Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides

Bacteria can evade antibiotics by acquiring resistance genes, as well as switching to a non-growing dormant state without accompanying genetic modification. Bacteria in this quiescent state are called persisters, and this non-inheritable ability to withstand multiple antibiotics is referred to as an...

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Main Authors: Minjeong Kang, Tae-Rim Choi, Soyeon Ahn, Hee Young Heo, Hyerim Kim, Hye Soo Lee, Yoo Kyung Lee, Hwang-Soo Joo, Philip S. Yune, Wooseong Kim, Yung-Hun Yang
Format: Article
Language:English
Published: MDPI AG 2022-07-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/11/8/1019
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author Minjeong Kang
Tae-Rim Choi
Soyeon Ahn
Hee Young Heo
Hyerim Kim
Hye Soo Lee
Yoo Kyung Lee
Hwang-Soo Joo
Philip S. Yune
Wooseong Kim
Yung-Hun Yang
author_facet Minjeong Kang
Tae-Rim Choi
Soyeon Ahn
Hee Young Heo
Hyerim Kim
Hye Soo Lee
Yoo Kyung Lee
Hwang-Soo Joo
Philip S. Yune
Wooseong Kim
Yung-Hun Yang
author_sort Minjeong Kang
collection DOAJ
description Bacteria can evade antibiotics by acquiring resistance genes, as well as switching to a non-growing dormant state without accompanying genetic modification. Bacteria in this quiescent state are called persisters, and this non-inheritable ability to withstand multiple antibiotics is referred to as antibiotic tolerance. Although all bacteria are considered to be able to form antibiotic-tolerant persisters, the antibiotic tolerance of extremophilic bacteria is poorly understood. Previously, we identified the psychrotolerant bacterium <i>Pseudomonas</i> sp. B14-6 from the glacier foreland of Midtre Lovénbreen in High Arctic Svalbard. Herein, we investigated the resistance and tolerance of <i>Pseudomonas</i> sp. B14-6 against aminoglycosides at various temperatures. This bacterium was resistant to streptomycin and susceptible to apramycin, gentamicin, kanamycin, and tobramycin. The two putative aminoglycoside phosphotransferase genes <i>aph</i>1 and <i>aph</i>2 were the most likely contributors to streptomycin resistance. Notably, unlike the mesophilic <i>Pseudomonas</i> <i>aeruginosa</i> PA14, this cold-adapted bacterium demonstrated reduced susceptibility to all tested aminoglycosides in a temperature-dependent manner. <i>Pseudomonas</i> sp. B14-6 at a lower temperature formed the persister cells that shows tolerance to the 100-fold minimum inhibitory concentration (MIC) of gentamicin, as well as the partially tolerant cells that withstand 25-fold MIC gentamicin. The temperature-dependent gentamicin tolerance appears to result from reduced metabolic activity. Lastly, the partially tolerant <i>Pseudomonas</i> sp. B14-6 cells could slowly proliferate under the bactericidal concentrations of aminoglycosides. Our results demonstrate that <i>Pseudomonas</i> sp. B14-6 has a characteristic ability to form cells with a range of tolerance, which appears to be inversely proportional to its growth rate.
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spelling doaj.art-a051488eb9814908af8073ec8236be742023-12-03T13:14:18ZengMDPI AGAntibiotics2079-63822022-07-01118101910.3390/antibiotics11081019Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to AminoglycosidesMinjeong Kang0Tae-Rim Choi1Soyeon Ahn2Hee Young Heo3Hyerim Kim4Hye Soo Lee5Yoo Kyung Lee6Hwang-Soo Joo7Philip S. Yune8Wooseong Kim9Yung-Hun Yang10College of Pharmacy, Graduate School of Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, KoreaDepartment of Biological Engineering, College of Engineering, Konkuk University, Seoul 05029, KoreaCollege of Pharmacy, Graduate School of Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, KoreaCollege of Pharmacy, Graduate School of Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, KoreaCollege of Pharmacy, Graduate School of Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, KoreaDepartment of Biological Engineering, College of Engineering, Konkuk University, Seoul 05029, KoreaKorea Polar Research Institute, Incheon 21990, KoreaDepartment of Biotechnology, College of Engineering, Duksung Women’s University, Seoul 01370, KoreaDivision of Infectious Diseases, Department of Medicine, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY 10467, USACollege of Pharmacy, Graduate School of Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, KoreaDepartment of Biological Engineering, College of Engineering, Konkuk University, Seoul 05029, KoreaBacteria can evade antibiotics by acquiring resistance genes, as well as switching to a non-growing dormant state without accompanying genetic modification. Bacteria in this quiescent state are called persisters, and this non-inheritable ability to withstand multiple antibiotics is referred to as antibiotic tolerance. Although all bacteria are considered to be able to form antibiotic-tolerant persisters, the antibiotic tolerance of extremophilic bacteria is poorly understood. Previously, we identified the psychrotolerant bacterium <i>Pseudomonas</i> sp. B14-6 from the glacier foreland of Midtre Lovénbreen in High Arctic Svalbard. Herein, we investigated the resistance and tolerance of <i>Pseudomonas</i> sp. B14-6 against aminoglycosides at various temperatures. This bacterium was resistant to streptomycin and susceptible to apramycin, gentamicin, kanamycin, and tobramycin. The two putative aminoglycoside phosphotransferase genes <i>aph</i>1 and <i>aph</i>2 were the most likely contributors to streptomycin resistance. Notably, unlike the mesophilic <i>Pseudomonas</i> <i>aeruginosa</i> PA14, this cold-adapted bacterium demonstrated reduced susceptibility to all tested aminoglycosides in a temperature-dependent manner. <i>Pseudomonas</i> sp. B14-6 at a lower temperature formed the persister cells that shows tolerance to the 100-fold minimum inhibitory concentration (MIC) of gentamicin, as well as the partially tolerant cells that withstand 25-fold MIC gentamicin. The temperature-dependent gentamicin tolerance appears to result from reduced metabolic activity. Lastly, the partially tolerant <i>Pseudomonas</i> sp. B14-6 cells could slowly proliferate under the bactericidal concentrations of aminoglycosides. Our results demonstrate that <i>Pseudomonas</i> sp. B14-6 has a characteristic ability to form cells with a range of tolerance, which appears to be inversely proportional to its growth rate.https://www.mdpi.com/2079-6382/11/8/1019psychrotolerant bacteriaantibiotic tolerancepersistersantibiotic resistanceaminoglycosides
spellingShingle Minjeong Kang
Tae-Rim Choi
Soyeon Ahn
Hee Young Heo
Hyerim Kim
Hye Soo Lee
Yoo Kyung Lee
Hwang-Soo Joo
Philip S. Yune
Wooseong Kim
Yung-Hun Yang
Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
Antibiotics
psychrotolerant bacteria
antibiotic tolerance
persisters
antibiotic resistance
aminoglycosides
title Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
title_full Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
title_fullStr Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
title_full_unstemmed Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
title_short Arctic Psychrotolerant <i>Pseudomonas</i> sp. B14-6 Exhibits Temperature-Dependent Susceptibility to Aminoglycosides
title_sort arctic psychrotolerant i pseudomonas i sp b14 6 exhibits temperature dependent susceptibility to aminoglycosides
topic psychrotolerant bacteria
antibiotic tolerance
persisters
antibiotic resistance
aminoglycosides
url https://www.mdpi.com/2079-6382/11/8/1019
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