Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa

ABSTRACT The single polar flagellar motor in Pseudomonas aeruginosa is equipped with two stator systems, MotAB and MotCD, both driven by H+ ions. The torque-speed relationship for flagellar motors with two stator systems has not been explored previously. In this study, we developed a method that uti...

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Main Authors: Haolin Wu, Zhengyu Wu, Maojin Tian, Rongjing Zhang, Junhua Yuan
Format: Article
Language:English
Published: American Society for Microbiology 2024-12-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.00745-24
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author Haolin Wu
Zhengyu Wu
Maojin Tian
Rongjing Zhang
Junhua Yuan
author_facet Haolin Wu
Zhengyu Wu
Maojin Tian
Rongjing Zhang
Junhua Yuan
author_sort Haolin Wu
collection DOAJ
description ABSTRACT The single polar flagellar motor in Pseudomonas aeruginosa is equipped with two stator systems, MotAB and MotCD, both driven by H+ ions. The torque-speed relationship for flagellar motors with two stator systems has not been explored previously. In this study, we developed a method that utilizes optical trapping and fluorescence labeling to measure the torque-speed relationships for the wild-type P. aeruginosa motor with dual stators and mutant strains with a single stator system, revealing surprising differences in them. Moreover, we found that the MotAB stators exhibit slip-bond behavior in load dependence, contrasting with the catch-bond behavior of the MotCD stators and Escherichia coli stators. Further examination of the solvent isotope and pH effects on the torque-speed relationships of these stator systems provided additional insights into their dynamics. Interestingly, we discovered that the torque of the wild-type motor is similar to the combined torque of motors with MotAB or MotCD stators, indicating an additive contribution from the two stator types in the wild-type motors. These findings underscore the enhanced adaptability of P. aeruginosa to a wide range of external environments with varying load conditions.IMPORTANCEWe developed a novel method to measure the flagellar motor torque-speed relationship by trapping a swimming bacterium using optical tweezers. Using the P. aeruginosa flagellar motor as a model system to investigate motor dynamics with dual stator types, we measured the torque-speed relationships for wild-type motors with dual stator types and mutants with a single type. We found drastic differences that stem from the varying load dependencies of stator stability. These variations enable bacteria to rapidly adjust their stator composition in response to external load conditions. Interestingly, we observed that the torque of the wild-type motor is akin to the cumulative torque of motors with either stator type, indicating an additive contribution from the two stator types in wild-type motors. The methodology we established here can be readily employed to study motor dynamics in other flagellated bacteria.
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spelling doaj-art-1925c75afa1649929add7eae584bdee42025-08-20T01:58:59ZengAmerican Society for MicrobiologymBio2150-75112024-12-01151210.1128/mbio.00745-24Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosaHaolin Wu0Zhengyu Wu1Maojin Tian2Rongjing Zhang3Junhua Yuan4Hefei National Research Center for Physical Sciences at the Microscale and Department of Physics, University of Science and Technology of China, Hefei, Anhui, ChinaHefei National Research Center for Physical Sciences at the Microscale and Department of Physics, University of Science and Technology of China, Hefei, Anhui, ChinaCenter of Translational Medicine, Zibo Central Hospital Affiliated to Binzhou Medical University, Zibo, Shandong, ChinaHefei National Research Center for Physical Sciences at the Microscale and Department of Physics, University of Science and Technology of China, Hefei, Anhui, ChinaHefei National Research Center for Physical Sciences at the Microscale and Department of Physics, University of Science and Technology of China, Hefei, Anhui, ChinaABSTRACT The single polar flagellar motor in Pseudomonas aeruginosa is equipped with two stator systems, MotAB and MotCD, both driven by H+ ions. The torque-speed relationship for flagellar motors with two stator systems has not been explored previously. In this study, we developed a method that utilizes optical trapping and fluorescence labeling to measure the torque-speed relationships for the wild-type P. aeruginosa motor with dual stators and mutant strains with a single stator system, revealing surprising differences in them. Moreover, we found that the MotAB stators exhibit slip-bond behavior in load dependence, contrasting with the catch-bond behavior of the MotCD stators and Escherichia coli stators. Further examination of the solvent isotope and pH effects on the torque-speed relationships of these stator systems provided additional insights into their dynamics. Interestingly, we discovered that the torque of the wild-type motor is similar to the combined torque of motors with MotAB or MotCD stators, indicating an additive contribution from the two stator types in the wild-type motors. These findings underscore the enhanced adaptability of P. aeruginosa to a wide range of external environments with varying load conditions.IMPORTANCEWe developed a novel method to measure the flagellar motor torque-speed relationship by trapping a swimming bacterium using optical tweezers. Using the P. aeruginosa flagellar motor as a model system to investigate motor dynamics with dual stator types, we measured the torque-speed relationships for wild-type motors with dual stator types and mutants with a single type. We found drastic differences that stem from the varying load dependencies of stator stability. These variations enable bacteria to rapidly adjust their stator composition in response to external load conditions. Interestingly, we observed that the torque of the wild-type motor is akin to the cumulative torque of motors with either stator type, indicating an additive contribution from the two stator types in wild-type motors. The methodology we established here can be readily employed to study motor dynamics in other flagellated bacteria.https://journals.asm.org/doi/10.1128/mbio.00745-24optical tweezersbacterial motilitybacterial flagellar motorload dependenceslip bondcatch bond
spellingShingle Haolin Wu
Zhengyu Wu
Maojin Tian
Rongjing Zhang
Junhua Yuan
Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
mBio
optical tweezers
bacterial motility
bacterial flagellar motor
load dependence
slip bond
catch bond
title Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
title_full Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
title_fullStr Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
title_full_unstemmed Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
title_short Torque-speed relationship of the flagellar motor with dual-stator systems in Pseudomonas aeruginosa
title_sort torque speed relationship of the flagellar motor with dual stator systems in pseudomonas aeruginosa
topic optical tweezers
bacterial motility
bacterial flagellar motor
load dependence
slip bond
catch bond
url https://journals.asm.org/doi/10.1128/mbio.00745-24
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AT zhengyuwu torquespeedrelationshipoftheflagellarmotorwithdualstatorsystemsinpseudomonasaeruginosa
AT maojintian torquespeedrelationshipoftheflagellarmotorwithdualstatorsystemsinpseudomonasaeruginosa
AT rongjingzhang torquespeedrelationshipoftheflagellarmotorwithdualstatorsystemsinpseudomonasaeruginosa
AT junhuayuan torquespeedrelationshipoftheflagellarmotorwithdualstatorsystemsinpseudomonasaeruginosa