The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum

Mycobacterial persistence mechanisms remain to be fully characterized. Screening a transposon insertion library of Mycobacterium marinum identified kdpA, whose inactivation reduced the fraction of persisters after exposure to rifampicin. kdpA encodes a transmembrane protein that is part of the Kdp-A...

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Main Authors: Xiaofan Liu, Chuan Wang, Bo Yan, Liangdong Lyu, Howard E. Takiff, Qian Gao
Format: Article
Language:English
Published: Taylor & Francis Group 2020-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2019.1710090
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author Xiaofan Liu
Chuan Wang
Bo Yan
Liangdong Lyu
Howard E. Takiff
Qian Gao
author_facet Xiaofan Liu
Chuan Wang
Bo Yan
Liangdong Lyu
Howard E. Takiff
Qian Gao
author_sort Xiaofan Liu
collection DOAJ
description Mycobacterial persistence mechanisms remain to be fully characterized. Screening a transposon insertion library of Mycobacterium marinum identified kdpA, whose inactivation reduced the fraction of persisters after exposure to rifampicin. kdpA encodes a transmembrane protein that is part of the Kdp-ATPase, an ATP-dependent high-affinity potassium (K+) transport system. We found that kdpA is induced under low K+ conditions and is required for pH homeostasis and growth in media with low concentrations of K+. The inactivation of the Kdp system in a kdpA insertion mutant caused hyperpolarization of the cross-membrane potential, increased proton motive force (PMF) and elevated levels of intracellular ATP. The KdpA mutant phenotype could be complemented with a functional kdpA gene or supplementation with high K+ concentrations. Taken together, our results suggest that the Kdp system is required for ATP homeostasis and persister formation. The results also confirm that ATP-mediated regulation of persister formation is a general mechanism in bacteria, and suggest that K+ transporters could play a role in the regulation of ATP levels and persistence. These findings could have implications for the development of new drugs that could either target persisters or reduce their presence.
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spelling doaj-art-2ec6ea5b634942f1a047f3a588a2e6f42025-08-20T02:12:20ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512020-01-019112913910.1080/22221751.2019.1710090The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinumXiaofan Liu0Chuan Wang1Bo Yan2Liangdong Lyu3Howard E. Takiff4Qian Gao5Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College and Shanghai Public Health Clinical Center, Fudan University, Shanghai, People’s Republic of ChinaKey Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College and Shanghai Public Health Clinical Center, Fudan University, Shanghai, People’s Republic of ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, People’s Republic of ChinaKey Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College and Shanghai Public Health Clinical Center, Fudan University, Shanghai, People’s Republic of ChinaIntegrated Mycobacterial Pathogenomics Unit, Institut Pasteur, Paris, FranceKey Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College and Shanghai Public Health Clinical Center, Fudan University, Shanghai, People’s Republic of ChinaMycobacterial persistence mechanisms remain to be fully characterized. Screening a transposon insertion library of Mycobacterium marinum identified kdpA, whose inactivation reduced the fraction of persisters after exposure to rifampicin. kdpA encodes a transmembrane protein that is part of the Kdp-ATPase, an ATP-dependent high-affinity potassium (K+) transport system. We found that kdpA is induced under low K+ conditions and is required for pH homeostasis and growth in media with low concentrations of K+. The inactivation of the Kdp system in a kdpA insertion mutant caused hyperpolarization of the cross-membrane potential, increased proton motive force (PMF) and elevated levels of intracellular ATP. The KdpA mutant phenotype could be complemented with a functional kdpA gene or supplementation with high K+ concentrations. Taken together, our results suggest that the Kdp system is required for ATP homeostasis and persister formation. The results also confirm that ATP-mediated regulation of persister formation is a general mechanism in bacteria, and suggest that K+ transporters could play a role in the regulation of ATP levels and persistence. These findings could have implications for the development of new drugs that could either target persisters or reduce their presence.https://www.tandfonline.com/doi/10.1080/22221751.2019.1710090PersisterMycobacterium marinumpotassiumATPrifampicin
spellingShingle Xiaofan Liu
Chuan Wang
Bo Yan
Liangdong Lyu
Howard E. Takiff
Qian Gao
The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
Emerging Microbes and Infections
Persister
Mycobacterium marinum
potassium
ATP
rifampicin
title The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
title_full The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
title_fullStr The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
title_full_unstemmed The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
title_short The potassium transporter KdpA affects persister formation by regulating ATP levels in Mycobacterium marinum
title_sort potassium transporter kdpa affects persister formation by regulating atp levels in mycobacterium marinum
topic Persister
Mycobacterium marinum
potassium
ATP
rifampicin
url https://www.tandfonline.com/doi/10.1080/22221751.2019.1710090
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