A Bacterial Ras-Like Small GTP-Binding Protein and Its Cognate GAP Establish a Dynamic Spatial Polarity Axis to Control Directed Motility

Zhang, Yong; Franco, Michel; Ducret, Adrien; Mignot, Tâm

doi:10.1371/journal.pbio.1000430

Cited by 98 publications

(359 citation statements)

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“…MglA plays a central regulatory role in establishing the polar axis for gliding motility. Mutations in mglA cause dramatic changes in the reversal frequency of gliding cells (13,14). We tested whether MglA directly interacts with the gliding motor protein AglR in the absence of the other gliding-associated proteins present in M. xanthus using a bacterial adenylate cyclase two-hybrid (BACTH) assay.…”

Section: Single Gliding Motors Frequently Reverse Their Direction Of mentioning

confidence: 99%

“…MglA has been observed to localize primarily at the cell poles (13,14); however, most of the components in the gliding machinery, including AglR, localize along the whole cell body (8,9,21), creating a spatial dilemma for the interaction between MglA and the motors. We confirmed the observation that cells expressing MglA-GFP showed bright fluorescence spots primarily at the cell poles; however, we also found blurry GFP fluorescence at nonpolar regions along the cell length (Fig.…”

Section: Single Gliding Motors Frequently Reverse Their Direction Of mentioning

confidence: 99%

“…Gliding M. xanthus cells on 1.5% agar plates typically reverse their polarity approximately every 8-12 min (12). The Frz chemosensory pathway regulates the reversal frequency and thus the direction of cell movements of both motility systems (12)(13)(14)(15)(16). MglA, a Ras family GTPase, has been identified as the central regulator of cell polarity and the principal responder to Frz pathway signaling (13)(14)(15).…”

mentioning

confidence: 99%

“…The Frz chemosensory pathway regulates the reversal frequency and thus the direction of cell movements of both motility systems (12)(13)(14)(15)(16). MglA, a Ras family GTPase, has been identified as the central regulator of cell polarity and the principal responder to Frz pathway signaling (13)(14)(15). It has been reported that MglA is connected to the Frz pathway by the response regulator RomR (17)(18)(19).…”

mentioning

confidence: 99%

“…It has been reported that MglA is connected to the Frz pathway by the response regulator RomR (17)(18)(19). Importantly, MglA switches between an active GTP-bound form and an inactive GDP-bound form, which is regulated by MglB, the cognate GTPase-activating protein (GAP) of MglA, providing another layer of regulation (13,14).…”

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confidence: 99%

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The polarity of myxobacterial gliding is regulated by direct interactions between the gliding motors and the Ras homolog MglA

Nan¹,

Bandaria

Guo³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Gliding motility in Myxococcus xanthus is powered by flagella stator homologs that move in helical trajectories using proton motive force. The Frz chemosensory pathway regulates the cell polarity axis through MglA, a Ras family GTPase; however, little is known about how MglA establishes the polarity of gliding, because the gliding motors move simultaneously in opposite directions. Here we examined the localization and dynamics of MglA and gliding motors in high spatial and time resolution. We determined that MglA localizes not only at the cell poles, but also along the cell bodies, forming a decreasing concentration gradient toward the lagging cell pole. MglA directly interacts with the motor protein AglR, and the spatial distribution of AglR reversals is positively correlated with the MglA gradient. Thus, the motors moving toward lagging cell poles are less likely to reverse, generating stronger forward propulsion. MglB, the GTPase-activating protein of MglA, regulates motor reversal by maintaining the MglA gradient. Our results suggest a mechanism whereby bacteria use Ras family proteins to modulate cellular polarity.

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Section: Single Gliding Motors Frequently Reverse Their Direction Of mentioning

confidence: 99%

Section: Single Gliding Motors Frequently Reverse Their Direction Of mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The polarity of myxobacterial gliding is regulated by direct interactions between the gliding motors and the Ras homolog MglA

Nan¹,

Bandaria

Guo³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Unorthodox regulation of the MglA Ras‐like GTPase controlling polarity in Myxococcus xanthus

Dinet

Mignot

2023

FEBS Letters

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Motile cells have developed a large array of molecular machineries to actively change their direction of movement in response to spatial cues from their environment. In this process, small GTPases act as molecular switches and work in tandem with regulators and sensors of their guanine nucleotide status (GAP, GEF, GDI and effectors) to dynamically polarize the cell and regulate its motility. In this review, we focus on Myxococcus xanthus as a model organism to elucidate the function of an atypical small Ras GTPase system in the control of directed cell motility. M. xanthus cells direct their motility by reversing their direction of movement through a mechanism involving the redirection of the motility apparatus to the opposite cell pole. The reversal frequency of moving M. xanthus cells is controlled by modular and interconnected protein networks linking the chemosensory‐like frizzy (Frz) pathway – that transmits environmental signals – to the downstream Ras‐like Mgl polarity control system – that comprises the Ras‐like MglA GTPase protein and its regulators. Here, we discuss how variations in the GTPase interactome landscape underlie single‐cell decisions and consequently, multicellular patterns.

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Nanomicrobiology

2014

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A Bacterial Ras-Like Small GTP-Binding Protein and Its Cognate GAP Establish a Dynamic Spatial Polarity Axis to Control Directed Motility

Abstract: Directional control of bacterial motility is regulated by dynamic polarity inversions driven by pole-to-pole oscillation of a Ras family small G-protein and its associated GTPase-activating protein.

Cited by 98 publications

References 43 publications

The polarity of myxobacterial gliding is regulated by direct interactions between the gliding motors and the Ras homolog MglA

The polarity of myxobacterial gliding is regulated by direct interactions between the gliding motors and the Ras homolog MglA

Unorthodox regulation of the MglA Ras‐like GTPase controlling polarity in Myxococcus xanthus

Nanomicrobiology

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