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Urease production using corn steep liquor as a low-cost nutrient source by

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Environmental Science and Pollution Research
https://doi.org/10.1007/s11356-021-16568-6

RESEARCH ARTICLE

Urease production using corn steep liquor as a low-cost nutrient

source by Sporosarcina pasteurii: biocementation and process
optimization via artificial intelligence approaches
Mahdi Maleki-Kakelar 1 & Mohammad Javad Azarhoosh 2 & Sina Golmohammadi Senji 3 &
Abbas Aghaeinejad-Meybodi 2

Received: 10 April 2021 / Accepted: 12 September 2021

# The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract
To commercialize the biocementation through microbial induced carbonate precipitation (MICP), the current study aimed at
replacing the costly standard nutrient medium with corn steep liquor (CSL), an inexpensive bio-industrial by-product, on the
production of urease enzyme by Sporosarcina pasteurii (PTC 1845). Multiple linear regression (MLR) in linear and quadratic
forms, adaptive neuro-fuzzy inference system (ANFIS), and genetic programming (GP) were used for modeling of process based
on the experimental data for improving the urease activity (UA). In these models, CSL concentration, urea concentration, nickel
supplementation, and incubation time as independent variables and UA as target function were considered. The results of
modeling showed that the GP model had the best performance to predict the extent of urease, compared to other ones. The
GP model had higher R2 as well as lower RSME in comparison with the models derived from ANFIS and MLR. Under the
optimum conditions optimized by GP method, the maximum UA value of 3.6 Mm min–1 was also obtained for 5%v/v CSL
concentration, 4.5 g L–1 urea concentration, 0 μM nickel supplementation, and 60 h incubation time. A good agreement between
the outputs of GP model for the optimal UA and experimental result was obtained. Finally, a series of laboratory experiments
were undertaken to evaluate the influence of biological cementation on the strengthening behavior of treated soil. The maximum
shear stress improvement between bio-treated and untreated samples was 292% under normal stress of 55.5 kN as a result of an
increase in interparticle cohesion parameters.

Keywords Microbial induced carbonate precipitation . Biogrout . Industrial waste . Soil improvement . Shear strength . Genetic
programming . Adaptive neuro-fuzzy inference system

Introduction and control of soil properties are essential for geo-environ-

As the demand for engineering constructions is constantly
increasing, new and sustainable methods are required to adapt
the mechanical and physical properties of soils in an environ-
mentally friendly and cost-effective approach. Modification
Responsible Editor: Ta Yeong Wu
* Mahdi Maleki-Kakelar
mmaleki@znu.ac.ir
1
Department of Chemical Engineering, University of Zanjan,
Zanjan, Iran
2
Chemical Engineering Department, Urmia University, Urmia, Iran
3
Department of Civil Engineering, University of Tehran, Tehran, Iran
mental, geotechnical, and agricultural applications (DeJong
et al. 2011). Conventional methods of ground improvement
such as chemical grouting are frequently applied to improve
the strength and stiffness of the soil; however, such environ-
mentally unfriendly methods are costly and energy consum-
ing. These methods are also disturbing urban infrastructure
and may involve chemicals having adverse environmental im-
pacts (Van Paassen 2009).
To overcome these drawbacks, an emerging and promising
bio-mediated soil improvement technology termed as micro-
bial induced carbonate precipitation (MICP) has attracted a
significant amount of interests over the past decade. MICP
has been technologically developed for modification of the
engineering properties of soil through in situ cementation
(DeJong et al. 2010).

