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Evaluation of Antibiotic Tolerance in Pseudomonas Aeruginosa for Aminoglycosides and Its Predicted Gene Regulations Through In-Silico Transcriptomic Analysis

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Evaluation of Antibiotic Tolerance in Pseudomonas Aeruginosa for Aminoglycosides and Its Predicted Gene Regulations Through In-Silico Transcriptomic Analysis Article Evaluation of Antibiotic Tolerance in Pseudomonas aeruginosa for Aminoglycosides and Its Predicted Gene Regulations through In-Silico Transcriptomic Analysis Abishek Kumar B 1,* , Bency Thankappan 2, Angayarkanni Jayaraman 2,* and Akshita Gupta 1 1 Department of Microbiology, Kasturba Medical College (Manipal), Manipal Academy of Higher Education (MAHE), Manipal 576104, India; [email protected] 2 Department of Microbial Biotechnology, Bharathiar University, Coimbatore 641046, India; [email protected] * Correspondence: [email protected] (A.K.B.); [email protected] (A.J.); Tel.: +91-801-521-6350 or +91-908-031-0146 (A.K.B.) Abstract: Pseudomonas aeruginosa causes chronic infections, such as cystic fibrosis, endocarditis, bacteremia, and sepsis, which are life-threatening and difficult to treat. The lack of antibiotic response in P. aeruginosa is due to adaptive resistance mechanism, which prevents the entry of antibiotics into the cytosol of the cell to achieve tolerance. Among the different groups of antibiotics, aminoglycosides are used as a parenteral antibiotic for the treatment of P. aeruginosa. This study aimed to determine the kinetics of antibiotic tolerance and gene expression changes in P. aeruginosa Citation: Kumar B, A.; Thankappan, exposed to amikacin, gentamicin, and tobramycin. These antibiotics were exposed to P. aeruginosa B.; Jayaraman, A.; Gupta, A. at their MICs and the experimental setup was monitored for 72 h, followed by the measurement Evaluation of Antibiotic Tolerance in of optical density every 12 h. The growth of P. aeruginosa in the MICs of antibiotics represented Pseudomonas aeruginosa for the kinetics of antibiotic tolerance in amikacin, gentamicin, and tobramycin. The transcriptomic Aminoglycosides and Its Predicted profile of antibiotic exposed P. aeruginosa PA14 was taken from the Gene Expression Omnibus (GEO), Gene Regulations through In-Silico NCBI as microarray datasets. The gene expressions of two datasets were compared by test versus Transcriptomic Analysis. Microbiol. control. Tobramycin-exposed P. aeruginosa failed to develop tolerance in MICs of 0.5 µg/mL, 1 µg/mL, Res. 2021, 12, 630–645. https:// and 1.5 µg/mL, whereas amikacin- and gentamicin-treated P. aeruginosa developed tolerance. This doi.org/10.3390/microbiolres12030045 illustrated the superior in vitro response of tobramycin over gentamicin and amikacin. Further, in Academic Editors: Juan M. Tomás silico transcriptomic analysis of tobramycin-treated P. aeruginosa resulted in differentially expressed and Maria Teresa genes (DEGs), enriched in 16s rRNA methyltransferase E, B, and L, alginate biosynthesis genes, Ceccherini Guicciardini and several proteins of the type II secretion system (T2SS) and type III secretion system (T3SS). The regulation of mucA in alginate biosynthesis, and gidB in RNA methyltransferases, suggested Received: 1 May 2021 an increased antibiotic response and a low probability of developing resistance during tobramycin Accepted: 20 July 2021 treatment. The use of tobramycin as a parenteral antibiotic with its synergistic combination might Published: 29 July 2021 combat P. aeruginosa with increased response. Publisher’s Note: MDPI stays neutral Keywords: adaptive resistance; antibiotic tolerance; in vitro exposure; aminoglycoside; Pseudomonas with regard to jurisdictional claims in aeruginosa; differentially expressed genes (DEGs); transcriptomic analysis published maps and institutional affil- iations. 1. Introduction P. aeruginosa is an opportunistic pathogen, which causes chronic infections that are Copyright: © 2021 by the authors. difficult to treat due to its limited response to antimicrobials and the emergence of antibiotic Licensee MDPI, Basel, Switzerland. resistance during therapy [1]. Multi-drug resistance (MDR) is increasing due to over- This article is an open access article exposure to antibiotics [2]. Drug resistance in P. aeruginosa is developed as a result of distributed under the terms and various physiological and genetic mechanisms, which include multidrug efflux pumps, conditions of the Creative Commons beta-lactamase production, outer membrane protein (porin) loss, and target mutations. Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ In hospitals, MDR P. aeruginosa are, in most cases, concurrently resistant to ciprofloxacin, 4.0/). imipenem, ceftazidime, and piperacillin-tazobactam, which limits treatment options [3]. Microbiol. Res. 2021, 12, 630–645. https://doi.org/10.3390/microbiolres12030045 https://www.mdpi.com/journal/microbiolres Microbiol. Res. 2021, 12 631 Aminoglycosides are a major group of antibiotics with a potential bacteriocidic effect for the treatment of Pseudomonas infections. They are used in monotherapy or in combina- tion with antimicrobials to treat various infections to overcome drug resistance, particularly in cystic fibrosis patients [4] and infective endocarditis [5]. In the face of systemic infection with septic shock and sepsis, antimicrobial therapy should consist of two antimicrobial agents, with one of these being an aminoglycoside [6], because it exhibits concentration- dependent bactericidal activity and produces prolonged post-antibiotic effects [7]. β-lactam antibiotic coupled with an aminoglycoside is a commonly used synergistic combination for the treatment of clinical infections. Other combinations include fluoro- quinolone and aminoglycosides, and tetracycline and aminoglycosides. Clinical isolates show a high susceptibility to aminoglycosides as compared to other first-line antibiotics [8]. Despite high susceptibility to aminoglycosides in clinical isolates, P. aeruginosa exhibits physiological adaptations to these antibiotics, which results in less response to its synergis- tic combinations. P. aeruginosa thrives in the inhibitory concentration of antibiotics and acquires adaptive resistance gradually, which makes treatment more complicated [9]. The adaptive resistance mechanism is characterized by the modification of the cytoplasmic membrane, condensa- tion of membrane proteins, and the reduction of phospholipid content [10], which reduces penetration of antibiotics into the plasma membrane. Studies show that adaptive resistance can also develop by the up-regulation of efflux pumps, especially MexXY-OprM [11]. Among immunocompromised patients, P. aeruginosa are favored to adapt to the administered antibiotics and enable better survival of the bacterial generation by emerging as physiologically resistant groups [12]. Adaptive resistance is developed due to rapid transcriptomic alteration in response to antibiotics [13]. A better understanding of the kinetics and transcriptomic changes during antibiotic exposure can develop scientific insight on the adaptive resistance mechanism in P. aeruginosa [13,14]. In light of this, our study was designed to gain a better understanding of the adaptive resistance mechanism in P. aeruginosa to the aminoglycosides gentamicin, amikacin, and tobramycin, which are commonly used as first line antibiotics. 2. Materials and Methods 2.1. Broth Dilution Method The minimum inhibitory concentrations (MICs) of P. aeruginosa ATCC 27853 was determined by the broth dilution method as per the Clinical and Laboratory Standards Institute (CLSI) guidelines. MIC assay was performed for gentamicin, amikacin, and tobramycin (purchased from Sigma Aldrich, Bangalore, Karnataka, India) with log phase culture (5 × 108 CFU/mL) in Mueller Hinton broth (MHB) using a 96-well microtiter plate. ™ The final optical density (OD600) at 600 nm wavelength was determined via an Epoch Microplate spectrophotometer (BioTek Instruments Inc., Winooski, VT, USA). 2.2. In Vitro Exposure of Antibiotics to P. aeruginosa From the observed MICs in the broth dilution method, antibiotic concentrations of 1 µg/mL, 2 µg/mL, and 3 µg/mL for amikacin and 0.5 µg/mL, 1 µg/mL, and 1.5 µg/mL for gentamicin and tobramycin were prepared separately in 10 mL of MHB dispensed in Tarsons tubes. P. aeruginosa ATCC 27853 was inoculated and the initial cell density at OD600 was adjusted to =∼ 0.26 uniformly in all the tubes. The experimental set up was observed for 72 h. The experimental condition was incubated at 37 ◦C with optimal shaking at 74 rpm. ™ Every 12 h, the turbidity was monitored by measuring the OD600 in an Epoch microtiter plate reader (BioTek Instruments Inc., Winooski, VT, USA) [14,15]. The tubes with growth were sub-cultured in nutrient agar. The colonies were confirmed for P. aeruginosa through the matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) automated identification system VITEK® MS (BioMérieux, SA, Marcy l’Etoile, France) by following the standard procedure for sample preparation [16]. Microbiol. Res. 2021, 12 632 2.3. In Silico Transcriptomic Analysis 2.3.1. Retrieval of Microarray Datasets The differential gene expression analysis was performed by exploring microarray datasets from the Gene Expression Omnibus (GEO), NCBI. The datasets which mimicked our experimental condition, P. aeruginosa exposed to an MIC of tobramycin, were avail- able as accessible series no. GSE9991 and GSE9989. Two datasets were analyzed: (1) a tobramycin-treated planktonic culture of P. aeruginosa (GSE9991), and (2) a tobramycin- treated P. aeruginosa biofilm (GSE9989). In GSE9991, a planktonic culture of PA14 was exposed to an MIC of tobramycin of 5 µg/mL for 30 min at 37 ◦C[17]. Two samples, GSM252561 and GSM252562, of tobramycin-treated PA14 planktonic culture was taken as a test, which was compared to two controls,
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