Chemosphere 203 (2018) 139e150
Contents lists available at ScienceDirect
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
Review
Application of molecular docking for the degradation of organic
pollutants in the environmental remediation: A review
Zhifeng Liu a, 1, *, Yujie Liu a, 1, Guangming Zeng a, **, Binbin Shao a, Ming Chen a,
Zhigang Li a, Yilin Jiang a, Yang Liu a, Yu Zhang b, Hua Zhong a, c
a
College of Environmental Science and Engineering, Hunan University and Key Laboratory of Environmental Biology and Pollution Control (Hunan
University), Ministry of Education, Changsha 410082, PR China
Shaanxi Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, Shaanxi University of Chinese Medicine, Xi'an, Shaanxi 712046,
PR China
c
State Key Laboratory of Water Resources and Hydropower Engineering Science, Wuhan University, Wuhan, Hubei 430072, PR China
b
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
The theories and methods of molecular docking are summarized in
details.
The applications of molecular docking in the biodegradable mechanism
of main organic pollutants are
summarized.
The future of molecular docking and
molecular simulation in environmental remediation is discussed.
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 21 August 2017
Received in revised form
24 March 2018
Accepted 26 March 2018
Available online 27 March 2018
The molecular docking has been employed successfully to study the mechanism of biodegradation in
the environmental remediation in the past few years, although medical science and biology are the
main application areas for it. Molecular docking is a very convenient and low cost method to understand the reaction mechanism of proteins or enzymes with ligands with a high accuracy. This paper
mainly provides a review for the application of molecular docking between organic pollutants and
enzymes. It summarizes the fundamental knowledge of molecular docking, such as its theory, available
softwares and main databases. Moreover, five types of pollutants, including phenols, BTEX (benzene,
toluene, ethylbenzene, and xylenes), nitrile, polycyclic aromatic hydrocarbons (PAHs), and high
polymer (e.g., lignin and cellulose), are discussed from molecular level. Different removal mechanisms
are also explained in detail via docking technology. Even though this method shows promising
application in the research of biodegradation, further studies are still needed to relate with actual
condition.
© 2018 Elsevier Ltd. All rights reserved.
Handling Editor: I. Cousins
Keywords:
Molecular docking
Organic pollutants
Enzyme catalysis
Biodegradation
Environmental remediation
* Corresponding author.
** Corresponding author.
E-mail addresses: zhifengliu@hnu.edu.cn (Z. Liu), zgming@hnu.edu.cn (G. Zeng).
1
These authors contribute equally to this article.
https://doi.org/10.1016/j.chemosphere.2018.03.179
0045-6535/© 2018 Elsevier Ltd. All rights reserved.
140
Z. Liu et al. / Chemosphere 203 (2018) 139e150
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140
Technology of molecular docking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
2.1.
Basic theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
2.2.
Comparison of software . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
2.3.
Database . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
Molecular docking applications in biodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
3.1.
Phenols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
3.2.
Nitrile . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
3.3.
BTEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
3.4.
Polycyclic aromatic hydrocarbon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
3.5.
High polymer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
Conclusion and future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
one kind of microorganism could convert and decompose several
organic compounds due to the secretion of a variety of enzymes,
such as Pseudomonas spp., Acinetobacter spp., Nocardia globerula
spp., Bacillus spp., Phanerochaete spp., and Trametes spp. The related
results were shown in Table 1.
In recently two decades, a large group of researchers have
explored the removal mechanism of biodegradation at the molecular level (Zhang et al., 2012b; Chen et al., 2015b, 2016, 2017;
Chushak et al., 2015). Generally speaking, the biodegradation of
organic contaminants is carried out by enzymatic catalysis, which
can convert organic pollutants to small molecules and become
carbon dioxide and water eventually. In this process, the pollutants
are bound to the active site of enzymes. The catalytic center is
composed of a series of amino acids whose 3D arrangement forms
the active site that permits them to combine with substrates.
Certain active site may contain mental ion (Stubbe and Donk, 1998).
These phenomena can be described in a detail by molecular
methods (Chen et al., 2015b; Chushak et al., 2015).
People gradually pay more attention to the perniciousness of
phenol and its derivatives due to their carcinogenesis, mutagenesis
1. Introduction
Organic pollution, mainly including polychlorinated biphenyls
(PCBs), polycyclic aromatic carbons (PAHs), and hydrocarbon derivatives, has attracted more and more environmental attention.
According to the list of priority control pollutants established by
Environmental Protection Agency (EPA) in environmental sample,
BTEX(benzene, toluene, ethylbenzene and three xylene isomers),
phenols, PAHs, and nitriles are harmful to our environment (Keith
and Telliard, 1979; Zeng et al., 2013a). Owing to their volatility,
persistence, and poisonousness, it is hard to eliminate their environmental hazards by chemical, physical or biological methods
absolutely (Walker, 2001; Feng et al., 2010; Hu et al., 2011; Zeng
et al., 2013b). However, according to a further comparison in
removal efficiency and practicability, the biodegradation may be
more promising because of its advantage (Alexander, 2001), such as
breakdown completely, lower cost, and little secondary pollution
(Fan et al., 2008; Chen et al., 2015a). Until now, scientists have
found a lot of microorganisms can degrade organic matters,
including fungus and bacteria (Dua et al., 2002). Moreover, usually
Table 1
The related research progress of molecular docking for main organic pollutants in environmental bioremediation at present.