The most commonly studied system of MICP to date is
based on the hydrolysis of urea in a calcium-rich environment
owing to its simplicity and efficiency (Whiffin et al. 2007). In
MICP through microbial ureolysis, hydrolysis of urea enzy-
matically induces precipitation of CaCO3 and consequently
creates a cemented product in accordance with the following
equations (Stabnikov et al. 2011)
COðNH2 Þ2 þ 2H2 O→2NHþ
4 þ CO3
2−
ð1Þ
Ca2þ þ CO2−
3 →CaCO3 ðsÞ ð2Þ
The MICP process, as an effective and eco-friendly tech-
nology, can be utilized so far to solve different geo-
environmental problems, such as improvement in liquefaction
resistance (Xiao et al. 2018), heavy metal immobilization
(Zhao et al. 2017), suppression of coal dust (Song et al.
2019), and increasing resistance against wind erosion
(Maleki et al. 2016).
In the commercialization of bio-cement production, reduc-
tion of costs related to nutritional requirements is indispens-
able since the most costly stage of the biocementation process
is microbial growth and cultivation reaching up to 60% of the
total cost (Whiffin 2004). As a result, it would be a promising
idea to replace the existing standard nutrient medium with
commercially available nutrients such as bio-industrial waste
for cultivation of ureolytic bacteria and production of urease
enzyme prior to scale-up.
Several bio-industrial wastes rich in proteins such as
chicken manure effluent (Yoosathaporn et al. 2016), lac-
tose mother liquor (Achal et al. 2009), corn steep liquor
(Joshi et al. 2018), and activated sludge from agricul-
tural, dairy, and bakery industries (Cheng and Cord-
Ruwisch2013) could be adopted as different highly nu-
tritious supplements in biocementation processes. If ef-
fectively utilized, these byproducts provide a dual pur-
pose through both environmental protection via waste
recycling and cost reduction (Cuzman et al. 2015). In
particular, corn steep liquor (CSL) as a by-product of
wet-milling of the corn industry enjoys a nutrient-rich
supplement to encourage robust fermentation and micro-
bial growth (Lawford and Rousseau 1997).
Mathematical modeling is an appropriate tool for designing
and controlling the biochemical processes, particularly for
MICP (Martinez et al. 2014). Existing mathematical modeling
studies have described specific aspects of MICP including
biological, mechanical, and chemical processes. Several stud-
ies tended to focus on multicomponent reactive transport by
combining urea hydrolysis rate to calcite precipitation kinetics
as well as multidimensional fluid transport (Barkouki et al.
2011; Dupraz et al. 2009). A small number of studies have
also investigated the influences of reactive transport to me-
chanical modifications in soil using finite element analysis
(Martinez et al. 2014).
Environ Sci Pollut Res
Nevertheless, substantial attention has recently shifted to
modeling developments in engineering sciences through arti-
ficial intelligence-based approaches, i.e., adaptive neuro-
fuzzy inference system (ANFIS) and genetic programming
(GP), as well as multilinear regression (MLR) method
(Azarhoosh et al. 2018; Faradonbeh et al. 2016). Unlike the
physically based models, these models (ANFIS, GP, and
MLR) are data-driven models that only depend on the exper-
imental input and output to characterize the structure of sys-
tem, with the least assumptions about the physical perfor-
mance of the process. Furthermore, these methods do not uti-
lize any transport equation to derive the underlying relation-
ships of the system. ANFIS as a neural network is on the basis
of the Takagi-Sugeno fuzzy system. By coupling the neural
network and fuzzy logic concepts, ANFIS can take advantage
of both (Jang 1993). Moreover, the GP method is an extended
form of the genetic algorithm system, in which the programs
are represented by means of tree structures in functional pro-
gramming languages (Azarhoosh et al. 2017). This smart
method, which is not a black-box method, has been also found
to be highly accurate in modeling complex and nonlinear
functions (Azarhoosh et al. 2019).
However, no one as far as we know has studied the appli-
cation of the MLR, GP, and ANFIS methodologies for model-
ing the economical production of bacterial urease at high
levels, which is recognized as being a vital issue for large-
scale MICP applications. Accordingly, as one of the innova-
tions of the present study, the inexpensive CSL-urea media
were firstly investigated for its feasibility to serve as a suitable
alternative media for bacterial urease production as well as
biocementation of sandy soil. As the principal stage of the
MICP process, the production of urease was then modeled
and optimized by the application of MLR, ANFIS, and GP.
The mutual interactive effect of the factors such as CSL-urea
concentrations and incubation time was also investigated on
urease production. After that, a comparison was made among
the results of these models to reveal their performances, and
consequently, the optimum conditions were identified for the
urease production. Finally, laboratory tests were performed to
examine the interparticle interactions and strengthening be-
havior of MICP-treated soils.
Materials and methods
Materials
CSL was obtained from Glucosan Products (Qazvin, Iran) and
kept at 4°C. The crude CSL was treated as follows: crude CSL
was diluted ten-fold (v/v) with tap water, and then, the solu-
tion pH was adjusted to 7.5 applying 2 M KOH. After that, the
CSL solution was filtered by paper-filter to separate solid ma-
terials. The CSL medium comprising autoclaved tap water
Environ Sci Pollut Res
(TW) was completed with paper-filtered clarified corn steep
liquor. Liquid media were heat sterilized by autoclaving, and
afterward, urea and NiCl2 were added using a sterile 0.22 μm
Millipore filter.
Bacterial growth and urease activity
As an urease-positive bacterium, Sporosarcina pasteurii
(PTCC 1645) was utilized in this work. Inoculation of
S. pasteurii cells was undertaken in 200 mL of a CSL-based
media (different concentrations of CSL, urea, and NiCl2) by
moving aseptically approx. 10% (v/v) of the flask culture. In
the meantime, culture media were aerobically incubated at
30°C on a rotating shaker operating at 200 rpm. The culture
was harvested and stored at 4°C prior to use. The biomass
concentration was specified by quantifying the absorbance
(optical density) of the suspension using a spectrophotometer
(Spectroquant, PHaro 300, Merck, KGaA) at 600 nm wave-
length (OD600). By comparing OD600 and plate cell counting,
the concentration of cells suspended in the stock culture was
determined by the expression: C = 8.6 × 107 X1.36, where X is
reading at OD600 and C is the concentration of cells mL–1.
During the experiments, the bacterial suspension conduc-
tivity was utilized to ascertain the activity of urease in the lack
of calcium ions, as described elsewhere. It is worthwhile not-
ing that 1 mS/min is correlated with the enzyme activity of
11 mM urea/min in the measured range of activities
(Omoregie et al. 2019). A consort multiparameter analyzer
C20-30 with S K10T electrodes was employed for measuring
the electrical conductivity.
Experimental setup
So as to evaluate the potential of MICP on the shear strength
of soil, cubic molds were prepared with a manual inlet and
outlet. These molds were made of galvanized steel sheets hav-
ing standard dimensions of the direct shear test sample
(60×60×20 mm). The bottom and top of the mold were cov-
ered with an approximately 1 cm filter gravel layer to get a
uniform distribution of bacterial flow throughout the sample.
In the middle part of molds (10 cm), the soil specimen prep-
aration was carried out by dry tamping technique. The tapped
density of the soil specimen was approximately determined to
be 1.8 g cm–3(Fig. 1).
The sandy soil used in the current work was collected from
a dune near the Tabriz margin and sieved to get a consistent
form to reduce the effects of gradation in shear stress. The
gradation curve of soil and particle distribution is shown in
Fig. 2. In order to ensure the technical efficiency of
biocementation and bacterial activity between soil particles,
the specimens were molded by poorly graded coarse sand with
a mean grain size D 50 = 2.30 mm. The minimum and
maximum void ratios of soil samples were determined to be
emin = 0.61 and emax = 0.76.
The concentration and urease activity of the bacterial sus-
pension was determined immediately before use in the bio-
cement experiments. First, 15 mL of bacteria (containing
4.5×109 cells and urease activity of 3 mM urea hydrolyzed
min–1) was gravitationally decanted into the specimens for
filling the 0.25 pore volume of soil sample. Next, 15 mL of
the cementation fluid containing 1 M urea and 1 M CaCl2 was
transferred to initiate cementation. The injection procedure
was correspondingly fulfilled in the remaining 0.5 pore vol-
ume of soil to complete 4 layers of reagent and bacteria based
on the percolation method (Cheng and Cord-Ruwisch2012).
This treatment was periodically repeated (every 24 h) for 3
days to ensure acceptable improvement in the strength of soil
specimens. The biologically treated samples were allowed to
be air-dried for about 10 days in the laboratory condition. The
treated samples were then extruded from the cubic molds.
Finally, the samples were carefully prepared for direct shear
testing. The direct shear tests were conducted under several
normal stresses (55 kPa, 111 kPa, and 222 kPa) and were
continued until reaching 10% of shear strain, in compliance
with ASTM D3080 (Amini Kiasari et al. 2019). The speci-
mens were deformed at the continual rate of displacement (0.6
mm/min).
Methods of modeling
In this study, three modeling methods, namely MLR, ANFIS,
and GP, were carried out to predict the urease activity using
MATLAB R2020b software. For this purpose, the experimen-
tal design based on response surface methodology (RSM) was
applied in four main variables (CSL, urea concentration, time,
and nickel supplementation). Table 1 indicates the range of
models’ input parameters. A total of 31 runs were designed by
a central composite design (CCD) based on RSM which are
presented in Table 2.
Multilinear regression (MLR)
MLR is generally adopted to make predictions about a target
(dependent) variable through the use of several independent
variables. This technique estimated a correlation between in-
dependent (CSL, urea concentration, time, and nickel supple-
mentation) and dependent variables (urease activity) using a
linear polynomial. Notwithstanding the absence of a percepti-
ble physical association among the variables, the variables can
be interrelated via a mathematical correlation. Even though
this function is physically senseless, it can be significant for
forecasting a variable value as far as the data related to other
variables (Asadzadeh et al. 2019; Bingöl et al. 2013). The first
and second orders of MLR modeling methods (linear and
quadratic methods) were carried out. The MLR models were
 Environ Sci Pollut Res

