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

2014 ◽  
Vol 112 (2) ◽  
pp. E186-E193 ◽  
Author(s):  
Beiyan Nan ◽  
Jigar N. Bandaria ◽  
Kathy Y. Guo ◽  
Xue Fan ◽  
Amirpasha Moghtaderi ◽  
...  
Keyword(s):  
Spatial Distribution ◽  
Cell Polarity ◽  
Myxococcus Xanthus ◽  
Proton Motive Force ◽  
Gliding Motility ◽  
Cellular Polarity ◽  
Gtpase Activating Protein ◽  
Chemosensory Pathway ◽  
Ras Family ◽  
Ras Family Proteins

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.

scholarly journals MglC, a Paralog of Myxococcus xanthus GTPase-Activating Protein MglB, Plays a Divergent Role in Motility Regulation

2015 ◽  
Vol 198 (3) ◽  
pp. 510-520 ◽  
Author(s):  
Anna L. McLoon ◽  
Kristin Wuichet ◽  
Michael Häsler ◽  
Daniela Keilberg ◽  
Dobromir Szadkowski ◽  
...  
Keyword(s):  
Gene Duplication ◽  
Cell Polarity ◽  
Response Regulator ◽  
Myxococcus Xanthus ◽  
Social Behaviors ◽  
Gliding Motility ◽  
Cellular Polarity ◽  
Gtpase Activating Protein ◽  
Content Type ◽  
Motility Regulation

ABSTRACTIn order to optimize interactions with their environment and one another, bacteria regulate their motility. In the case of the rod-shaped cells ofMyxococcus xanthus, regulated motility is essential for social behaviors.M. xanthusmoves over surfaces using type IV pilus-dependent motility and gliding motility. These two motility systems are coordinated by a protein module that controls cell polarity and consists of three polarly localized proteins, the small G protein MglA, the cognate MglA GTPase-activating protein MglB, and the response regulator RomR. Cellular reversals are induced by the Frz chemosensory system, and the output response regulator of this system, FrzZ, interfaces with the MglA/MglB/RomR module to invert cell polarity. Using a computational approach, we identify a paralog of MglB, MXAN_5770 (MglC). Genetic epistasis experiments demonstrate that MglC functions in the same pathway as MglA, MglB, RomR, and FrzZ and is important for regulating cellular reversals. Like MglB, MglC localizes to the cell poles asymmetrically and with a large cluster at the lagging pole. Correct polar localization of MglC depends on RomR and MglB. Consistently, MglC interacts directly with MglB and the C-terminal output domain of RomR, and we identified a surface of MglC that is necessary for the interaction with MglB and for MglC function. Together, our findings identify an additional member of theM. xanthuspolarity module involved in regulating motility and demonstrate how gene duplication followed by functional divergence can add a layer of control to the complex cellular processes of motility and motility regulation.IMPORTANCEGene duplication and the subsequent divergence of the duplicated genes are important evolutionary mechanisms for increasing both biological complexity and regulation of biological processes. The bacteriumMyxococcus xanthusis a soil bacterium with an unusually large genome that carries out several social processes, including predation of other bacterial species and formation of multicellular, spore-filled fruiting bodies. One feature of the largeM. xanthusgenome is that it contains many gene duplications. Here, we compare the products of one example of gene duplication and divergence, in which a paralog of the cognate MglA GTPase-activating protein MglB has acquired a different and opposing role in the regulation of cellular polarity and motility, processes critical to the bacterium's social behaviors.

scholarly journals A gated relaxation oscillator controls morphogenetic movements in bacteria

2017 ◽  
Author(s):  
Mathilde Guzzo ◽  
Seán M. Murray ◽  
Eugénie Martineau ◽  
Sébastien Lhospice ◽  
Grégory Baronian ◽  
...  
Keyword(s):  
Cell Polarity ◽  
Myxococcus Xanthus ◽  
Dynamic Control ◽  
Relaxation Oscillator ◽  
Critical Importance ◽  
Gtpase Activating Protein ◽  
Wide Range ◽  
Direction Of Movement ◽  
Polarity Reversals ◽  
Cellular Development

