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Universidade Federal de Santa Maria
Ci. e Nat., Santa Maria, v. 44, Ed. Esp. VI SSS, e17, 2022
DOI: 10.5902/2179460X68835
ISSN 2179-460X
Submitted: 8/12/2021 • Approved: 9/12/2021 • Published: 1/4/2022
Special Edition
The use of bacteria for bioremediation of environments contaminated with toluene: a molecular docking analysis
O uso de bactérias para biorremediação de ambientes contaminados com tolueno: uma análise molecular por docking
Estela Fernandes e Silva II
Karine Laste Macagnan II
Louise Vargas Ribeiro III
Tainã Figueiredo Cardoso IV
Daiana Kaster Garcez V
I Instituto Federal de Educação, Ciência e Tecnologia Sul-rio-grandense, Pelotas, RS, Brazil
II Prefeitura Municipal de Rio Grande, Rio Grande, RS, Brazil
III Universidade Federal de Pelotas, Pelotas, RS, Brazil
IV Embrapa Pecuária Sudeste, Pelotas, RS, Brazil
V Universidade Federal do Rio Grande, Rio Grande, RS, Brazil
ABSTRACT
Bacteria can be helpful organisms for environmental decontamination through bioremediation processes. Among the environmental contaminants, toluene is one of the compounds present in gasoline and can be toxic in the aquatic environment, causing significant damage to organisms in this ecosystem. The detailed understanding of the main proteins and processes involved in cellular bioremediation pathways is little explored, which encourages studies in the area to optimize these processes. The ABC transporter system is involved in the transport of a wide variety of inorganic compounds and complex organic molecules. Molecular docking (DM) is an in silico methodology in which two molecules are joined (receptor versus ligand), and the chemical characteristics of this bond are verified. possibilitando identificar espécies promissoras para a biorremediação do tolueno.Thus, through the molecular docking tool, this study aimed to evaluate the interaction between toluene and ABC transporters of bacterial species of Staphylococcus aureus and Thermotoga maritima, enabling the identification of promising species for toluene bioremediation. For the DM, UCFS Chimera software (for the elimination of heteroatoms and production of 3D images), AutoDock Tools (for preparation of proteins and toluene for docking), AutoDock Vina (for docking per se), and LigPlot + (for checking amino acids and types of binding between molecules) were used. The binding energy between ABC transporters and toluene was similar for both species, being -5.2 Kcal/mol for S. aureus and -5.5 Kcal/mol for T. maritima. The number of transporter amino acids bound to toluene differed for the two species: S. aureus bound through three amino acids, while T. maritima bound through seven amino acids. The results presented in this study demonstrate that both species evaluated are promising for in vitro and in vivo studies for toluene bioremediation.
Keywords: BTXs; Proteins; Fuels
RESUMO
As bactérias podem ser organismos úteis para a descontaminação ambiental através de processos de biorremediação. Dentre os contaminantes ambientais, o tolueno é um dos compostos presentes na gasolina e pode ser tóxico no ambiente aquático, causando danos significativos aos organismos deste ecossistema. A compreensão detalhada sobre as principais proteínas e processos envolvidos em rotas celulares de biorremediação é pouco explorada, o que encoraja os estudos na área para a otimização desses processos. Sabe-se que o sistema transportador ABC está envolvido no transporte de uma ampla variedade de compostos inorgânicos e de moléculas orgânicas complexas. O docking molecular (DM) é uma metodologia in silico na qual unem-se duas moléculas (receptor versus ligante) e verifica-se características químicas dessa ligação. Desse modo, o objetivo desse estudo foi avaliar, através da ferramenta de docking molecular, a interação entre o tolueno e transportadores ABC das espécies bacterianas de Staphylococcus aureus e Thermotoga maritima, possibilitando identificar espécies promissoras para a biorremediação do tolueno. Para o DM utilizou-se os softwares UCFS Chimera (para eliminação de heteroátomos e produção das imagens em 3D), AutoDock Tools (para preparação das proteínas e do tolueno para o docking), AutoDock Vina (para o docking per se) e LigPlot + (para verificação de aminoácidos e tipos de ligação entre moléculas). A energia de ligação entre os transportadores ABC e o tolueno foi semelhante para ambas as espécies, sendo para S. aureus -5.2 Kcal/mol e para T. maritima -5.5 Kcal/mol. O número de aminoácidos do transportador que se ligaram ao tolueno foi diferente para as duas espécies: S. aureus uniu-se através de três aminoácidos, enquanto T. maritima uniu-se através de sete aminoácidos. Os resultados apresentados nesse estudo demonstram que ambas as espécies avaliadas são promissoras para estudo in vitro e in vivo para biorremediação do tolueno.