Fig. 1 Preparation of samples for

direct shear measurement and
injection procedure

obtained using least squares. For this purpose, the “regress” trained with both hybrid and backpropagation methods, and
function was used in MATLAB R2020b software. the hybrid method had a better performance than
backpropagation.
Adaptive neuro-fuzzy inference system (ANFIS)

Adaptive neuro-fuzzy inference system (ANFIS) is the hybrid
of a Takagi-Sugeno fuzzy system with an artificial neural
network. Since this system integrates neural networks and
concepts of fuzzy logic, it can benefit from the facilities of
both methods in one mold. Its compatible system is in accor-
dance with the set of if-then fuzzy rules which could learn to
estimate complicated functions. Therefore, ANFIS is known
as a global estimation operator (Khajeh and Modarress 2010;
Rahman et al. 2012). Herein, a Sugento type of ANFIS model
has been also adopted to model the urease activity. The
ANFIS models have 4 inputs (CSL, urea concentration, time,
and Ni supplementation), and each input has 2 “guassmf”
functions. So, the ANFIS models had 16 rules totally
(2rules4inputs = 16) (Bingöl et al. 2013). The training method
was selected by trial and error. The ANFIS models were
Genetic programming (GP)
Genetic programming (GP) is recognized as being a category
of evolutionary algorithms. In GP, computer programs, which
are expressed as a tree structure with dynamically convertible
shapes and sizes, are developed so as to solve a problem
(Kiadehi et al. 2020). Starting with a preliminary population
of programs, which are generated at random, GP brings the
progressively breeding of tree population on the basis of the
natural selection (Darwinian principle) and genetic operations.
In a GP population, programs (individuals) consist of func-
tions and terminals. Functions, which are identified within the
problem domain, probably include standard arithmetic opera-
tions (e.g., +, −), conditional operators (e.g., if, for), and
problem-specific functions (e.g., sin, exp). Terminals are

Fig. 2 Gradation curve of sieved 100

Tabriz sand
90
Cumulative percentage passing [%]

80

70

60

50

40

30

20

10

0
0.01 0.1 1 10

Sieve size [mm]

