Dataset Information

A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis.

ABSTRACT: In the natural environment bacteria predominantly live adhered to a surface as part of a biofilm. While many of the components needed for biofilm assembly are known, the mechanism by which microbes sense and respond to contact with a surface is poorly understood. Bacillus subtilis is a Gram-positive model for biofilm formation. The DegS-DegU two-component system controls several multicellular behaviours in B.?subtilis, including biofilm formation. Here we identify the B.?subtilis flagellum as a mechanosensor that activates the DegS-DegU regulatory pathway. Inhibition of flagellar rotation by deletion or mutation of the flagellar stator gene, motB, results in an increase in both degU transcription and DegU?P driven processes, namely exoprotease production and poly-?-dl-glutamic acid biosynthesis. Similarly, inhibition of flagellar rotation by engaging the flagellar clutch or by tethering the flagella with antibodies also promotes an increase in degU transcription that is reflective of increased DegU?P levels in the cell. Collectively, these findings strongly indicate that inhibition of flagellar rotation acts as a mechanical trigger to activate the DegS-DegU two-component signal transduction system. We postulate that inhibition of flagellar rotation could function as a mechanical trigger to activate bacterial signal transduction cascades in many motile bacteria upon contact with a surface.

SUBMITTER: Cairns LS

PROVIDER: S-EPMC3963450 | biostudies-other | 2013 Oct

REPOSITORIES: biostudies-other

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A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis.

Cairns Lynne S LS Marlow Victoria L VL Bissett Emma E Ostrowski Adam A Stanley-Wall Nicola R NR

Molecular microbiology 20130814 1

In the natural environment bacteria predominantly live adhered to a surface as part of a biofilm. While many of the components needed for biofilm assembly are known, the mechanism by which microbes sense and respond to contact with a surface is poorly understood. Bacillus subtilis is a Gram-positive model for biofilm formation. The DegS-DegU two-component system controls several multicellular behaviours in B. subtilis, including biofilm formation. Here we identify the B. subtilis flagellum as a ...[more]

PMID: 23888912

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Project description:Environmental awareness is an essential attribute of all organisms. The homeoviscous adaptation system of Bacillus subtilis provides a powerful experimental model for the investigation of stimulus detection and signaling mechanisms at the molecular level. These bacteria sense the order of membrane lipids with the transmembrane (TM) protein DesK, which has an N-terminal sensor domain and an intracellular catalytic effector domain. DesK exhibits autokinase activity as well as phosphotransferase and phosphatase activities toward a cognate response regulator, DesR, that controls the expression of an enzyme that remodels membrane fluidity when the temperature drops below ∼30°C. Membrane fluidity signals are transmitted from the DesK sensor domain to the effector domain via rotational movements of a connecting 2-helix coiled coil (2-HCC). Previous molecular dynamic simulations suggested important roles for TM prolines in transducing the initial signals of membrane fluidity status to the 2-HCC. Here, we report that individual replacement of prolines in DesKs TM1 and TM5 helices by alanine (DesKPA) locked DesK in a phosphatase-ON state, abrogating membrane fluidity responses. An unbiased mutagenic screen identified the L174P replacement in the internal side of the repeated heptad of the 2-HCC structure that alleviated the signaling defects of every transmembrane DesKPA substitution. Moreover, substitutions by proline in other internal positions of the 2-HCC reestablished the kinase-ON state of the DesKPA mutants. These results imply that TM prolines are essential for finely tuned signal generation by the N-terminal sensor helices, facilitating a conformational control by the metastable 2-HCC domain of the DesK signaling state.IMPORTANCE Signal sensing and transduction is an essential biological process for cell adaptation and survival. Histidine kinases (HK) are the sensory proteins of two-component systems that control many bacterial responses to different stimuli, like environmental changes. Here, we focused on the HK DesK from Bacillus subtilis, a paradigmatic example of a transmembrane thermosensor suited to remodel membrane fluidity when the temperature drops below 30°C. DesK provides a tractable system for investigating the mechanism of transmembrane signaling, one of the majors interrogates in biology to date. Our studies demonstrate that transmembrane proline residues modulate the conformational switch of a 2-helix coiled-coil (2-HCC) structural motif that controls input-output in a variety of HK. Our results highlight the relevance of proline residues within sensor domains and could inspire investigations of their role in different signaling proteins.

Dataset Information

A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis.

Publications

A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis.

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