Palavras-chave: BTXs; Proteínas; Combustíveis
Environmental pollution and contamination have grown exponentially in recent years. Among the environmental contaminants, gasoline is one of the most representative pollutants found in the soil and has in its composition a mixture that includes a variety of BTXs compounds (benzene, toluene, and xylene) (AN; LEE, 2008). Sams et al. (2004) report that the BTXs can cause severe groundwater contamination, mainly due to spills involving the release of petroleum products such as gasoline, diesel fuel, and lubricating oil and from leaking oil tank heaters. Data indicate that about 5.74 million tons of oil and oil products were spilled into marine ecosystems between 1970 and 2013 (ITOPF, 2009). The presence of the BTXs in water can cause harm to the environment and public health, even at low concentrations (SAMS et al., 2004). Among BTXs, toluene - also known as methylbenzene, is a water-insoluble homolog of benzene that is toxic in the aquatic environment and can cause significant damage to organisms in this ecosystem, affecting growth, development, and reproduction (XU et al., 2020). Li et al. (2021) explored the ototoxicity of toluene in the early development of zebrafish embryos/larvae. They found that toluene can affect the development of the inner ear and lateral line systems in zebrafish, to the point that the lateral line system may be more sensitive to toluene than the inner ear.
An alternative for controlling this compound would be the bioremediation, a process in which living organisms-usually plants, microorganisms, or their enzymes, are used technologically to remove (remediate) or reduce pollutants in the environment. Bioremediation has received attention in the past two decades as an alternative method to remove or mitigate toluene contamination in the ecosystem (OYETIBO et al., 2017). Bacteria are key organisms for bioremediation due to their rapid growth rate, ability to adapt quickly to environmental conditions, and simple growth requirements (FIELD; SIERRA, 2008; PARSEK; MCFALL; CHAKRABARTY, 1995). The first bioassay for toxicity monitoring was developed using the luminescent bacterium Vibrio fischeri in the 1970s (CLÉMENT; CADIER, 1998). The biodegradation of toluene by a microbial consortium with Pseudomonas sp., Escherichia coli, and Bacillus sp. has already been reported (RAJAMANICKAM et al., 2017). Some other examples of isolated bacteria that degrade toluene are: Pseudomonas aeruginosa AT18, Acinetobacter genospecies Tol 5, Bacterium Ex-DG74, Magnetospirillum sp. 15-1, Bacillus cereus THH39, Burkholderia sp. JS150, and Thauera sp. DNT-1 (AFROUZOSSADAT et al., 2013; HEYDARNEZHAD et al., 2018; JOHNSON; OLSEN 1997; KIM; JEON, 2009; MEYER et al., 2017; PEREZ et al., 2006; SHINODA et al., 2004).
Some of the mechanisms involved in bioremediation processes are well known, occurring through, for example, pathways such as alk (c5 to c12 n-alkanes), nah (naphthalene; PAHs) (WHYTE et al., 1997), and xyl (toluene; aromatic hydrocarbons) (NAKAI et al., 1983). Despite this, details about which proteins are involved in these pathways remain scarce. It is necessary to determine in more detail the identity of these proteins and the interaction between them, and the activation of their genes under polluting conditions (GILBERT, 2001). Regarding bioremediation, the ABC transporter system is known to be involved in the transport of a wide variety of molybdenum, nickel, arsenic, and more complex organic molecules (BEHERA et al., 2020). Behera et al. (2020) evaluated the presence of a microbial community with bioremediation potential in sediment samples from the Ganga and Yamuna Rivers (India). Through functional analysis, many bioremediation-related protein domains were found in the metagenome of the river samples, among them the ABC transporter (BEHERA et al., 2020). This mechanism was also reported in the degradation of alkaline lignin by Bacillus ligniniphilus. By comparing proteomic data and metabolomic analysis, positive regulation of the ABC transporter system was found (ZHU et al., 2017).