Environ Sci Pollut Res

Table 1 The range of the important parameters for urease activity individual in solving the problem is indicated by the fitness
Parameter Minimum Maximum Step value for a given situation. Once the preliminary population
has been created, several parents are selected from the popu-
CSL (% v/v) 1 5 1 lation according to fitness measure. Then genetic operators,
Urea (g/L) 0 10 2.5 namely crossover and mutation, are employed on the parents
Time (h) 20 60 10 aimed at forming a new generation, which is typically fitter
Ni (μM) 0 10 2.5 than the earlier one. This process continues to proceed until
the stop criterions are fulfilled (Koza et al. 2002).
The main objective of GP is developing a mathemat-
ical formulation for predicting the enzymatic activity of
mostly in the format of variables (e.g., external inputs) or urease. The input variables are CSL, urea concentration,
constants (Koza and Koza 1992). time, and Ni supplementation. The constraints of input
Each individual surrounded by this population is later ex- variables are given in Table 1. The fitness function of
amined using a predefined fitness function, which is problem GP is the difference between experimental UA and re-
specific. In other words, the ability of the corresponding sults of GP model, and the objective function is mini-
mizing the fitness function. The GP parameters were
organized as detailed in Table 3. Most properties of
Table 2 The RSM-designed experiments with the observed responses GP such as function set, parent selection method, cross-
Run CSL Urea (g/L) Time (h) Ni (μM) UA (mM urea min–1) over and mutation methods, max depth, and crossover
(% v/v) and mutation probability are based on a previous study
of the authors (Azarhoosh et al. 2019). But about the
1 4 2.5 30 7.5 2.30
population size, the GP program was run in different
2 3 5 40 5 2.20
population sizes. In a small population size (i.e., 50),
3 2 7.5 50 2.5 1.60 the output of the program was not the optimum solu-
4 1 5 40 5 1.35 tion. With an increase in the population size, the accu-
5 2 2.5 30 2.5 1.55 racy of the GP model increased as well. Although the
6 4 7.5 30 2.5 1.50 population size was bigger than 100, the accuracy had
7 4 7.5 50 7.5 2.49 no meaningful change. So, a population size of 100 was
8 3 5 40 5 2.00 chosen with crossover probability of 0.75 and mutation
9 4 7.5 50 2.5 2.53 probability of 0.25. The population was randomly pro-
10 3 5 40 5 2.23 duced through a maximum depth of 8. As the parent
11 3 5 20 5 1.62 selection method, tournament selection is adopted with
12 3 5 40 0 2.27 the tour size of 15. Arithmetic crossover and Gaussian
13 4 2.5 30 2.5 2.43 method were used as crossover and mutation methods,
14 2 2.5 50 7.5 1.85 respectively. Fig. 3 shows a flowchart diagram of GP
15 3 0 40 5 1.10 model (Kiadehi et al. 2020).
16 5 5 40 5 2.57
17 4 2.5 50 7.5 2.70
18 3 5 40 5 2.27 Results and discussion
19 4 2.5 50 2.5 2.90
20 3 5 40 5 2.27 Modeling results
21 3 10 40 5 0.95
22 4 7.5 30 7.5 1.17 Table 4 details the predicted model-based results by the
23 2 7.5 30 2.5 0.92 models (MLR, ANFIS, and GP) and experimentally obtained
24 3 5 40 5 2.23 results for the production of urease. To examine the accuracy
25 3 5 40 10 2.20 of these models for future researches and unobserved data,
26 2 2.5 50 2.5 1.47 experimental data were indiscriminately split into two groups
27 3 5 40 5 2.22 (train and test). To this end, data relating to 21 experiments
28 2 2.5 30 7.5 1.52 were applied as train data to describe the model, while the
29 2 7.5 50 7.5 2.00 remaining data were adopted as test data to evaluate the model
30 3 5 60 5 2.65 accuracy. The normalization of the whole data was performed,
31 2 7.5 30 7.5 1.11 and experimental values are adjusted to coded values in the
[−1, +1] range.
 Environ Sci Pollut Res

Table 3 Configuration of GP-

based models Parameter Value Parameter Value

Function set (+,−,*,/,^) Number of generations 250,000

Population size 100 Max depth 8
Parent selection Tournament selection Crossover probability 0.75
Tour size 15 Per node mutation probability 0.25

MLR modeling results In Table 5, the results of the analysis of variance

(ANOVA) for the above regression models are listed.
In this section, the linear (first-order) and polynomial (second- The parameter F in this table determines whether the
order) terms of MLR were performed for modeling the UA. proposed models can generally describe dependent var-
MLR results were as follows: iables. This parameter should be compared with the
Linear model: critical value obtained from the F distribution function.
Given the confidence level of 0.05 (α = 0.05) and the
Y ¼ 0:6698X 1 −0:2902X 2 þ 0:6135X 3 þ 0:1819X 4 −0:0899 ð3Þ degrees of freedom of 4 and 26 respectively for the
regression and residues from the F distribution function,
Quadratic model:
the critical area value is defined as equation (Azarhoosh
2 2 2 et al. 2019):
Y ¼ −0:1616X 1 −1:0556X 2 þ 0:0657X 3
2 F ≥ F ð0:05Þ ð4:26Þ ¼ 2:74 ð5Þ
þ 0:1919X 4 −0:5404X 1 X 2

þ 0:4091X 1 X 3 −0:3535X 1 X 4
þ 0:6465X 2 X 3 −0:0051X 2 X 4 þ 0:2778X 3 X 4
þ 0:7071X 1 −0:2929X 2 þ 0:5758X 3 −0:0202X 4
þ 0:2020
Comparison of the values obtained for F and the critical
value of 2.74 revealed the model was able to establish a proper
fit between the independent and dependent variables. In this
case, it can be stated that the relationship between independent
and dependent variables is not random and Eqs. (1) and (2) are
ð4Þ meaningful (Azarhoosh et al. 2019).