Organic
Degrading microorganism
pollutants
Docking
molecules
Phenols
Phenol
ab
Bisphenol A
Benzene
Toluene
Ethylbenzene
Xylenes
Acetonitrile
Acrylonitrile
BTEX
Pseudomonas spp.,
Acinetobacter spp.,etc
Pseudomonas spp., etc
Nitrile
Amycolatopsis spp., Nocardia globerula
spp., Bacillus subtilis spp., etc
PAHs
Pseudomonas spp., Agrobacterium spp.,
Bacillus spp., etc
High
Phanerochaete spp., Trametes spp., etc
polymer
Docking Enzymes
References
Lac MnP Nhase Nitrilase HRP LiP NDO CIP DIO DmpR AY Glucosidase TDO
Anthracene
Phenanthrene
Pyrene
Benzo[a]
pyrene
Lignin
ab ab
Cellulose
a
b
c
ab
a
acd
acd
acd
ab
ab
ab
ab
ab
ac
ac
ac
ac
ab
ab
(Zhang et al., 2012b)
(Song et al., 2014)
(Ajao et al., 2011)
(Ajao et al., 2011)
e
(Ajao et al., 2011)
(Zhang et al., 2013)
(Peplowski et al.,
2007; Yu et al., 2008)
(Jin et al., 2016b)
(Jin et al., 2016b)
(Jin et al., 2015)
(Librando and
Pappalardo, 2011)
(Chen et al., 2012)
(Khairudin and
Mazlan, 2013)
Lac, laccase; MnP, manganese peroxidase; HRP, Horseradish peroxidase; LiP, lignin peroxidase; NDO, naphthalene dioxygenase; CIP, coprinus cinereus peroxidase; DIO,
dioxygenases; TDO, toluene dioxygenase; AY, amylase; DmpR, DmpR protein.
The different letter represented mainly different interactions between enzyme and substrate. a, hydrogen bonding; b, hydrophobic interaction; c, p-p stacking; d, Van der
Waals force.
Z. Liu et al. / Chemosphere 203 (2018) 139e150
and tetratogenesis. It is found that hydrogen bond and hydrophobic
interaction can fix the position of phenol in the active pocket of
enzyme according to the molecular docking analysis (Zhang et al.,
2012b). The nonionic surfactant, such as Triton X-100, could
improve the removal efficiency of phenol by stimulating the active
group of laccase produced by Trametes versicolor (Liu et al., 2012a;
Zhang et al., 2012b). Moreover, horse radish peroxidase and
dioxygenase-catalysed are often employed to degrade phenolic
n and Esposito,
compounds on account of high efficiency (Dura
2000). Bisphenol A (BPA), is regarded as a representative
endocrine-disrupting compound to both animals and human
(Vandenberg et al., 2007; Huang et al., 2012). Molecular docking
has been applied to study the reaction mechanism. It is obvious that
OH group of BPA plays an essential role in the formation of
hydrogen bonds and p-p interactions with related enzymes or
protein (Liu et al., 2010a; Zhang et al., 2010, 2012a; Babu et al., 2012;
Yang et al., 2013; Jayakanthan et al., 2015; Makarova et al., 2016).
Benzene series, such as BTEX, mainly relied on p-p interactions and
Van der Waals interactions to combine with related enzymes, such
as naphthalene 1,2-dioxygenase and catechol-2,3-dioxygenase
ska et al.,
(Carredano et al., 2000; Ajao et al., 2011; Wojcieszyn
2012; Chushak et al., 2015). Nitrile, a chain compound without
benzene ring, is a kind of high toxic substance. It is found that water
molecules, metal ion, and amino acid residue of degrading enzyme
make it possible to disintegrate nitriles in the process of biodegradation by using molecular docking technology (Peplowski et al.,
2007; Ma et al., 2008; Yu et al., 2008; Zhang et al., 2013). Contrary to Nitrile, PAHs are typical multiple-ring organic pollutants.
Some investigations also indicated that two adjacent carbon atoms
of the benzene ring are the beginning of reaction with dioxygenase
and close to the center of active site of enzymes (Librando and
Forte, 2005; Librando and Pappalardo, 2011, 2013; 2014; Jin et al.,
2015). High polymer, such as lignin and cellulose, formed by the
monomers, was decomposed via lignin peroxidase, manganese
peroxidase or laccase (Chen et al., 2012; Khairudin and Mazlan,
2013; Awasthi et al., 2015; Recabarren et al., 2016). The related
research progress of molecular docking for various organic pollutants in environmental bioremediation is illustrated in Table 1.
Numerous review papers have been published with respect to
the process of biodegradation to many kinds of pollutants (Haritash
and Kaushik, 2009; Huang et al., 2012; Ukiwe et al., 2013). Most of
these studies paid attention to the summary of degrading microorganisms and various environmental factors (Haritash and
Kaushik, 2009), but few review papers focused on the application
of molecular docking in environmental remediation. None of them
comprehensively discussed the importance of molecular docking in
biodegradation, especially the interactions between organic pollutants and degrading enzymes. Therefore, the objectives of this
study are to summarize the application of molecular docking and
analyze the specific interactions from molecular level. This review
points out that molecular docking will play more and more
important roles in biodegradation in the future.
2. Technology of molecular docking
2.1. Basic theory
Molecular docking is a method which finds out the preferred
orientation of one or more molecules in the active sites of proteins
(Lengauer and Rarey, 1996). The best conformation will be selected
by scoring functions, while the docking generated a series of
possible complex. At the same time, the preferred orientation in
turn may be used to predict the binding affinity. Molecular docking
is frequently employed for drug design because it has the ability of
predicting the optimal conformation between small molecules and
141
the binding sites of protein (Alonso et al., 2006). Characterization of
the binding structure plays a great role in the reasonable design of
drugs as well as clarifying essential of biochemical processes
(Kitchen et al., 2004).
Complementarity is the main principle of molecular docking.
There are two key parts including geometry and energy in the
process of docking. The view of geometric complementary points
out that protein and ligand match descriptors of topographical
features to generate favorable configuration. For example, in order
to explain the enzyme's catalytic mechanism, Emil Fischer et al.
(Fischer, 2006) thought that both enzyme and the substance
possess geometric complementary shapes to fix one into another in
1894, namely “lock-and-key” model (Stryer et al., 2002). Although
the model can explain the combined selectivity of enzymes
reasonably, it fails to explicate the stabilization in the transition
state of the enzyme reaction. Until 1958, Daniel Koshland (Jr, 1995)
suggested that the initial interaction between substrate and
enzyme is very weak, but these interactions gradually induce the
changes of enzyme conformation that strengthen substrate binding
affinity, namely induced fit, which is shown in Fig. 1(A). In this case,
the configuration and direction of the substrate are changed so that
the complex become more approximately stable during transition
state (Purves, 2000). In fact, the shape of active site will continue to
be changed until the substrate is entirely bound, the final structure
and charge distribution are confirmed (Boyer, 2002).
