A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus

Mathilde Guzzo; Seán M. Murray; Eugénie Martineau; Sébastien Lhospice; Grégory Baronian; Laetitia My; Yong Zhang; Leon Espinosa; Renaud Vincentelli; Benjamin P. Bratton; Joshua W. Shaevitz; Virginie Molle; Martin Howard; Tâm Mignot

doi:10.1038/s41564-018-0203-x

A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus

Mathilde Guzzo, Seán M. Murray, Eugénie Martineau, Sébastien Lhospice, Grégory Baronian, Laetitia My, Yong Zhang, Leon Espinosa, Renaud Vincentelli, Benjamin P. Bratton, Joshua W. Shaevitz, Virginie Molle, Martin Howard, Tâm Mignot^*

^*Corresponding author for this work

16 Citations (Scopus)

Abstract

Dynamic control of cell polarity is of critical importance for many aspects of cellular development and motility. In Myxococcus xanthus, MglA, a G protein, and MglB, its cognate GTPase-activating protein, establish a polarity axis that defines the direction of movement of the cell and that 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 identify as a target of the Frz kinase, provides the gating and thus acts as the trigger for reversals. Slow relocalization 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. Thus, this architecture results in a highly tuneable switch that allows a wide range of reversal frequencies.

Original language	English
Journal	Nature Microbiology
Volume	3
Issue number	8
Pages (from-to)	948-959
Number of pages	12
ISSN	2058-5276
DOIs	https://doi.org/10.1038/s41564-018-0203-x
Publication status	Published - 2018
Externally published	Yes

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Guzzo, M., Murray, S. M., Martineau, E., Lhospice, S., Baronian, G., My, L., Zhang, Y., Espinosa, L., Vincentelli, R., Bratton, B. P., Shaevitz, J. W., Molle, V., Howard, M., & Mignot, T. (2018). A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus. Nature Microbiology, 3(8), 948-959. https://doi.org/10.1038/s41564-018-0203-x

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title = "A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus",

abstract = "Dynamic control of cell polarity is of critical importance for many aspects of cellular development and motility. In Myxococcus xanthus, MglA, a G protein, and MglB, its cognate GTPase-activating protein, establish a polarity axis that defines the direction of movement of the cell and that 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 identify as a target of the Frz kinase, provides the gating and thus acts as the trigger for reversals. Slow relocalization 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. Thus, this architecture results in a highly tuneable switch that allows a wide range of reversal frequencies.",

author = "Mathilde Guzzo and Murray, {Se{\'a}n M.} and Eug{\'e}nie Martineau and S{\'e}bastien Lhospice and Gr{\'e}gory Baronian and Laetitia My and Yong Zhang and Leon Espinosa and Renaud Vincentelli and Bratton, {Benjamin P.} and Shaevitz, {Joshua W.} and Virginie Molle and Martin Howard and T{\^a}m Mignot",

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T1 - A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus

AU - Guzzo, Mathilde

AU - Murray, Seán M.

AU - Martineau, Eugénie

AU - Lhospice, Sébastien

AU - Baronian, Grégory

AU - My, Laetitia

AU - Zhang, Yong

AU - Espinosa, Leon

AU - Vincentelli, Renaud

AU - Bratton, Benjamin P.

AU - Shaevitz, Joshua W.

AU - Molle, Virginie

AU - Howard, Martin

AU - Mignot, Tâm

PY - 2018

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N2 - Dynamic control of cell polarity is of critical importance for many aspects of cellular development and motility. In Myxococcus xanthus, MglA, a G protein, and MglB, its cognate GTPase-activating protein, establish a polarity axis that defines the direction of movement of the cell and that 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 identify as a target of the Frz kinase, provides the gating and thus acts as the trigger for reversals. Slow relocalization 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. Thus, this architecture results in a highly tuneable switch that allows a wide range of reversal frequencies.

AB - Dynamic control of cell polarity is of critical importance for many aspects of cellular development and motility. In Myxococcus xanthus, MglA, a G protein, and MglB, its cognate GTPase-activating protein, establish a polarity axis that defines the direction of movement of the cell and that 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 identify as a target of the Frz kinase, provides the gating and thus acts as the trigger for reversals. Slow relocalization 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. Thus, this architecture results in a highly tuneable switch that allows a wide range of reversal frequencies.

U2 - 10.1038/s41564-018-0203-x

DO - 10.1038/s41564-018-0203-x

M3 - Journal article

C2 - 30013238

AN - SCOPUS:85049935380

SN - 2058-5276

VL - 3

SP - 948

EP - 959

JO - Nature Microbiology

JF - Nature Microbiology

IS - 8

ER -

A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus

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