Fig. 3 A flowchart diagram of

GP model (Kiadehi et al. 2020)
Environ Sci Pollut Res

Table 4 Comparison between experimental and predicted values of UA the determination coefficient (R2) and the root mean
No. Data type Experimental Predicted square error (RMSE)), have been computed and detailed
in Table 6. The proposed MLR models, especially the
Linear Quadratic ANFIS GP linear form of MLR, appear to be oversimplistic and
inefficient in predicting the extent of urease enzyme,
1 Train 2.30 2.08 2.11 2.30 2.30
as highlighted in Fig. 4a. Furthermore, when comparing
2 Test 2.20 1.82 2.11 2.11 2.22
the efficiency of the MLR models in UA prediction, the
3 Train 1.60 1.56 1.71 1.60 1.52
second-order polynomial regression model (quadratic
4 Test 1.35 1.16 1.25 1.53 1.35
model) has a better performance than the linear regres-
5 Train 1.55 1.24 1.50 1.55 1.55
sion model on the basis of the aforementioned criteria.
6 Train 1.50 1.62 1.57 1.50 1.47
7 Train 2.49 2.40 2.46 2.49 2.49
8 Train 2.00 1.82 2.11 2.11 2.06 ANFIS results
9 Test 2.53 2.22 2.52 2.55 2.53
10 Test 2.23 1.82 2.11 2.11 2.22 The correlation between the ANFIS model output and the
11 Train 1.62 1.21 1.61 1.62 1.62 experimentally obtained data of UA is illustrated in Fig. 4c.
12 Test 2.26 1.64 2.32 2.06 2.27 There is a perfect agreement between the experimentally ob-
13 Test 2.43 1.90 2.44 2.41 2.44 served UA and the ANFIS model output for the testing and
14 Train 1.85 2.03 1.71 1.85 1.85 training (seen) data sets. Clearly, this consistency between
15 Train 1.10 2.11 1.35 1.10 1.10 experimental and predicted ANFIS-based data can prove
16 Train 2.57 2.48 2.65 2.57 2.57 higher accuracy of the ANFIS model compared to the results
17 Train 2.70 2.69 2.70 2.70 2.78 of the MLR models.
18 Test 2.27 1.82 2.11 2.11 2.22
19 Train 2.90 2.51 2.76 2.90 2.91
20 Test 2.27 1.82 2.11 2.11 2.22 GP results
21 Train 0.95 1.53 0.77 0.95 0.95
22 Test 1.17 1.80 1.23 1.17 1.22 GP was applied to train data set and the remaining (test data
23 Train 0.92 0.95 1.16 1.01 0.93 set) was used for validation. Here follows the list of formula-
24 Test 2.23 1.82 2.11 2.11 2.22 tions obtained by GP:
25 Train 2.20 2.00 2.28 2.20 2.18
A  ðB þ C Þ
26 Train 1.47 1.85 1.41 1.47 1.79 Y ¼ ð6Þ
D
27 Train 2.22 1.82 2.11 2.11 2.22
28 Train 1.52 1.42 1.52 1.52 1.52 X1
29 Train 2.00 1.74 2.00 2.00 1.97 1 þ X 1 þ X 3 þ X 4 23 þ 6 þ X 4
A¼3þ
 þ
30 Train 2.65 2.43 2.75 2.65 2.61
 2þX 1 343
31 Train 1.11 1.13 1.18 1.11 1.11 3 þ X1


53 117 1 þ X 3
þ 9X 3 þ
4 6 þ X1
The predicted results of the UA by the models þ   ð7Þ
(MLR, ANFIS, and GP) against those obtained experi- 2

 3 3þ 7X 1

mentally are plotted in Fig. 4 based on 31 data sets 2þX 1 11þ8X 2

4 5
(Table 4). The regression equations of MLR, ANFIS,
3þX 3
and GP models, as well as the statistical criteria (e.g.,

Table 5 The results of ANOVA

for the MLR models Source Degree of freedom (df) Sum of squares (SS) Mean of squares (MS) Fvalue

Regression 4 5.754 1.438 9.59

Error 26 3.896 0.150
Total 30 9.650
 Environ Sci Pollut Res

Table 6 Modelling capability of

different methods on the basis of Model Performance criteria Data type Regression equation
statistical criterions
Train Test Total

MLR Linear R2 0.5952 0.9298 0.5763 y=0.581x+0.693

RMSE (mM/min) 0.3633 0.4101 0.3790
Quadratic R2 0.9633 0.9481 0.9579 y= 0.935x+0.112
RMSE (mM/min) 0.1094 0.1261 0.1150
ANFIS R2 0.9965 0.9580 0.9816 y=0.948x+0.082
RMSE (mM/min) 0.0339 0.1309 0.0794
GP R2 0.9967 0.9977 0.9968 y=0.935x+0.036
RMSE (mM/min) 0.0329 0.0263 0.0310

!

 X1 X1
1 þ 2X 2 2X 2 þ þ
2X 3 2 þ X 2 þ X 3 −X 4 5 þ 2X 3 −X 4
B¼ −

 ð8Þ
1 þ X3 56X 3 5 3 þ X 3 6 þ X 2
4−2X 1 −X 2 −X 4 þ þ
4 þ X2 39 24

1
C ¼ X1 þ ! ð9Þ 0

1
2
34 4 X2
4 þ X3 X1 þ X4
2 þ X3 − D¼
7 @
7 þ X1 þ
X2
þ A ð10Þ
21 4 15 10 3


! 3þX 1 þX 2 X4
1 X4 X1 þ
þ þ X1 þ − 8
12 5 9X 3
2 þ X2 þ
7

Fig. 4 Comparison between the

measured and predicted model-
based values of UA using a linear,
b quadratic, c ANFIS, and d GP
models
Environ Sci Pollut Res

where the dependent variable Y is the dimensionless value of

UA and the independent variables X 1 , X 2 , X 3 , and X 4 repre-
sent the normalized values of CSL, urea concentration, time,
and Ni supplementation, respectively. The whole experimen-
tal data were transformed into normalized form in the [−1, +1]
range using Eq. 1. Parameters of A, B, C, and D are physically
meaningless only used to simplify the GP model. A compar-
ison plot between the GP function output (Eq. 9) and its cor-
responding experimental data of UA for testing and training
data is highlighted in Fig. 4d. It can infer from this figure that
the GP-based predictions are in obviously better agreement
with the experimental observations as compared to the MLR
and ANFIS models. It is worthwhile noting that the predicted
values by MLR, ANFIS, and GP models and real values of
UA are presented in Table 4.