There are many affinities between substrate and enzyme, which
contains ionic interactions, hydrogen bonding, hydrophobic interaction, and Van der Waals force, etc. Usually, hydrogen bonding is
formed by a hydrogen atom attached to a high electronegative
atom, such as oxygen, and nitrogen (Cleland, 2010), playing a vital
role in keeping up the stability of interactions. Ionic interactions
involve the attraction of ions or molecules with opposite charge,
and are a strong force among molecule in electrostatic interactions.
For instance, ionic interactions can maintain thermostability in
protein (Vetriani et al., 1998). The van der Waals belongs to the
repulsive or attractive forces between molecular entities different
from the formation of ionic bonds, nor covalent bonds (Mc Naught
and Wilkinson, 2012). Hydrophobic interactions, representing the
relations between hydrophobes and water, are weaker interactions
during the inner molecules or molecules. Hydrophobes, usually
composed of long carbon chains that didn't interact with water
molecules, are non-polar molecules. Hydrophobic interactions are
also significant for the stability of spatial structure and biological
activity, because the hydrophilic surface of proteins will become
small and it decreases the bad interactions with water (Chang,
2005; Atkins and De Paula, 2006).
As shown in Fig. 1(B), the organic pollutant (such as phenol) will
enter into the active pocket of enzyme during the process of
biodegradation starting. Additionally, the posture of substrate is
changed in order to reach an optimal situation by hydrophobic
interaction (the arc, orange), electrostatic force (sign, blue), and
hydrogen bond (dashed, light green), etc. The hydrophobic interaction is formed through the neighboring residues of amino acid,
while the difference of electronegativity results in the formation of
hydrogen bond. Therefore, molecular docking can express the
interaction, and analyze the reaction mechanism in enzymatic
reaction.
2.2. Comparison of software
Molecular docking depends on the professional software
running on the computer with the windows or linux operating
system. It tries to form the structure of the intricate combination
between two or more monomer molecules. Although there is a
great deal of software to be employed in molecular docking, they
142
Z. Liu et al. / Chemosphere 203 (2018) 139e150
Fig. 1. The model structure of ligand-receptor in the active site.
are different in function or accuracy. The software mainly includes
DOCK (Allen et al., 2015), AutoDock (Morris et al., 2009), AutoDock
Vina (Trott and Olson, 2009; Tanchuk et al., 2016), FlexX
(Schellhammer and Rarey, 2004), GOLD (Verdonk et al., 2003),
Surflex (Jain, 2003, 2007) and Molegro Virtual Docker (Thomsen
and Christensen, 2006). With the fast development of computer
science, the software is improved frequently to satisfy with the
human requirement in feature and Graphical User Interface (GUI).
As shown in Table 2, some main types of software are introduced
for molecular docking in applications. These types of software
carried out the inequable algorithm, and had different accuracy.
DOCK, using a geometric matching algorithm to fix the ligand
onto the center of the binding pocket, is a rigid docking method.
Some important features that enhanced the search algorithm's
capacity to find out the lowest-energy binding model, involving
force-filed based on on-the-fly optimization, scoring function, a
docking algorithm of alterable ligand and a matching algorithm of
fixed molecules, have been added into previous editions over the
years. Nowadays, DOCK 6.8 is the latest version. Many new features
have been added in this version. AutoDock is an automated docking
software. It can be used easily by little interoperation. Some small
molecules, such as drug candidates or substrates, bind to the active
cavity of the known three-dimensional structure by this tool.
AutoDock actually is composed of two main programs, including
autodock and autogrid, of which the autodock program carries out
the process of the ligand to virtual grids showing the target protein.
The autogrid program will calculate these grids in advance. AutoDock Vina, a new generation of molecular docking tool, is based on
AutoDock from the Molecular Graphics Lab. It significantly improves the accuracy of the docking model, also has a faster speed
than the previous AutoDock because AutoDock vina can use multiple CPU cores or CPUs to speed up the efficiency of docking. FlexX
uses an incremental construction algorithm to dock between receptor and ligand, which consists of three phases including base
placement, base selection, and complex construction (Rarey et al.,
1996). GOLD, a highly configurable program, allows the user to
make full use of the information of ligand-protein system so as to
maximize docking performance. It employs an advanced methodology which is able to avoid the high computational overhead of
ligands into multiple receptor proteins, simultaneously docking
with GOLD also settles the difficulty of model selection (Hartshorn
et al., 2007). Surflex-Dock integrates the most advanced speed,
accuracy, and availability for high throughput virtual screening. It
employs an improved scoring function and a Search Engine relying
Table 2
The algorithm and accuracy of docking software.
Software
Algorithm
Accuracy
Cost
References
DOCK
MolDock
AutoDock
PythDock
AutoDock Vina
FlexX
GOLD
Surflex-Dock
Molegro Virtual Docker
Geometric matching
Guided differential evolution
Lamarckian Genetic
Particle swarm
Broyden-Fletcher-Goldfarb-Shanno
Incremental construction
Genetic
Molecular similarity-based search
MolDock SE
e
87%
42%
e
80%
58%
78%
76%
87%
free
free
free
free
free
pay
pay
pay
pay
(Allen et al., 2015)
(Thomsen and Christensen, 2006)
(Morris et al., 2009)
(Chung et al., 2011)
(Trott and Olson, 2009)
(Schellhammer and Rarey, 2004)
(Verdonk et al., 2003)
(Jain, 2007)
(Storn and Price, 1997)
Z. Liu et al. / Chemosphere 203 (2018) 139e150
143
Table 3
The main websites of database and related information.
