Junhua Yuan

Hefei National Center for Physical Sciences at Nanoscale

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Rongjing Zhang

Hefei National Center for Physical Sciences at Nanoscale

Chi Zhang

Hebei Agricultural University

Rui He

Sichuan University

Howard C. Berg

Harvard University

Zhengyu Wu

Jinan Central Hospital

Maojin Tian

Central Hospital of Zibo

Caijuan Yue

Hefei National Center for Physical Sciences at Nanoscale

Antai Tao

Hefei National Center for Physical Sciences at Nanoscale

Guangzhe Liu

Ocean University of China

Paul Waldron

University of Nottingham

Cooperative Institutions

University of Science and Technology of China

Hefei National Center for Physical Sciences at Nanoscale

Chinese Academy of Sciences

Shanghai Jiao Tong University

University of Chinese Academy of Sciences

Harvard University

Ministry of Agriculture and Rural Affairs

Sichuan University

Hefei University

Microbiology Institute of Shaanxi

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Precise Measurement of the Stoichiometry of the Adaptive Bacterial Flagellar Switch

mBio (2023)

Antai Tao Guangzhe Liu Rongjing Zhang Junhua Yuan

The cytoplasmic ring (C-ring) of the bacterial flagellar motor controls the motor rotation direction, thereby controlling bacterial run-and-tumble behavior. The C-ring has been shown to undergo adaptive remodeling in response to changes in motor directional bias. However, the stoichiometry and arrangement of the C-ring is still unclear due to contradiction between the results from fluorescence studies and cryo-electron microscopy (cryo-EM) structural analysis. Here, by using the copy number of FliG molecules (34) in the C-ring as a reference, we precisely measured the copy numbers of FliM molecules in motors rotating exclusively counterclockwise (CCW) and clockwise (CW). We surprisingly found that there are on average 45 and 58 FliM molecules in CW and CCW rotating motors, respectively, which are much higher than previous estimates. Our results suggested a new mechanism of C-ring adaptation, that is, extra FliM molecules could be bound to the primary C-ring with probability depending on the motor rotational direction. We further confirmed that all of the FliM molecules in the C-ring function in chemotaxis signaling transduction because all of them could be bound by the chemotactic response regulator CheY-P. Our measurements provided new insights into the structure and arrangement of the flagellar switch. IMPORTANCE The bacterial flagellar switch can undergo adaptive remodeling in response to changes in motor rotation direction, thereby shifting its operating point to match the output of the chemotaxis signaling pathway. However, it remains unclear how the flagellar switch accomplishes this adaptive remodeling. Here, via precise fluorescence studies, we measured the absolute copy numbers of the critical component in the switch for motors rotating counterclockwise and clockwise, obtaining much larger numbers than previous relative estimates. Our results suggested a new mechanism of adaptive remodeling of the flagellar switch and provided new insights for updating the conformation spread model of the switch.

10.1128/mbio.00189-23

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Switching dynamics of the bacterial flagellar motor near zero load

Proceedings of the National Academy of Sciences (2014)

Fangbin Wang Junhua Yuan Howard C. Berg

Significance The behavior of the flagellar rotary motor was monitored by following the rotation of small gold particles attached to flagellar hooks, nanometer-sized components found at the ends of motor drive shafts, providing an accurate readout of motor function. Some measurements were made in the past with large markers on flagellar filaments that suggested the presence of hidden steps preceding switching events. These steps were probably filament polymorphic transformations. Our data argue for a simple two-state system with transitions between clockwise and counterclockwise states that occur at random times.

Clockwise

Dynamics

Molecular motor

10.1073/pnas.1418548111

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Reviewer #1 (Public Review): Potassium-mediated bacterial chemotactic response

Chi Zhang Rongjing Zhang Junhua Yuan

Bacteria in biofilms secrete potassium ions to attract free swimming cells. However, the basis of chemotaxis to potassium remains poorly understood. Here, using a microfluidic device, we found that Escherichia coli can rapidly accumulate in regions of high potassium concentration on the order of millimoles. Using a bead assay, we measured the dynamic response of individual flagellar motors to stepwise changes in potassium concentration, finding that the response resulted from the chemotaxis signaling pathway instead of the motor response to changes in the proton motive force (PMF). To characterize the chemotactic response to potassium, we exposed the bacteria to a range of potassium concentrations and measured the dose-response curve and adaptation kinetics via a FRET assay, finding that the chemotaxis pathway exhibited a sensitive response and fast adaptation to potassium. We further found that the two major chemoreceptors Tar and Tsr respond differently to potassium. Tar receptors exhibit a biphasic response, whereas Tsr receptors respond to potassium as an attractant. These different responses were consistent with the responses of the two receptors to intracellular pH changes. Therefore, bacteria may sense the change in potassium concentration by sensing the change in intracellular pH. The sensitive response and fast adaptation allow bacteria to sense and localize small changes in potassium concentration. As the ratio of the two major chemoreceptors changes with bacterial growth stages, the differential responses of Tar and Tsr receptors to potassium suggest that cells at different growth stages respond differently to potassium and may have different requirements for potassium.