Selection of the best modeling method

The best modeling technique has been here ascertained by the

predicted model-based outputs (Table 4). The obtained
model-based results revealed that ANFIS and GP as artificial
intelligence-based techniques were accompanied by a consid-
erably greater accuracy when compared to the regression
methods. As powerful tools, these advanced techniques can
be undoubtedly adopted to apply intricate functions in numer-
ous fields. Furthermore, these methods have been put forward
to develop a practical equation between criterion and input
variables (Faradonbeh et al. 2016).
However, considering both testing and training datasets,
the ANFIS model had slightly lower R2 as well as higher
RSME in comparison with the models derived from GP
(Table 6). For instance, values of 0.9580 and 0.1309 for R2
Fig. 5 The effect of CSL and Ni on UA a 2D and b 3D (urea=5 g/L,
and RMSE, respectively, demonstrate a worse prediction per- time=40 h)
formance of ANFIS for testing dataset, while these values
were achieved as 0.9977 and 0.0263, respectively, for the the experimental ranges, with the other two variables held at
GP technique. The lower degree of accuracy for ANFIS could an unvaried constant level for each plot.
be explained by the rather low number of datasets. The pre-
diction accuracy based on the genetic models was also great
Effect of corn steep liquor (CSL)
for the testing dataset (unseen) as well as for the training
dataset (seen). Accordingly, both of these modeling ap-
The effect of CSL concentration and nickel supplementation
proaches could perfectly estimate the values of the UA taken
on the production of urease at a fixed urea concentration and
to use input factors. Evidently, GP as an optimal modeling
40 h reaction time is shown in Fig. 5. As might have been
approach has been used to investigate the influences of oper-
expected, the hydrolysis of urea depends strongly on the CSL
ational parameters on the urease production.
concentration. In particular, by increasing concentration of
CSL, the activities greater than 2.4 mM urea/min are obtained.
Influence of operating parameters on MICP This can be justified by the profound influences of CSL con-
centration on culture media that not only supplies principal
To investigate the mutual interaction between the factors on nutritional requirements for the bacterial growth but also pro-
UA, 2D contour plots were used according to the GP model, motes the ureolysis (Al-Thawadi 2008).
whereas 3D response surface plots were utilized to predict UA Moreover, nickel supplementation to the nutrient solution
for various variables values. Figs. 5, 6 and 7 illustrate the is of fundamental importance for the structural integrity as
effect of the independent variables on enzyme activity, in well as the functional activity of the urease enzyme

Fig. 6 The effect of urea and Ni on UA a 2D and b 3D (time = 60 h and
CSL = 5 %v/v)
(Bachmeier et al. 2002). The results indicate that the addition
of NiCl2 (0–10 μM) as a nickel supplementation improves the
enzyme activity at low CSL concentrations (0–2% v/v),
whereas it plays a role in decreasing urease hydrolysis rate at
the higher concentration of CSL. At a low concentration of
CSL, the hydrolysis rate of urease is increased by the addition
of Ni2+ ion up to 10 μM, showing the significance of Ni
supplement on the ureolysis. On the other hand, at the con-
centrations above 2% v/v CS, urea hydrolysis is somewhat
inhibited by supplementing the media with nickel.
The apparent decrease in UA might be attributed to the
presence of various heavy metal ions (e.g., Fe, Cu, and Ni
ions) in CSL at a significant level (Hull et al. 1996). As a
consequence, nickel supplementation could lead to an inhibi-
tory effect on the enzymatic activity as highlighted in Fig. 5.
Environ Sci Pollut Res
Fig. 7 The effect of time and Ni on UA a 2D and b 3D (CSL = 3 % v/v,
urea=5 g/L)
Effect of urea concentration
The interactive effect of the urea and nickel supplementation
is provided in Fig. 6. Urea at high concentrations up to 6 g/L is
responsible for an increase in activity of the enzyme, whereas
with further increase in urea concentration, the production of
urease declines. A reasonable explanation for high tolerance
to urea may be that although no ammonium salts have been
added to all of the inoculated media, the concentration of
ammonium is constantly increasing during the course of cul-
tivation through urea hydrolysis (Eq. 1). Accordingly, an in-
cremental change in the urea concentration can be a repressive
effect on UA. This hypothesis is supported by another
evidence that the urease activity is negatively correlated
with urea concentration, particularly at higher concentra-
tions (Whiffin 2004).
Environ Sci Pollut Res

Table 7 Optimal values of the independent variables, experimental, and GP-predicted urease activity

YE concentration NH4concentration Incubation Nickel supplementation The urease activity [mM urea min–1] Error [%]
[% v/v] [g L–1] time [h] (μM)
Experimental Predicted

5 4.5 60 0 3.6 3.9 8.4

Effect of time proportionate to the biomass concentration and, there-

fore, urease activity in S. pasteurii (PTCC 1645) has
The combined influence of incubation time and nickel not been constitutively regulated.
supplementation on UA, at a fixed CSL and urea con-
centration, is presented in Fig. 7. Extended periods of Optimization
incubation result in the slight promotion trend in urease
activity yield reaching up to a maximum of 2.7 mM Herein, optimal conditions are obtained to maximize the en-
urea min–1, whereas growth yield is significantly en- zymatic activity of urease. The interval for each of the vari-
hanced as the incubation time rises. This points towards ables affecting UA is represented by Eq. (14) to (17).
the idea that a condition encouraging bacterial growth is
not principally favorable to the high production of ure- 20 h ≤ incubation time≤ 60 h ð11Þ
ase. The regulation of the UA in S. pasteurii has report- 1%v=v ≤ CSL concentration ≤ 5%v=v ð12Þ
edly been constitutive (Whiffin 2004), in contrast to this
finding that the production of urease has not been 0 μM ≤ nickel supplementation≤ 10 μM ð13Þ

Table 8 The results of comparison between utilization of different nutrient sources for urease production and this study

Nutrient source Mo. Application Main findings Ref.