Main database
Website
Type
The number of molecular
structure/million
Ref.
PubChem
https://pubchem.ncbi.nlm.nih.gov/
http://zinc15.docking.org/
http://www.ebi.ac.uk/
http://www.rcsb.org/pdb/home/home.do
https://www.ncbi.nlm.nih.gov/
http://www.chemspider.com/
http://www.chemdb.com/
1.2
94
235
100
e
1.2
e
50
5
(Wang et al., 2017)
(Kim et al., 2016)
ZINC
EMBL
RCSB
NCBI
ChemSpider
ChemDB
BioAssay
Compound
Substance
Chemical
Gene, Protein and Chemical
Protein
Gene, Protein and Chemical
Chemical
Chemical
on the surface molecular similarity. Molegro Virtual Docker (MVD),
a high-quality docking program, uses MolDock SE algorithm to
achieve the screening of the optimal protein-ligand complex. According to previous reports (Thomsen and Christensen, 2006), the
accuracy of FlexX, Surflex, GOLD, Glide, and MVD is 58%, 76%, 78%,
82% and 87%, respectively.
2.3. Database
It is of great importance for molecular docking to obtain the
molecular structure which the researchers want to dock. Therefore,
how to gain ligand and receptor from the website or experiment is
necessary. According to the previous references, several main
websites, which used frequently and possess a powerful database,
are listed as shown in Table 3. For example, the receptor usually is
downloaded from these sites, such as the Research Collaboratory
for Structural Bioinformatics Protein Date Bank (RCSB PDB), the
European Molecular Biology Laboratory (EMBL) and the National
Center for Biotechnology Information (NCBI), etc. The ligand can be
derived from the PubChem Compound Database, the ChemSpider
Database, and the ZINC Database, etc. From these databases, the
generally used data of protein and small molecule compound can
be obtained. However, some specific structures of molecule might
not be found. Therefore, ChemDraw, a type of powerful software in
chemistry, will be employed to draw molecular two-dimensional
(2D) and three-dimensional (3D) structures. How to utilize the
database is very crucial. These web-sites and tools play a significant
role in molecular science. At the same time, the database of bioinformatics will be further perfected by experiment or simulation.
However, it is lack of 3D structure of receptor but with 2D or
amino acid sequence for research. In this case, perhaps homology
modeling (Schwede, 2003) can solve the problem. Homology
modeling, also called comparison-based modeling of protein, refers
to building similar molecular model of the “receptor” protein from
its gene sequence data and a laboratorial three-dimensional
structure of a correlative homologous protein as “template”
(Cavasotto and Phatak, 2009). It depends upon the recognition of
those known protein structure which might be similar to the
structure of needed query sequence, matches the corresponding
residues in this query sequence to known residues in the template.
What's more, this method is likely to produce high-accuracy and
quality structural model if the template and target are closely
matched via the comparison of gene sequences (Schwede, 2003).
3. Molecular docking applications in biodegradation
3.1. Phenols
Phenols are typically classified into two main types on the basis
of the number of phenol units, including polyphenols and simple
phenols. Phenols are not only synthesized industrially, but also
(Sterling and Irwin, 2015)
(Hingamp et al., 2004)
(Rose et al., 2017)
(Coordinators, 2016)
(Pence and Williams, 2010)
(Chen et al., 2007)
produced by plants and microorganisms (Hattenschwiler and
Vitousek, 2000; Khoddami et al., 2013). They would accumulate
in surface water, ground water and soil when released into the
environment (Gianfreda et al., 2003). Generally, microorganisms
can be applied to water treatment with phenol pollution, such as
Pseudomonas spp. and Acinetobacter spp. (Nair et al., 2008). Phenol
is an important chemical raw material, and is widely used in
bakelite, oil, coke, spinning, dye, pesticides, and medicine. It is one
of the main pollutants in above mentioned industrial waste water.
Phenol and its vapors are erosive to the respiratory tract, the skin,
and the eyes (Amp, 1996). Its corrosivity influencing on mucous
membranes and skin is due to protein denaturation (Franz et al.,
2016).
Actually, enzymes are the main reactants in the process of
biodegradation. In order to study the interactions between enzyme
and phenol at the molecular level, some simulation technology has
been adopted. Nowadays, with the development of science and
software technology, molecular docking approach has been used to
analysis the interactions between substrates and enzymes, such as
laccase with phenol, by many researchers (Zhang et al., 2012b).
Recently, some molecular docking results (Fig. 2(a)) indicated
that the phenol formed hydrophobic interactions and hydrogen
bonds with laccase in the binding pocket (Zhang et al., 2012b). The
surface of microorganism can't effectively contact with hydrophobic organic contaminants in aqueous phase (Zeng et al., 2011).
However, adding specific surfactants can reduce the toxicity of
phenol to cell and increase the phenol removal rate while using
Candida tropicalis as degrading bacteria (Liu et al., 2010b, 2011,
2012b; Zeng et al., 2011). Besides, the bioavailability improvement
is due to the formation of aggregation composed by surfactants and
pollutants in water environment (Zhong et al., 2014; Liu et al., 2017;
Shao et al., 2017). More importantly, further study showed that
surfactants, such as Triton X-100, only constituted hydrophobic
interactions with laccase by molecular docking (Zhang et al.,
2012b). So this situation may heighten the enzyme's activity and
accelerate the rate of reaction. The DmpR protein, from Pseudomonas putida and definitely controlled and regulated the expression by the total derived methyl phenol (dmp) operon, acted as
receptor to dock with phenol. Autodock Vina software was used to
study the probable binding model (Ray and Banerjee, 2015). The
results showed that all of them had aromatic stacking with Phe50
(abbreviation of amino acid plus its number, the same as below)
residue. Besides, the benzene ring of phenol was deemed to have
effect on the benzene ring of phenylalanine through p-p stacking.