10.7554/elife.91452.1.sa1

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Flagellar motors of swimming bacteria contain an incomplete set of stator units to ensure robust motility

Science Advances (2023)

Yuhui Niu Rongjing Zhang Junhua Yuan

Flagellated bacteria, like

10.1126/sciadv.adi6724

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Citations (9)

Author Index Vol. 80, 2007

Pharmacology (2007)

Peter Kamerman Anthony Koller Lisa C. Loram Yujiro Hayashi Shingo Tsuji

10.1159/000109844

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Bacteria exhibit optimal diffusivity near surfaces

arXiv (Cornell University) (2024)

Antai Tao Guangzhe Liu Rongjing Zhang Junhua Yuan

In natural environments, solid surfaces present both opportunities and challenges for bacteria. On one hand, they serve as platforms for biofilm formation, crucial for bacterial colonization and resilience in harsh conditions. On the other hand, surfaces can entrap bacteria, constraining their environmental exploration compared to the freedom they experience in bulk liquid. Here, through systematic single-cell behavioral measurements, phenomenological modeling, and theoretical analysis, we reveal how bacteria strategically navigate these factors. We observe that bacterial surface residence time decreases sharply with increasing tumble bias, transitioning to a plateau at a tumble bias of around 0.25, consistent with the mean tumble bias of wild-type Escherichia coli. Furthermore, we find that bacterial surface diffusivity peaks near the mean tumble bias of wild-type E. coli. This reflects a bet-hedging strategy: some bacteria swiftly escape from the surface, while others, with longer surface residence times, explore this two-dimensional environment most efficiently.

10.48550/arxiv.2409.01597

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Observation of broken detailed balance in polymorphic transformation of bacterial flagellar filament

Biophysical Journal (2022)

S. Ma Rongjing Zhang Junhua Yuan

Detailed balance

Entropy production

Collective Behavior

10.1016/j.bpj.2022.05.022

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Spatial integration of sensory input and motor output inPseudomonas aeruginosachemotaxis through colocalized distribution

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Zhengyu Wu Maojin Tian Sanyuan Fu Min Chen Rongjing Zhang

Abstract The opportunistic pathogen Pseudomonas aeruginosa serves as a model organism for studying multiple signal transduction pathways. The chemoreceptor cluster, a core component of the chemotaxis pathway, is assembled from hundreds of proteins. The unipolar distribution of receptor clusters has long been recognized, yet the precise mechanism governing their assembly remains elusive. Here, we directly observed the relative positions of the flagellar motor and chemoreceptor cluster using flagellar filament labeling and gene editing techniques. Surprisingly, we found that both are located at the same cell pole, with the distribution pattern controlled by the polar anchor protein FlhF. Additionally, the efficient assembly of the chemoreceptor cluster is partially dependent on the integrity of the motor structure. Furthermore, we discovered that overexpression of the chemotaxis regulatory protein CheY leads to high intracellular levels of the second messenger c-di-GMP, triggering cell aggregation. Therefore, the colocalization of the chemoreceptor cluster and flagellum in P. aeruginosa serves to avoid cross-pathway signaling interference, enabling cells to conduct various physiological activities in an orderly manner.

Colocalization

Molecular motor

10.1101/2024.03.13.584826

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Measurement of the Internal Frictional Drag of the Bacterial Flagellar Motor by Fluctuation Analysis

Biophysical Journal (2020)

R. Wang Qiaopeng Chen Rongjing Zhang Junhua Yuan

Friction torque

10.1016/j.bpj.2020.04.020

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Swimming Escherichia coli Cells Explore the Environment by Lévy Walk

Applied and Environmental Microbiology (2021)

Haiyan Huo Rui He Rongjing Zhang Junhua Yuan

Escherichia coli cells swim in aqueous environment in a random walk of alternating runs and tumbles. The diffusion characteristics of this random walk remains unclear. In this study, by tracking the swimming of wild-type cells in a three-dimensional (3D) homogeneous environment, we found that their trajectories are superdiffusive, consistent with Lévy walk behavior. For comparison, we tracked the swimming of mutant cells that lack the chemotaxis signaling noise (the steady-state fluctuation of the concentration of the chemotaxis response regulator CheY-P) and found that their trajectories are normal diffusive. Therefore, wild-type E. coli cells explore the environment by Lévy walk, which originates from the chemotaxis signaling noise. This Lévy walk pattern enhances their efficiency in environmental exploration.IMPORTANCEE. coli cells explore the environment in a random walk of alternating runs and tumbles. By tracking the 3D trajectories of E. coli cells in an aqueous environment, we found that their trajectories are superdiffusive, with a power-law shape for the distribution of run lengths, which is characteristics of Lévy walk. We further show that this Lévy walk behavior is due to the random fluctuation of the output level of the bacterial chemotaxis pathway, and it enhances the efficiency of the bacteria in exploring the environment.

Tracking (education)

10.1128/aem.02429-20

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Citations (16)