Lactose mother
liquor (LML)
Commercial milk
powder or by lysed
activated sludge
Cord-Ruwisch2013)
Chicken manure effluent
(CME)-urea medium
Corn steep liquor (CSL)
medium
Food-grade yeast media
(FG-YE)
Corn steep liquor (CSL)
urea medium
Sporosarcina Biocalcification Calcite constituted 24.0% of the total (Achal et al. 2009)
pasteurii in cement mortar weight of the sand samples plugged
(NCIM 2477) by S. pasteurii, and urease production
was found to be 0.353 mM urea
hydrolyzed (min ml)–1 in LML-urea medium
Bacillus pasteurii Biocementation of When using a pH of 10 and about 0.2 M urea, (Cheng and
enriched by sand soil ureolytic bacteria developed under aerobic
using selective chemostat operation at hydraulic retention
conditions time of about 10 h with urease levels of
(high pH and high about 0.060 mM urea hydrolyzed (min ml)–1
ammonia culture
concentration)
Bacillus pasteurii Biocalcification in The highest urease production (0.016766 mM urea (min mg (Yoosathaporn et al.
(KCTC 3558) cement cubes protein)–1) was obtained. The bacterial cultivation cost 2016)
reduced by more than 80%. The density of bacterial cement
cube was 5.1% higher than control, and the compressive
strength of cement mixed with bacterial cells increased up to
30.2% compared with control
Bacillus sp. CT5, Biocalcification Addition of CSL medium had no adverse effect on the setting (Joshi et al. 2018)
isolated by us from in concrete characteristics of cement paste. The urease activity was not
the cement sample reported
Sporosarcina Biocalcification A urease activity (14.77 mM urea hydrolysed min–1) was (Omoregie et al.
pasteurii NB28 in falcon tubes obtained in FG-YE medium. The food-grade yeast extract can 2019)
(SUTS) containing serve as a potential candidate for bacterial cultivation in
cementation MICP application from the perspective of cost reduction
solution
Sporosarcina Biocementation of Under the optimum conditions optimized by GP method The present study
pasteurii (PTC sand soil (5%v/v, 4.5 g L–1, 0 μM, and 60 h for CSL and urea
1845) concentration, nickel supplementation, and incubation time,
respectively), the UA has been achieved to a value as high as
3.6 mM min–1
 Environ Sci Pollut Res

Fig. 8 Representative stress- 450.00

Biotreated _222 kPa Biotreated _111 kPa Biotreated _55 kPa
strain correlation of bio-treated
and untreated sand 400.00 Untreated_222 kPa Untreated_111 kPa Untreated_55 kPa

350.00

300.00

Shear stress (kPa)

250.00

200.00

150.00

100.00

50.00

0.00
0.00 2.00 4.00 6.00 8.00 10.00 12.00

Horizontal displacement (mm)

0 g=L ≤ urea concentration ≤ 10 g=L ð14Þ concentration, incubation time, and nickel supplementation
are set to 5% v/v, 4.5 g L–1, 60 h, and 0 μM, respectively
As stated in the previous section, by increasing the CSL
(Table 7). The experimentally obtained maximal enzyme ac-
concentration and incubation time, the UA raises. Thus, to
tivity (3.6 mM urea min–1) is in good agreement with the
achieve optimality, CSL concentration and incubation time
estimated UA by GP model.
must be at the maximum value. However, as urea concentra-
The results of comparison between utilization of different
tion rises, the UA first increases and then decreases. For nickel
nutrient sources for urease production and this research are
supplementation, the trend is quite reversed. To calculate the
presented in Table 8. It should be noted that a precise com-
optimum value, the UA variation diagram in terms of urea
parison between the results is impossible due to the difference
concentration and nickel supplementation is plotted in Fig.
in microbial spices and also the difference in experimental
6. As highlighted in this figure, the maximum UA (3.9 mM
conditions. Furthermore, almost all previous works have
urea min–1) can be attained as the values of CSL, urea

Fig. 9 Summary of peak and 300.00

residual shear strength envelopes Biotreated _Peak Untreated Sample Biotreated_Residual
of bio-treated and untreated sand
250.00
peak = 0.6155 + 130.84
R² = 0.9782
Shear stress (kPa)