In silico methods are used before toxic xenobiotics biodegradation assays to find viable cultures for their application (KHAN; SAJID; CAMEOTRA, 2013). This can help decrease the time and money spent on the initial screening and identifying environmentally viable strains. Some studies have successfully applied in silico techniques involving the molecular docking to identify and study compounds/enzymes and amino acid residues involved in biodegradation (LIU et al., 2018; SRINIVASAN et al., 2019). Thus, through this tool, this work aimed to evaluate the interaction between toluene and ABC transporters of the bacterial species of Staphylococcus aureus and Thermotoga maritima, enabling the identification of promising species for toluene bioremediation.
The proteins were selected in the Protein Data Bank (PDB) by searching the term "ABC transporter." The unmutated structure of this transporter was found for two organisms: Staphylococcus aureus (PDB ID: 2HYD) and Thermotoga maritima (PDB ID: 3QF4) (BERMAN et al., 2000). The chemical structure of toluene was obtained from the PubChem database (PubChem ID: 1140) (BOLTON et al., 2008). The heteroatoms were removed from the proteins by using UCSF ChimeraX software (GODDARD et al., 2018), and with AutoDock Tools, the proteins (removing the information from water molecules, adding polar hydrogens and Kollman charges) and the toluene ligand (updating Gasteiger and TORSDOF charges) were prepared. Molecular docking analyses were performed by AutoDock Vina (TROTT; OLSON, 2010). A "blind docking" was performed, performing the complete protein's coverage and increasing the exhaustiveness parameter. The configurations present in Table 1 were used to perform the docking simulations. The PyMol software (SCHRÖDINGER, 2015) was used for conversion into PDB format and LigPlot + (WALLACE; LASKOWSKI; THORNTON, 1995) for binding analysis on specific residues.
Table 1 – Summary of the parameters used in AutoDock Vina software to molecular docking analysis
|
PDB ID |
Grid box size |
Coordinates of the center of the grid box |
Exhaustiveness |
|
2HYD |
x: 98; y: 60; z: 112 |
x: 116.899; y: 67.679; z: 142.384 |
500 |
|
3QF4 |
x: 118; y: 62; z: 82 |
x: -53.901; y: 5.998; z: 35.316 |
500 |
Source: Authors, 2021
Bioinformatic tools offer a fast and robust way to screen targets for bioremediation. The molecular docking tool can help to screen the degradation susceptibility of the pollutant by already characterized enzymes. In addition, the existence of several methodologies and software packages available for molecular docking is another critical factor, as it provides predictions coupled with good performance and speed with low computational cost (GUEDES et al., 2014). Although molecular docking studies are widely used for drug discovery, their use in predicting targets for bioremediation is still developing (SRIDHAR et al., 2013).
In this study, molecular docking analysis between bacterial ABC transporters and toluene was performed considering active site interactions. The results were examined based on binding energies, binding sites, and amino acid residues. The bacterial species showed similar binding free energy (BFE) between protein and ligand (Table 2) and < - 5.2 Kcal/mol, which may indicate a similar ability to bioremediate toluene through pathways involving the ABC protein. A BFE affinity < 0 means that a ligand and its receptor can bind spontaneously, and the lower the BFE value, the stronger the binding capacity (DU et al., 2016).
Table 2 – Binding free energy values (BFE) and amino acids (AA) involved in the interaction of the ABC transporters with the toluene
|
Specie |
PDB ID |
BFE |
AA |
|
Staphylococcus aureus |
2HYD |
-5.2 Kcal/mol |
Lys 477 (B chain); Tyr 349 e 391 (A chain) |
|
Thermotoga maritima |
3QF4 |
-5.5 Kcal/mol |
Phe 218 (chain A); Ile 141 (B chain); Phe 117 (B chain); Leu 116 e 120 (B chain); Val 195 (A chain) e 140 (B chain); |
Source: Authors, 2021
The ABC protein can be an important target, as it is a transporter that may be a determinant for the entry of toluene into bacterial cells to initiate bioremediation (ORELLE et al., 2019). The ABC protein of the T. maritima showed a FEB slightly better than of the S. aureus. In addition, the ABC protein of the T. maritima was had the highest number of amino acid residues involved in binding (Table 1). For both bacteria, the toluene was ligated near the transmembrane region (Figure 1).
The ABC transporters of the plasma membranes of Gram-negative and Gram-positive bacteria are widely different in their organization and composition (GOFFEAU; HERTOGH, 2013). However, these structural differences were minimal for the binding stability between the ABC transporter and the toluene since S. aureus (Gram-positive bacteria) and T. maritima (Gram-negative) showed little difference between the FEBs (Table 2).