SummaryDynamic control of cell polarity is of critical importance for many aspects of cellular development and motility. In Myxococcus xanthus, a G-protein and its cognate GTPase-activating protein establish a polarity axis that defines the direction of movement of the cell and which can be rapidly inverted by the Frz chemosensory system. Although vital for collective cell behaviours, how Frz triggers this switch has remained unknown. Here, we use genetics, imaging and mathematical modelling to show that Frz controls polarity reversals via a gated relaxation oscillator. FrzX, which we newly identify as the primary Frz output, provides the gating and thus acts as the trigger for reversals. Slow relocalisation of the polarity protein RomR then creates a refractory period during which another switch cannot be triggered. A secondary Frz output, FrzZ, decreases this delay allowing rapid reversals when required. This architecture thus results in a highly tunable switch that allows a wide range of motility responses.

scholarly journals Interaction between a Ras and a Rho GTPase Couples Selection of a Growth Site to the Development of Cell Polarity in Yeast

2003 ◽  
Vol 14 (12) ◽  
pp. 4958-4970 ◽  
Author(s):  
Keith G. Kozminski ◽  
Laure Beven ◽  
Elizabeth Angerman ◽  
Amy Hin Yan Tong ◽  
Charles Boone ◽  
...  
Keyword(s):  
Cell Polarity ◽  
Rho Gtpase ◽  
Cell Cortex ◽  
Nucleotide Exchange ◽  
Yeast Saccharomyces Cerevisiae ◽  
Growth Site ◽  
Ras Family ◽  
Rho Family ◽  
Polarity Establishment ◽  
Selection Of

Polarized cell growth requires the coupling of a defined spatial site on the cell cortex to the apparatus that directs the establishment of cell polarity. In the budding yeast Saccharomyces cerevisiae, the Ras-family GTPase Rsr1p/Bud1p and its regulators select the proper site for bud emergence on the cell cortex. The Rho-family GTPase Cdc42p and its associated proteins then establish an axis of polarized growth by triggering an asymmetric organization of the actin cytoskeleton and secretory apparatus at the selected bud site. We explored whether a direct linkage exists between the Rsr1p/Bud1p and Cdc42p GTPases. Here we show specific genetic interactions between RSR1/BUD1 and particular cdc42 mutants defective in polarity establishment. We also show that Cdc42p coimmunoprecipitated with Rsr1p/Bud1p from yeast extracts. In vitro studies indicated a direct interaction between Rsr1p/Bud1p and Cdc42p, which was enhanced by Cdc24p, a guanine nucleotide exchange factor for Cdc42p. Our findings suggest that Cdc42p interacts directly with Rsr1p/Bud1p in vivo, providing a novel mechanism by which direct contact between a Ras-family GTPase and a Rho-family GTPase links the selection of a growth site to polarity establishment.

scholarly journals Three-dimensional observations of an aperiodic oscillatory gliding motility behaviour in Myxococcus xanthus using confocal interference reflection microscopy

2019 ◽  
Author(s):  
Liam M. Rooney ◽  
Lisa S. Kölln ◽  
Ross Scrimgeour ◽  
William B. Amos ◽  
Paul A. Hoskisson ◽  
...  
Keyword(s):  
Myxococcus Xanthus ◽  
Three Dimensional ◽  
Basal Membrane ◽  
Gliding Motility ◽  
The Novel ◽  
Force Transmission ◽  
Topological Information ◽  
Type Iv ◽  
Microscopy Techniques