200.00

residual = 0.7676 + 16.386

150.00 R² = 0.9999

100.00

= 0.6392 + 5.226
R² = 0.9999
50.00

0.00
0.00 50.00 100.00 150.00 200.00 250.00

Vertical stress(kPa)
Environ Sci Pollut Res
Table 9 Direct shear test results under various vertical stresses for bio-
treated and untreated samples
Sample Normal stress
55 kPa 111 kPa
Biotreated_Peak 158.8 208.01
Biotreated_Residual 57.68 101.86
Untreated 40.7 75.7
addressed identifying alternative nutrient sources for bacteria
in microbial concrete. However, the produced urease activity
in the present study for CSL-urea medium under optimum
conditions is comparable or even better than other works.
Furthermore, and most importantly, none of these studies
has examined the application of the artificial intelligence
methodologies for modeling the economical production of
bacterial urease at high levels. Moreover, the final level of
urease activity produced on the CSL-urea medium was suffi-
cient for cementation of sandy soil. Evidently, the strengths of
soil samples are effectively increased through biocementation
process, which is discussed below.
Direct shear strength of bio-treated sand
The shear strength of a soil may be described as the magnitude
of the shear stress that a soil can withstand. The direct shear
test is recognized as being a proper experiment for qualitative-
ly evaluating the stress-strain behaviors along a thin zone of
shear failure band (Chang and Cho 2019). To compare inher-
ent parameters of shear strength, i.e., the angle of internal
friction and cohesion, the biologically treated and untreated
soils were characterized in the shear box device. The Mohr-
Coulomb criterion was used to evaluate the increase of
strength in each specimen. In the shearing process, the untreat-
ed samples were deformed in a contractive manner, whereas
the biologically treated samples had a dilative behavior similar
to dense soils. Clearly, the shear stress levels of the treated
samples were significantly higher than those of the untreated
ones. In addition, all treated samples had similar behavior to
cemented soils with peak stress points. As the soil specimens
were prepared in their loose condition, this could be
interpreted as the cementation of the soil particles by CaCO3
crystals. Figure 8 shows the shear behavior of untreated and
biologically treated soils under different normal stress levels.
MICP treatment instantly improved the peak shear strength
(τpeak) of the bio-treated soil. As the normal stress increased,
τpeak of the bio-treated samples enhanced, while the soils ap-
peared to become less dilative. Under high normal stress, the
calcite bonds between the soil particles were broken; there-
fore, peak shear stress was not observed.
The maximum shear stress improvement between bio-
treated and untreated samples with 55.5kN, 111 kN, and 222
kN were 292%, 174%, and 79%, respectively (Fig. 9). The
highest effect of treatment happened under normal stress of
222 kPa 55.5 kN. The reason for less amount of improvement for 222
264.5
kN sample can be contributed to the effect of the high vertical
stress which may break the bonds before applying shear stress.
185.77
Furthermore, differences in residual shear stress between treat-
147.29
ed and untreated specimens indicate that the porosity of sam-
ples was changed after treatment which is consistent with the
finding of Cheng et al. (2013). The reason can be related to
covering the sand particles with CaCO3 which caused the
reduction of porosity.
There is a substantial increase (42–175%) in peak shear
stress when compared to residual shear stress in bio-treated
samples. The highest peak stress increase was in a sample with
55kN normal stress. It is obvious that lower vertical stress has
minor effects on bonds before applying shear stress.
Table 9 summarizes the direct shear test results under var-
ious vertical stresses for MICP treatments. The test results
highlight that the shear strength of bio-treated samples has
been significantly enhanced in various vertical stresses.
According to the Mohr-Coulomb criterion, there are two
points of view for the failure envelope. The first one would be
taken as the peak shear stress envelope, while the second one
would be the residual stress envelope (Goodman 1989; Hoek
2007). As the peak shear stress envelope, the angles of internal
friction before and after treatment were 32.58° and 31.61°,
respectively. Although there is a decrease in shear strength
at the peak state of each specimen, the frictional angle of
treated and untreated samples remains nearly constant. This
could have happened due to evaluating the frictional angle
with reference to peak shear stress of specimens. The cohesion
parameter was improved to 130kN. An increase in cohesion
for bio-treated samples can be related to cementing bond
interlocking between soil particles. This can be consistent with
the results of Amini Kiasari et al. (2019)(Amini Kiasari et al.
2019). In the residual stress envelope, the friction angle was
also increased to 37.51°, whereas the cohesion dropped to
16.38kN. By comparing the shear envelope of peak and resid-
ual stress of bio-treated and untreated samples, it can be con-
cluded that the treatment has affected the porosity of sample
and caused the increase in both frictional angle and cohesion.
Conclusion
Bio-industrial wastes can provide dual benefits in terms of
cost reduction and environmental protection in urease-driven
MICP applications. The current study has been undertaken so
as to optimize the production of urease as the most important
stage of the MICP process using CSL by making modeling
and experimental evaluations. To this end, particular focus has

been on the application of MLR, ANFIS, and GP approaches
to model and estimate the enzymatic activity of urease. The
assessment of statistical performance indices highlighted su-
perior reliability of the artificial intelligence-based models,
especially the GP method to estimate UA by using input fac-
tors. The biological treatment has affected the porosity of
sandy soil samples and brings out the increase in both friction-
al angle and cohesion. In addition to cost-effective production
of urease, the substantial improvement in mechanical proper-
ties of bio-treated soils offers the appreciable potential of
MICP applications for geo-environmental soil management.
Nomenclature R2, Correlation coefficient; y, The value (real or normal-
ized) of the independent variable; X, The value (real or normalized) of
output variable
Acknowledgements The authors are thankful to the Department of
Chemical Engineering, Sahand University of Technology, Tabriz, Iran,
for the experimental facilities.
Acronyms list MICPMicrobial induced carbonate precipitation
CSLCorn steep liquor
UAUrease activity
MLRMultiple linear regression
ANFISAdaptive neuro-fuzzy inference system
GPGenetic programming
RMSERoot mean squared error
Greek letter list ɛRandom error
Author contribution MMK and AAM were involved in planning and
supervised the work. MMK performed the preliminary experiments to
determine effective parameters on economical urease production and car-
ried out the measurements of bacterial growth and urease activity. MMK
and SGS prepared the soil samples for bacteria injection and direct shear
testing. SGS characterized inherent parameters of shear strength of the
biologically treated soil samples and aided in interpreting the results.
MJA and AAM processed the experimental data, developed the artificial
intelligence methods for modeling the economical production of bacterial
urease at high levels, and designed the figures. MMK and MJA drafted
the manuscript. All authors read and approved the final manuscript.
Data availability All data generated or analyzed during this study are
included in this published article.
Declarations
Ethics approval and consent to participate Not applicable
Consent for publication Not applicable
Competing interests The authors declare no competing interests.
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