table 4. Logistic model developed by Mercier et al. (1992)
matches the X and S with the correlation coefficient of 0.98 and 0.80 (see
Fig. 7d). This model matches the biosurfactant production with R2 of Fig. 10. Variation of activation energy and pre-exponential factor as a function of
0.84. All the models described above did not fit all X, S, and P perfectly. If degradation time.
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Day 1 308 1390.02 42.89 14 601.00
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