Figure 1 – Toluene chemical structure binding with ABC transporter protein (generated using UCSF Chimera software)
A: ABC transporter of S. aureus; B: ABC transporter of T. maritima. In both, the toluene chemical structure is in dark gray.
Source: Authors, 2021
Staphylococcus is Gram and catalase-positive cocci, which strains grow on standard media, broth, or plain agar, with a pH = 7 and at an optimum temperature of 37°C. The distribution of S. aureus is extensive since this bacterium can significantly resist desiccation and cold (SANTOS et al., 2007). Despite being a human bacterial pathogen that causes a wide variety of clinical manifestations (TONG et al., 2015), the use of S. aureus (strain K1) in bioremediation has already been reported. Zou et al. (2014) analyzed metal-contaminated locals and reported the ability of S. aureus to resist and reduce chromium (VI) to chromium (III) and adsorb uranium (VI). Tariq et al. (2019) confirmed through biochemical and phylogenetic analyses that the S. aureus K1 strain is promising and can remove chromium from metal-polluted environments. Furthermore, biofilms produced by S. aureus - one of the structures responsible for the bacterium's pathogenicity, have been tested for uranium bioremediation ability (SHUKLA et al., 2020). Biosorption and enzymatic removal of the S. aureus biofilm played a role in remediating up to 47% of 10 ppm uranium (VI) (SHUKLA et al., 2020).
Thermotoga maritima is a hyperthermophilic Gram-negative bacterium that utilizes a vast network of ABC transporters to efficiently metabolize various carbon sources to produce hydrogen (LATIF et al., 2015). T. maritima grows anaerobically and has an optimum growth temperature of around 80 °C (HUBER et al., 1986). Being a source of thermostable enzymes and an efficient hydrogen producer, the T. maritima has great biotechnological applications (CONNERS et al., 2006). Despite this, no studies were found relating the bioremediation capacity of this bacterium. Thus, this study may be indicating a new candidate for further studies.
Environmental contaminants are a concern and have gained attention in recent years due to the consequences for the environment and human and animal health. Remediation means, methods, and technologies are needed to reverse this scenario. The use of bacteria to remediate polluted and/or contaminated sites is a great strategy. The molecular docking may represent a fast and low-cost way to aid in research for the bioremediation of hydrocarbon-contaminated locals, assisting in choosing the ideal bacterium to carry out the depollution and/or decontamination process. In this study, S. aureus and T. maritime bacteria, concerning binding on ABC transporters, demonstrated similar interaction abilities with toluene, indicating a similar capacity for bioremediation. The results presented in this study show that both species evaluated are promising for in vitro and in vivo studies for toluene bioremediation.
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Authorship contributions
1 – Eduarda Medran Rangel (Corresponding author)
PhD in Materials Science and Engineering
https://orcid.org/0000-0003-3334-5091 • eduardamrangel@gmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing
2 – Estela Fernandes e Silva
PhD in Physiological Sciences
https://orcid.org/0000-0003-3254-6916 • estela.fernandes.e.silva1234@gmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing
3 – Karine Laste Macagnan
PhD in Biotechnology
https://orcid.org/0000-0002-8643-3397 • karinemacagnan@hotmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing
4 – Louise Vargas Ribeiro
PhD in Agronomy
https://orcid.org/0000-0002-0313-1001 • louiseribeiro@hotmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Validation, Visualization, Writing – original draft, Writing – review & editing
5 –Tainã Figueiredo Cardoso
PhD in Animal Production
https://orcid.org/0000-0002-6038-7521 • tainafcardoso@gmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing
6 – Daiana Kaster Garcez
PhD in Biology of Continental Aquatic Environments
https://orcid.org/0000-0003-4526-9647 • daiana_kg@hotmail.com
Contribution: Conceptualization, Formal Analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing
RANGEL, E. M.; SILVA, E. F.; MACAGNAN, K. L.; RIBEIRO, L. V.; CARDOSO, T. F.; GARCEZ, D. K. The use of bacteria for bioremediation of environments contaminated with toluene: a molecular docking analysis. Ciência e Natura, Santa Maria, v. 44, Ed. Esp. VI SSS, e17, 2022. DOI: 10.5902/2179460X68835.