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

A Bernards

A Ducret

A. B Bowman

Adrien Ducret

B Antonny

B. B Finlay

B. D Blackhart

C Janetopoulos

D. C Anderson

E Huitema

E. M Mauriello

E. V Koonin

G. H Wadhams

H Lam

H Sun

I Bulyha

J Hodgkin

J. E Berleman

J. H Dong

J. L Bos

K. M Ferguson

K. S Ramamurthi

L. D Sibley

M Franco

Michael T. Laub

Michel Franco

O. A Igoshin

P Hartzell

P. G Charest

R. F Yang

S Kappe

S Klein

S Leonardy

S Zhang

T Mignot

Tâm Mignot

V. H Bustamante

Y Li

Y. F Inclan

Yong Zhang

Z Tong

English

PubMed

Zhang Yong

Franco Michel

Ducret Adrien

Mignot Tâm

Public Library of Science (PLOS)

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

Crossref

PLoS Biology

Regulated cell polarity is central to many cellular processes. We investigated the mechanisms that govern the rapid switching of cell polarity (reversals) during motility of the bacterium Myxococcus xanthus. Cellular reversals are mediated by pole-to-pole oscillations of motility proteins and the frequency of the oscillations is under the control of the Frz chemosensory system. However, the molecular mechanism that creates dynamic polarity remained to be characterized. In this work, we establish that polarization is regulated by the GTP cycle of a Ras-like GTPase, MglA. We initially sought an MglA regulator and purified a protein, MglB, which was found to activate GTP hydrolysis by MglA. Using live fluorescence microscopy, we show that MglA and MglB localize at opposite poles and oscillate oppositely when cells reverse. In absence of MglB, MglA-YFP accumulates at the lagging cell end, leading to a strikingly aberrant reversal cycle. Spatial control of MglA is achieved through the GAP activity of MglB because an MglA mutant that cannot hydrolyze GTP accumulates at the lagging cell end, despite the presence of MglB. Genetic and cell biological studies show that the MglA-GTP cycle controls dynamic polarity and the reversal switch. The study supports a model wherein a chemosensory signal transduction system (Frz) activates reversals by relieving a spatial inhibition at the back pole of the cells: reversals are allowed by Frz-activated switching of MglB to the opposite pole, allowing MglA-GTP to accumulate at the back of the cells and create the polarity switch. In summary, our results provide insight into how bacteria regulate their polarity dynamically, revealing unsuspected conserved regulations with eukaryots

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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.

Regulated cell polarity is central to many cellular processes. We investigated the mechanisms that govern the rapid switching of cell polarity (reversals) during motility of the bacterium Myxococcus xanthus. Cellular reversals are mediated by pole-to-pole oscillations of motility proteins and the frequency of the oscillations is under the control of the Frz chemosensory system. However, the molecular mechanism that creates dynamic polarity remained to be characterized. In this work, we establish that polarization is regulated by the GTP cycle of a Ras-like GTPase, MglA. We initially sought an MglA regulator and purified a protein, MglB, which was found to activate GTP hydrolysis by MglA. Using live fluorescence microscopy, we show that MglA and MglB localize at opposite poles and oscillate oppositely when cells reverse. In absence of MglB, MglA-YFP accumulates at the lagging cell end, leading to a strikingly aberrant reversal cycle. Spatial control of MglA is achieved through the GAP activity of MglB because an MglA mutant that cannot hydrolyze GTP accumulates at the lagging cell end, despite the presence of MglB. Genetic and cell biological studies show that the MglA-GTP cycle controls dynamic polarity and the reversal switch. The study supports a model wherein a chemosensory signal transduction system (Frz) activates reversals by relieving a spatial inhibition at the back pole of the cells: reversals are allowed by Frz-activated switching of MglB to the opposite pole, allowing MglA-GTP to accumulate at the back of the cells and create the polarity switch. In summary, our results provide insight into how bacteria regulate their polarity dynamically, revealing unsuspected conserved regulations with eukaryots.</p

Zhang, Yong

Franco, Michel

Ducret, Adrien

Mignot, Tâm

Copenhagen University Research Information System

A bacterial ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility

A biochemical oscillator explains several aspects of Myxococcus xanthus behavior during development.

A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell.

A microscope automated fluidic system to study bacterial processes in real time.

Active and passive mechanisms of intracellular transport and localization in bacteria.

Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition.

AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus.

Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals.

Bacterial birth scar proteins mark future flagellum assembly site.

Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue,

Bacterial virulence strategies that utilize Rho GTPases.

Big roles for small GTPases in the control of directed cell movement.

Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites.

Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus.

Directional sensing during chemotaxis.

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Dynein light chains of the Roadblock/LC7 group belong to an ancient protein superfamily implicated in NTPase regulation.

Evidence that focal adhesion complexes power bacterial gliding motility.

Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus.

Frizzy’’ genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility.

FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus.

Function of MglA, a 22-kilodalton protein essential for gliding in Myxococcus xanthus.

GAP control: regulating the regulators of small GTPases.

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Genetics of gliding motility in myxococcus-xanthus (myxobacterales) - 2 gene systems control movement.

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Homologs of eukaryotic Ras superfamily proteins in prokaryotes and their novel phylogenetic correlation with their eukaryotic analogs.

Intracellular parasite invasion strategies.

Making sense of it all: bacterial chemotaxis.

Myristoylation-facilitated binding of the G protein ARF1GDP to membrane phospholipids is required for its activation by a soluble nucleotide exchange factor.

Negative membrane curvature as a cue for subcellular localization of a bacterial protein.

Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts.

Predataxis behavior in Myxococcus xanthus.

proteins in actin remodeling and intracellular transport.

Regulated pole-to-pole oscillations of a bacterial gliding motility protein.

Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins.

Spatiotemporal regulation of Ras activity provides directional sensing.

The influence of bound GDP on the kinetics of guanine nucleotide binding to G proteins.

The receiver domain of FrzE, a CheA-CheY fusion protein, regulates the CheA histidine kinase activity and Dynamic Polarity Control

Two localization motifs mediate polar residence of FrzS during cell movement and reversals of Myxococcus xanthus.

Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system.

Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus.

Wittinghofer A

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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

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Public Library of Science (PLOS)

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