Of course, horseradish peroxidase (HRP) is also used to deal with
wastewater which containing phenols and has the potential to
remediate the environmental problem that contaminated with an
array of persistent pollution (Tang et al., 2008; Alemzadeh and
Nejati, 2009; Kalaiarasan and Palvannan, 2014). Research also
illustrated that there was the maximum binding distance between
HRP and phenol (7.05 Å) than other four hormones including 17b-
144
Z. Liu et al. / Chemosphere 203 (2018) 139e150
Fig. 2. The results of molecular docking about phenol and Nitrile(a) Binding modes between laccase and phenol. Reprinted with permission from Ref. (Zhang et al., 2012b).
Copyright 2012 Elsevier. (b) A result of docking acrylonitrile and acryloamide into Nitrile hydratase. Reprinted with permission from Ref. (Peplowski et al., 2007). Copyright 2007
Springer-Verlag.
estradiol, estrogens estrone, 17a-ethinylestradiol and estriol (Cheng
and Harper, 2012). It seems that binding energy and distance have
great effects on the combination of enzyme and substrate than
molecular volume. The HRP interactions with plant-based phenolic
substrates (PBPCs) were also analyzed by the molecular docking
(Williams and Harper, 2015). It suggested that electrostatic interactions between the carboxylic group of the substrate and Arg38
compensated for weaker hydrogen bonding interactions between
the phenolic hydrogen of the substrate and His42. The binding
interactions of HRP and PBPCs are often stabilized by non-active
site interactions with Asp150 and Ser151. Coprinus cinereus peroxidase (CIP), the same as HRP, belongs to peroxidases. It was widely
used due to special selectivity toward alkyl phenols and the faster
reaction rate (Ikehata et al., 2005; Kim et al., 2005). There are three
hydrophobic residues (Pro156, Leu192, and Phe230) situated at the
entrance of the binding pocket of alkyl phenols and CIP based on
docking study (Park et al., 2011). It was found to be considerable in
the orientation of hydroxide radical and the interactions of alkyl
phenols.
Phenols are easily oxidized by the microorganisms in the natural
environment to translate all kinds of metabolites. Toluene dioxygenase (TDO) can transform the substituted phenol substance into
other products, such as chiral cyclohexenone cis-diol, hydroquinones, and catechols, etc. Although the structure of phenol substance is similar, such as o-cresol, m-cresol, and p-cresol, the ratio
of biotransformation is widely varied. It was found that the elliptical area of TDO, composed of amino acids His311, Gln215, and
Asp219, was divided into polar and hydrophobic region. The
phenolic hydroxyl group was firstly combined with His311 and
Gln15 in the binding site by hydrogen bond, that is, the type and
position of the substituent group had a great effect on the forma€ ring et al., 2016). In addition,
tion of transient intermediates (Ho
whether having dioxygen can impact the formation of hydrogen
bond between enzyme and substrate. The facts proved that many
organic matters with forms of benzene and OH are easier to form
hydrogen bonding than without it (Li et al., 2012). However, phenol
was able to substitute for cyclin E to combine with cyclindependent kinases via docking study, which was an effective inhibitor for cyclin E in the cell metabolism and cell cycle (Wang et al.,
2016). Therefore, decreasing the toxicity of phenol is tremendous
significance in wastewater treatment. Hemocyanins can transport
oxygen throughout the bodies of some invertebrate animals. Molecular docking studies demonstrated that the c-terminal b-domain
very close to the active site of this protein and have an effect on
degrading capability of the phenolic substance. The total binding
affinity to the active site of hemocyanins became stronger while
removing the c-terminal b-domain. Thus, the steric hindrance to
phenolic substance is more likely to associate with the existence of
b-domain in the hemocyanins. Furthermore, they have adopted
molecular dynamics (MD) simulation to show that sodium dodecyl
sulfate (SDS) can improve active site access by replacing the cterminal b-domain to enhance the binding of phenolic substance
and hemocyanin (Naresh et al., 2015). Perhaps, it is an effective
method that using specific chemicals to replace some constituents
of complicated protein for exploring the mechanism between
protein and ligand.
Bisphenol A (BPA, 2, 2-bis(4-hydroxyphenyl)-propane), containing two hydroxyphenyl groups, is an organic synthetic
Z. Liu et al. / Chemosphere 203 (2018) 139e150
compound with the chemical formula (CH3)2C(C6H4OH)2 belonging
to bisphenols. It was used to manufacture epoxy resins and special
plastics. In 2015, approximately four million tons of BPA raw material were produced for manufacturing polycarbonate plastic,
making it become one of the highest yields of chemicals around the
world (Pivnenko et al., 2015). BPA affects reproduction, development, and growth in aquatic organisms. It has a widespread variation in reported values, but many in the range of 1 mg/L to 1 mg/L
(Agency, 2011). BPA was counted as a hormone-like chemical
compound caused endocrine disorders. The latest review of the
literature said that the potential hazards caused by BPA always
were debatable. The further research was necessary because of the
relation between BPA exposure and bad human health (Giulivo
et al., 2016). In general, BPA and its metabolites have more harmful to human health.
The molecular docking has been widely applied in the identification of chemical toxicity such as xenoestrogens and their products of degradation and was likely to become an effective way for
human to avoid environmental hazards from hormone. In order to
elucidate the mechanism of toxicity of BPA from molecular level,
many researchers are interested in the interactions of BPA and
human/animal proteins. For example, Zhang et al. (2010) studied
the interactions of BPA and bovine serum albumin (BSA), and the
final result indicated the binding relation of BPA to BSA was
consistent with the partition law, BPA also stacked into the aromatic hydrocarbon groups of BSA and between nearby basic groups
of DNA via the hydrophobic interactions. Xie et al. (2010) also
illustrated that the BPA was located in the hydrophobic region of
human serum albumin (HSA) within sub-domain IIA. The existence
of hydrophobic forces plays a predominant role by investigating the
interaction of BPA and HAS. Pepsin, produced by the stomach, is one
of the major digestive enzymes in the digestive system of human
and many other animals. It can help digest proteins into smaller
peptides. BPA has an influence on the function and structure of
pepsin through the hydrogen bonds, steric contacts, and hydrophobic interactions (Zhang et al., 2012a). Moreover, the reactive site
caused by pepsin and BPA was situated in the region between
domain Ⅲ and domain Ⅰ. Jayakanthan et al. (2015) employed molecular docking to analyze the interactions of BPA and some antioxidant enzymes, including superoxide dismutase, glutathione
reductase, glutathione peroxidase, and catalase. It was found that
the binding model composed of BPA and catalase was the most
stable with the free energy of 32.103 kcal/mol and 5.536 docking score. The binding of BPA maintained fairly stable status
because of the relationship of a great deal of interacting residues.
