A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system
ABSTRACT Many bacteria utilize the type 9 secretion system (T9SS) for gliding motility, surface colonization, and pathogenesis. This dual-function motor supports both gliding motility and protein secretion, where rotation of the T9SS plays a central role. Fueled by the energy of the stored proton mo...
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| Language: | English |
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American Society for Microbiology
2025-07-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.01125-25 |
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| author | Abhishek Trivedi Jacob A. Miratsky Emma C. Henderson Abhishek Singharoy Abhishek Shrivastava |
| author_facet | Abhishek Trivedi Jacob A. Miratsky Emma C. Henderson Abhishek Singharoy Abhishek Shrivastava |
| author_sort | Abhishek Trivedi |
| collection | DOAJ |
| description | ABSTRACT Many bacteria utilize the type 9 secretion system (T9SS) for gliding motility, surface colonization, and pathogenesis. This dual-function motor supports both gliding motility and protein secretion, where rotation of the T9SS plays a central role. Fueled by the energy of the stored proton motive force and transmitted through the torque of membrane-anchored stator units, the rotary T9SS propels an adhesin-coated conveyor belt along the bacterial outer membrane like a molecular snowmobile, thereby enabling gliding motion. However, the mechanisms controlling the rotational direction and gliding motility of T9SS remain elusive. Shedding light on this mechanism, we find that in the gliding bacterium Flavobacterium johnsoniae, deletion of the C-terminus of the conveyor belt-associated protein GldJ controls and, in fact, reverses the rotational direction of T9SS from counterclockwise (CCW) to clockwise (CW). This suggests that the interface between the conveyor belt-associated protein GldJ and the T9SS ring protein GldK plays an important role in controlling the directionality of T9SS, potentially by modulating its interaction with the stator complex GldLM, which drives motor rotation. Combined with MD simulation of the T9SS stator units GldLM, we suggest a “tri-component gearset” model where GldJ controls the rotational direction of its driver, the T9SS, thus providing adaptive sensory feedback to influence the motility of the gliding bacterium.IMPORTANCEThe type 9 secretion system (T9SS) is fundamental to bacterial gliding motility, pathogenesis, and surface colonization. Our findings reveal that the C-terminal region of the conveyor belt-associated protein GldJ functions as a molecular switch which is capable of reversing the rotational direction of T9SS. Through the coordinated actions of the T9SS stator units (akin to a driving motor), the GldK ring (the gear that converts rotational energy into linear movement), and GldJ, this machinery forms a smart conveyor belt system reminiscent of flexible or cognitive mechanical conveyors. Such advanced conveyors can alter their direction to adapt to shifting demands. Here, we show that the bacterial T9SS similarly adjusts its rotational bias based on feedback from the conveyor belt-associated protein GldJ. This dual-role feedback mechanism underscores an evolved, controllable biological snowmobile, offering new avenues for studying how bacteria fine-tune motility in dynamic environments. |
| format | Article |
| id | doaj-art-e485d896fd734354bdfd7e5804a02c7d |
| institution | Kabale University |
| issn | 2150-7511 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj-art-e485d896fd734354bdfd7e5804a02c7d2025-08-20T03:28:10ZengAmerican Society for MicrobiologymBio2150-75112025-07-0116710.1128/mbio.01125-25A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion systemAbhishek Trivedi0Jacob A. Miratsky1Emma C. Henderson2Abhishek Singharoy3Abhishek Shrivastava4School of Life Sciences, Arizona State University, Tempe, Arizona, USABiodesign Institute, Arizona State University, Tempe, Arizona, USASchool of Life Sciences, Arizona State University, Tempe, Arizona, USABiodesign Institute, Arizona State University, Tempe, Arizona, USASchool of Life Sciences, Arizona State University, Tempe, Arizona, USAABSTRACT Many bacteria utilize the type 9 secretion system (T9SS) for gliding motility, surface colonization, and pathogenesis. This dual-function motor supports both gliding motility and protein secretion, where rotation of the T9SS plays a central role. Fueled by the energy of the stored proton motive force and transmitted through the torque of membrane-anchored stator units, the rotary T9SS propels an adhesin-coated conveyor belt along the bacterial outer membrane like a molecular snowmobile, thereby enabling gliding motion. However, the mechanisms controlling the rotational direction and gliding motility of T9SS remain elusive. Shedding light on this mechanism, we find that in the gliding bacterium Flavobacterium johnsoniae, deletion of the C-terminus of the conveyor belt-associated protein GldJ controls and, in fact, reverses the rotational direction of T9SS from counterclockwise (CCW) to clockwise (CW). This suggests that the interface between the conveyor belt-associated protein GldJ and the T9SS ring protein GldK plays an important role in controlling the directionality of T9SS, potentially by modulating its interaction with the stator complex GldLM, which drives motor rotation. Combined with MD simulation of the T9SS stator units GldLM, we suggest a “tri-component gearset” model where GldJ controls the rotational direction of its driver, the T9SS, thus providing adaptive sensory feedback to influence the motility of the gliding bacterium.IMPORTANCEThe type 9 secretion system (T9SS) is fundamental to bacterial gliding motility, pathogenesis, and surface colonization. Our findings reveal that the C-terminal region of the conveyor belt-associated protein GldJ functions as a molecular switch which is capable of reversing the rotational direction of T9SS. Through the coordinated actions of the T9SS stator units (akin to a driving motor), the GldK ring (the gear that converts rotational energy into linear movement), and GldJ, this machinery forms a smart conveyor belt system reminiscent of flexible or cognitive mechanical conveyors. Such advanced conveyors can alter their direction to adapt to shifting demands. Here, we show that the bacterial T9SS similarly adjusts its rotational bias based on feedback from the conveyor belt-associated protein GldJ. This dual-role feedback mechanism underscores an evolved, controllable biological snowmobile, offering new avenues for studying how bacteria fine-tune motility in dynamic environments.https://journals.asm.org/doi/10.1128/mbio.01125-25bacterial protein secretiontype 9 secretion system (T9SS)molecular motorsbacterial motilitygliding motilityFlavobacterium |
| spellingShingle | Abhishek Trivedi Jacob A. Miratsky Emma C. Henderson Abhishek Singharoy Abhishek Shrivastava A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system mBio bacterial protein secretion type 9 secretion system (T9SS) molecular motors bacterial motility gliding motility Flavobacterium |
| title | A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system |
| title_full | A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system |
| title_fullStr | A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system |
| title_full_unstemmed | A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system |
| title_short | A molecular conveyor belt-associated protein controls the rotational direction of the bacterial type 9 secretion system |
| title_sort | molecular conveyor belt associated protein controls the rotational direction of the bacterial type 9 secretion system |
| topic | bacterial protein secretion type 9 secretion system (T9SS) molecular motors bacterial motility gliding motility Flavobacterium |
| url | https://journals.asm.org/doi/10.1128/mbio.01125-25 |
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