The Delta-proteobacterium, Myxococcus xanthus, has been used as a model for bacterial motility and to provide insights of bacterial swarming behaviours. Fluorescence microscopy techniques have shown that various mechanisms are involved in gliding motility, but these have almost entirely been limited to 2D studies and there is currently no understanding of gliding motility in a 3D context. We present here the first use of confocal interference reflection microscopy (IRM) to study gliding bacteria, and we reveal aperiodic oscillatory behaviour with changes in the position of the basal membrane relative to the coverglass on the order of 90 nm in vitro. Firstly, we use a model plano-convex lens specimen to show how topological information can be obtained from the wavelength-dependent interference pattern in IRM. We then use IRM to observe gliding M. xanthus and show that cells undergo previously unobserved changes in their height as they glide. We compare the wild-type with mutants of reduced motility, which also exhibit the same changes in adhesion profile during gliding. We find that the general gliding behaviour is independent of the proton motive force-generating complex, AglRQS, and suggest that the novel behaviour we present here may be a result of recoil and force transmission along the length of the cell body following firing of the Type IV pili.

Genes required for both gliding motility and development in Myxococcus xanthus

1994 ◽  
Vol 14 (4) ◽  
pp. 785-795 ◽  
Author(s):  
Spencer D. MacNeil ◽  
Aram Mouzeyan ◽  
Patricia L Hartzell
Keyword(s):  
Myxococcus Xanthus ◽  
Gliding Motility

scholarly journals Three-Dimensional Observations of an Aperiodic Oscillatory Gliding Behavior in Myxococcus xanthus Using Confocal Interference Reflection Microscopy

mSphere ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Liam M. Rooney ◽  
Lisa S. Kölln ◽  
Ross Scrimgeour ◽  
William B. Amos ◽  
Paul A. Hoskisson ◽  
...  
Keyword(s):  
Myxococcus Xanthus ◽  
Three Dimensional ◽  
Oscillatory Behavior ◽  
Gliding Motility ◽  
Bacterial Cells ◽  
Force Transmission ◽  
Content Type ◽  
Gliding Bacteria ◽  
Microscopy Techniques

ABSTRACT The deltaproteobacterium Myxococcus xanthus is a model for bacterial motility and has provided unprecedented insights into bacterial swarming behaviors. Fluorescence microscopy techniques have been invaluable in defining the mechanisms that are involved in gliding motility, but these have almost entirely been limited to two-dimensional (2D) studies, and there is currently no understanding of gliding motility in a three-dimensional (3D) context. We present here the first use of confocal interference reflection microscopy (IRM) to study gliding bacteria, revealing aperiodic oscillatory behavior with changes in the position of the basal membrane relative to the substrate on the order of 90 nm in vitro. First, we use a model planoconvex lens specimen to show how topological information can be obtained from the wavelength-dependent interference pattern in IRM. We then use IRM to observe gliding M. xanthus bacteria and show that cells undergo previously unobserved changes in their adhesion profile as they glide. We compare the wild type with mutants that have reduced motility, which also exhibit the same changes in the adhesion profile during gliding. We find that the general gliding behavior is independent of the proton motive force-generating complex AglRQS and suggest that the novel behavior that we present here may be a result of recoil and force transmission along the length of the cell body following firing of the type IV pili. IMPORTANCE 3D imaging of live bacteria with optical microscopy techniques is a challenge due to the small size of bacterial cells, meaning that previous studies have been limited to observing motility behavior in 2D. We introduce the application of confocal multiwavelength interference reflection microscopy to bacteria, which enables visualization of 3D motility behaviors in a single 2D image. Using the model organism Myxococcus xanthus, we identified novel motility behaviors that are not explained by current motility models, where gliding bacteria exhibit aperiodic changes in their adhesion to an underlying solid surface. We concluded that the 3D behavior was not linked to canonical motility mechanisms and that IRM could be applied to study a range of microbiological specimens with minimal adaptation to a commercial microscope.

scholarly journals Gliding motility in Myxococcus xanthus: mgl locus, RNA, and predicted protein products.

1989 ◽  
Vol 171 (2) ◽  
pp. 819-830 ◽  
Author(s):  
K Stephens ◽  
P Hartzell ◽  
D Kaiser
Keyword(s):  
Myxococcus Xanthus ◽  
Gliding Motility
Sign in / Sign up

Export Citation Format

Share Document