The high correlations of the investigated compounds between
zebrafish and human receptors by comparing the toxicity of BPA
and some intermediate products of its degradation indicated that
toxic effects whose mechanism included estrogen-related receptorgamma (ERRg) and estrogen receptor-alpha (ERa) could be estimated from zebrafish studies to higher vertebrates (Makarova et al.,
2016), such as human. The method of estimation, through molecular docking calculations of attraction for the synthesized products
and its hydrolysis products to the ERa protein, showed that the
epoxy structure offered a moderate affinity to bond with hormonal
protein and formed the adverse conformation of the receptor.
Nevertheless, the hydrolysed structures of the epoxy compounds,
which had a bad effect on the human body cells, and revealed a
comparatively weak affinity to the ERa ligand binding domain in
their conformations (Zago et al., 2016). Researchers also analyzed
the active site in detail in order to comprehend the interactions of
BPA and its metabolites with the ERRg protein, the active pocket
was composed of the hydrophobic core and polar residue. And, a pp interaction was also seen between ligands and residues of protein, the stereo-chemical properties of chloro-ligand made it more
145
available to the hydrophobic region (Babu et al., 2012). Additionally,
most of BPA existed in sewage sludge (Song et al., 2014) can be
degraded by the enzyme secreted by microorganisms (i.e.,
amylase). Docking results showed that there are two hydrogen
bonds between two H atoms of BPA and the O atoms of Asp202 and
Asp161 in the binding pockets of a-amylase, which is consistent
with the binding characteristic by isothermal titration calorimetry
(Hou et al., 2017). Based on these previous studies about biodegradation of phenols by molecular docking, it is obviously clear that
the OH or H of phenolic compounds tended to form stable bonds
with the residues of enzyme secreted by microorganisms.
3.2. Nitrile
Nitrile, possessing a triple bond between carbon and nitrogen,
usually is highly toxic compound such as hydrocyanic acid and
cyanide in the natural environment. In some ways, biodegradation
is superior to chemical treatment in the effluent containing nitriles
compounds. Moreover, many microorganisms can degrade nitrile
effectively such as Amycolatopsis spp., Nocardia globerula spp., and
Bacillus subtilis spp. (Fang et al., 2015). Nevertheless, it is lack of the
mechanism research about enzymatic reaction. Judging from the
latest achievements and the outstanding literature, some groundbreaking performance also discovered from the innovator via
simulation.
The interactions between nitriles and some degrading enzymes
mainly including amidase, nitrile hydratase, and nitrilase, were
explicitly expressed by visual models (Zhang et al., 2013). Besides,
comparing the relative position of crystal water and acrylonitrile, it
is claimed that the hydroxide ion adsorbed into acrylonitrile due to
the nucleophilicity and activation (Fig. 2(b)) (Peplowski et al.,
2007). Therefore, the metal atom played an indispensable part on
the electronic receptor, namely, regarded as a Lewis acid. Moreover,
other workers have given specific steps about the biodegradation of
acrylonitrile mediated by Co-type nitrile hydratase, and found the
degrading process completely divided into three stages. Firstly, the
water molecules provide a eOH group with the cobalt ion of the
active site to form a Co2þeOH complex. Then, the oxygen atom
from this complex attacks a carbon atom of a carbon-nitrogen triple
bond belongs to acrylonitrile, which leads to the formation of a
carbon-nitrogen double bond and the connection of CeOH bond.
Finally, the hydrogen atom of the CeOH bond is despoiled by the
residue of serine. Therefore, the process has achieved the transformation from acrylonitrile to acrylamide (Yu et al., 2008)
(Fig. 3(a)). The degrading course of Fe-type nitrile hydratase is differ
from Co-type nitrile hydratase, the oxygen atom of carbonyl group
from the glutamine residue can active the H2O molecule and
participate in a chemical reaction by molecular docking and analysis (Song et al., 2007).
3.3. BTEX
BTEX, composed of benzene, toluene, ethylbenzene and xylene
isomers, is primarily produced in the process of catalytic reforming
of naphtha by petrochemical industries (Matar and Hatch, 2001).
Due to the low n-octanol/water partition coefficient (such as benzene, toluene, ethylbenzene, o-xylene, m-xylene, and p-xylene,
logKow is 2.13, 3.15, 2.69, 2.77, 3.20 and 3.15, respectively) and high
water solubility (their values are 1780, 515, 152, 175, 135 and
198 mg/L, respectively) at 20 C (Mitra and Roy, 1993), these compounds tend to be evaporated into the air spaces of the soil and
dissolved in the water phase. However, they are not damped very
much by the constituents or soil particles and can be transported
quite a long distance even in the suitable environment. Eventually,
these organic chemicals will exist in environment long time and be
146
Z. Liu et al. / Chemosphere 203 (2018) 139e150
Fig. 3. The specific steps about the biodegradation of acrylonitrile and the position of carbon atoms(a) Schematic catalysis mechanism of NHase converting acrylonitrile toacylamide. Reprinted with permission from Ref. (Yu et al., 2008). Copyright 2008 Elsevier. (b) The position of carbon atoms in the process of molecular docking.
harmful to human health.
Some reports suggested that the availability of an in silico
method, based on molecular docking and molecular similarity
search, for the identification and screening of protein with toluene.
Moreover, docking outcomes successfully showed important
binding of toluene to six proteins: histone H4, histone H3.2, DNA
polymerase, hemoglobin, serum albumin, and cytochrome P450
2E1 (Chushak et al., 2015). Catechol-2,3-dioxygenase (EC 1.13.11.2),
a typically multimeric enzyme, depends on Fe(Ⅱ) for their catalytic
ska et al., 2012) and interrupts benzene rings of
action (Wojcieszyn
some environmental pollutants such as naphthalene, xylene,
toluene, and biphenyl derivatives. Each hydrogen bond and Van der
Waals interactions occurred between catechol-2,3-dioxygenase
and substrates such as benzene, toluene, and o-xylene (Fig. 4(a)).
Interestingly, all of them had p-p stacking interaction with the
active site residue of His150 in the distance of ranges from 3.40 to
3.90 Å (Ajao et al., 2011). Practically docking technology can be
extended to the field of materials. For instance, using supercagepbased molecular docking to explore the adsorption capacity of
zeolite to benzene (Jirapongphan et al., 2006). Similarly, benzene
could be replaced by other contaminant to study their adsorption.
In brief, p-p stacking and Van der Waals interaction are predominant factors in the process of degrading BTEX by oxygenase, other
than the previous situation of phenols. Consequently, whether
there is hydroxyl may affect the reaction pathway in organic
pollution.
3.4. Polycyclic aromatic hydrocarbon
PAHs, containing both hydrogen and carbon, are composed of
two or more benzene rings, like anthracene, phenanthrene, pyrene,
and benzo[a]pyrene, etc. PAHs are further defined as lacking further
branching substituents on these ring structures and neutral, nonpolar molecules found in oil and coal. They are produced by
incomplete combustion of coal, oil, wood, tobacco, and organic
polymer compounds. They are serious environmental pollutant and
food contamination. Although PAHs are able to undergo adsorption,
decomposition, and attenuation by physical and chemical methods
(Gong et al., 2009; Xu et al., 2012), biodegradation might become
the most effective means (Haritash and Kaushik, 2009; Ukiwe et al.,
2013) to transform PAHs into H2O and CO2. Many microorganisms
play a major part in biodegradation. The mechanisms of degradation have already known from the molecular structure level.
However, from enzyme or protein aspects, it is lack of attention
paid to the interactions of receptor-ligand. Only several samples
referred to this level by gathering bioinformatics knowledge in
environmental remediation (Arun et al., 2008; Librando and
Pappalardo, 2011; Jin et al., 2015). Different species have different
removal efficiencies of PAHs. However, the pyrene was correspondingly effortless to be biodegraded through integrating
experimental analysis and simulation (Arun et al., 2008).
Through researching the dihydroxylation mechanism of pyrene
by naphthalene dioxygenase (NDO) in Rhodococcus sp. ustb-1, it
was observed that two oxygen atoms, located in the middle of
enzyme, almost parallel to the C4 and C5 (see Fig. 3(b)) of pyrene in
Z. Liu et al. / Chemosphere 203 (2018) 139e150
147
Fig. 4. The results of molecular docking about BTEX, PHAs, and high polymer(a) The molecular interactions of BTEX with Catechol 2, 3-dioxygenase. (b) The molecular interactions
of PAHs with Catechol 2, 3-dioxygenase. Reprinted with permission from Ref. (Ajao et al., 2011). Copyright 2011 Biomedical Informatics Publishing Group. (c) Interaction of laccase
with several lignin model compounds. Reprinted with permission from Ref. (Chen et al., 2015b). Copyright 2015 The Royal Society of Chemistry. (d) Image showing docked ligand
with stick representation of cellobiose (red), cellotetraose (green) and cellotriose (yellow) into the binding site of b-glucosidase. Reprinted with permission from Ref (Khairudin and
Mazlan, 2013). Copyright 2013 Biomedical Informatics Publishing Group. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version
of this article.)
three-dimensional space. It seems to indicate that the original
degradation procedure of pyrene by the dihydroxylation reaction at
C4eC5 positions in the enzyme is advisable (Jin et al., 2015), namely,
molecular docking has enough ability to estimate the reactive site.
Meanwhile, the interactions between phenanthrene and the active
point of NDO also were elucidated and similar to pyrene, both
having paralleled position in the C9eC10 (see Fig. 3(b)) and oxygen
atom (Jin et al., 2016b). The results are in agreement with another
research (Fig. 4(b)) (Ajao et al., 2011). Low bioavailability of PAHs
caused by its high hydrophobicity limits the reaction rate in the
process of biodegradation, thus it is too difficult to absolutely
degrade them. However, acquiring mutant based on the configuration of the original degrading enzyme (NDO) is a practical way to
improve bioavailability. Therefore, some scientists in the subject
have explored the influence between mutants and PAHs by molecular docking and molecular dynamics calculation. The mutants,
only changed steric relationships, could promote the formation and
minimize nuclear repulsion in an attempt to enhance degrading
capabilities (Librando and Pappalardo, 2014). Similarly, while discussing fluoranthene degradation and bond mechanism based on
the active site of ring-hydroxylating dioxygenase in Microbacterium paraoxydans JPM1, researchers have found the fluoranthene molecule was surrounded by hydrophobic residues. Two
oxygen atoms and mononuclear iron atom constituted a triangle,
and formed two hydrogen bonds with the terminal of Asn207.
Moreover, the distances of C1, C2 (see Fig. 3(b)) with O1, O2 were
2.87 Å and 2.77 Å, respectively. The chemical bonds of C1eC2 and
O1eO2 were parallel, which may lead to the reaction between
substrate and enzyme (Jin et al., 2016a).
The width/height ration of substrate is also a vital physical
parameter, notwithstanding the number of benzene rings takes
effect on the bonding energy (Librando and Pappalardo, 2011). This
result indicated that molecules have difficult combining with the
active site of enzyme when beyond the width/height ratio
threshold. Furthermore, eight mutants based on the structure of
the PAH-hydroxylating dioxygenase were studied to combine with
PAHs in order to seek out the most resultful conformation by
analyzing bond energy, root mean square deviation (RMSD), and
electrostatic potential, successfully ascertained a mutant with the
finest character (Librando and Pappalardo, 2012).
3.5. High polymer
High polymer, generally composed of many repeated subunits,
plays an essential and ubiquitous role in daily life. The number of
polymeric types is very tremendous. People have not sufficient
ability to totally utilize the natural macromolecule, such as lignin
and cellulose. Since these substances are hard to decompose in the
natural environment, researches should study the mechanism of
biodegradation by the process of enzyme catalysis in order to
design an optimal structure of enzyme for improving efficiency.
Additionally, the specific interactions could also be researched by
computer simulation to show the pivotal residues involving in the
formation of hydrogen bonds with the polymer.
148
Z. Liu et al. / Chemosphere 203 (2018) 139e150
Lignin, containing many different monomers like coniferyl
alcohol, p-coumaryl alcohol, 5-hydroxy coniferyl alcohol, and
sinapyl alcohol, is a phenolic polymeride. Lignin is particularly
important in the formation of the cell wall, especially wood and
bark, which provides plant cells with stable environment (Huang
et al., 2008). Normally, the acquirement of biofuel is based on the
degradation of a natural polymer. Therefore, lignin must be transformed to a small molecule by peroxidase, and laccase, etc (Li and
Zheng, 2017). Some theories have been determined about the
biodegradation, such as catalytic oxidation of lignin peroxidase
(LiP). Non-phenolic lignin model compounds could be decomposed
by LiP because of the interactions of the benzene free radical with
water or the hydrophilic reagent. However, laccase has the ability to
oxidize multiple types of phenolic and non-phenolic compounds
without participation of H2O2 (Piontek et al., 2002; Zhang et al.,
2007). For further study of enzymes in the degradation of lignin,
comparing the mechanism of enzymatic action from different
bacterial species can be summed up more perfect mechanism of
biodegradation. Molecular docking helps people to comprehend
the reason why the reaction rate is different by one type oxidation
enzyme from two microorganisms. Syringaldehyde, a lignin model
compound, was trapped into the active site of the laccase with
diverse depth. Of which, the one trapped the deepest position
showed the lower Michaelis constant (Km), it indicated that the
affinity between substrate and enzyme was stronger (Lahtinen
et al., 2009). Chen et al. (2012) have successfully achieved the
detection of interactions between lignin and ligninolytic enzymes
involving manganese peroxidase, lignin peroxidase, and laccase
based on the computerized simulation technique (Fig. 4(c)). It has
summarized the number and proportion of interaction force in
three complexes, finding the stability of aggregation and the
degrading capacity of enzyme can't directly be confirmed by the
binding affinity and the distance each other. Noteworthy, these
complexes will undergo the process with different time to reach a
point of equilibrium. Moreover, all the analysis of relevant parameter including Ca-RMSF, RMSD and, radius of gyration (Rg) indicated that the stability of complex with laccase and lignin model
compounds by carrying out molecular dynamics simulation (Chen
et al., 2015b). Therefore, molecular docking can reflect the relation among enzyme-substrate at a micro level.
Cellulose, an organic compound with the formula (C6H10O5)n, is
a kind of a polysaccharide composed of a linear chain of several
hundreds to many thousands of b(1,4) linked D-glucose unit
(Klemm et al., 2005). Glycoside hydrolases are often used to
degrade cellulose by interrupting its glycosidic linkage. This
enzyme includes exo-acting glucosidases and endo-acting cellulases. From molecular docking study of b-glucosidase with three
complexes, i.e. cellobiose, cellotriose, and cellotetraose, three residues, i.e. Glu167, Glu356, and Glu409, might play a vital role in the
pathway of enzymatic hydrolysis in all the three complexes
(Fig. 4(d)) (Khairudin and Mazlan, 2013). It is speculated that glutamic acid could recognize some certain configuration from polysaccharide due to its conformational freedom characteristic.
4. Conclusion and future research
During the past few years, researchers have focused on the
removal efficiency of contaminants by controlling and adjusting
reaction condition, less mentioned deeper reason such as the
transformation of enzymes. However, enzymes play a vital role in
biodegradation. Investigations on the interactions and changes
among enzyme-substrate are helpful to guide related experiments.
The interactions include hydrogen bond, hydrophobic interaction,
and electrostatic interaction, etc. This review has mainly demonstrated that molecular docking is a promising method. Molecular
docking was widely used in many research fields by virtue of its
convenience and low cost. Especially, molecular docking is able to
predict and account for the mechanism of biological reaction. With
the development of science and technology, not all advantages will
be brought for people, and a range of new pollutants need to be
solved. Molecular docking can be used for probing the characteristic of these pollutants as pre-experiments, and provides further
studies with theoretical data. Hence, molecular docking gradually is
used to explore interactions and structures, in order to develop a
new technology for predicting protein targets for chemical toxins
or more efficiently degrading environmental pollution by modifying the molecular structure in the future. In conclusion, applying
this method to research reaction mechanism will be hopeful in
environmental remediation. However, there are many challenges to
combine theory with reality because of different emphasis and
condition. Molecular docking is only a method to analyze physical
properties of substance at molecular level. It is hard to clarify
electron transfer and enzymatic reaction mechanisms at atomic
level. Therefore, quantum mechanics/molecular mechanics (QM/
MM) methods offer an attractive choice for further illuminating the
reaction mechanisms to assist molecular docking, which make it
possible to obtain optimal result (Sousa et al., 2017). The QM/MM
approach combines the advantages of the QM (accuracy) and MM
(speed) methods, hence allowing for the study of chemical processes in solution and in proteins.
Acknowledgments
The study was financially supported by the Program for
Changjiang Scholars and Innovative Research Team in University
(IRT-13R17), the National Natural Science Foundation of China
(51679085, 51378192, 51039001, 51378190, 51521006, 51508177),
the Fundamental Research Funds for the Central Universities of
China (531107050930).
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