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  • Review Article
  • Published:

Mechanosensitive channels in bacteria: signs of closure?

Nature Reviews Microbiology volume 5, pages 431–440 (2007)Cite this article

Key Points

  • Bacterial mechanosensitive (MS) channels are gated by the perturbation of membrane tension, forming non-selective pores of 16–40 Å through which hydrated ions and solutes can flow.

  • MS channels have a key role in the survival of hypoosmotic shock, but might also have other roles during cell-wall remodelling.

  • Using electrophysiology, three principal structural classes of MS channels have been defined in Escherichia coli. Species can have multiple homologues of each class, but not all have demonstrated MS channel activity. The homologues differ in their degree of conservation of the pore-lining helix residues, and their threshold sensitivity to tension might reflect this and be selected to enable them to have specific cellular functions.

  • MscS and MscL homologues are also found in plants, oomycetes, algae and in some fungi. MscS homologues are associated with chloroplast shape and development in Arabidopsis and Chlamydomonas.

  • Crystal structures of the Mycobacterium tuberculosis MscL (MscL-Mt) and the E. coli MscS (MscS-Ec) channels have revealed a homopentamer and a homoheptamer respectively. Structurally the channels are unrelated, as MscS has more complex packing and an extensive cytoplasmic domain that is required for assembly. Both MscL and MscS use a hydrophobic seal to maintain the channel pore in the closed state.

  • The emerging consensus is that the crystal structures represent either closed states or intermediates in the transition from closed to open states. MscS-Ec characteristically exhibits a desensitized, inactivated state and it is possible that the crystal structure is in this conformation rather than in the 'natural' closed state. MscL-Mt is generally accepted to have been crystallized in the closed state.

  • The structural transitions in MscL and MscS gating have been studied using biophysical, genetic and biochemical approaches. Both channels gate by tilting and rotating the helices surrounding the pore, which involves specific conserved residues.

  • Recent molecular analysis of MS channels has focused on the interaction of the channel-protein residues with surrounding membrane lipids. In this Review we define the absence of specific amino acids at the protein–lipid interface that might block mechanogating as central to MS channel function. We term this 'negative space'.

Abstract

Bacterial mechanosensitive channels are activated by increases in tension in the lipid bilayer of the cytoplasmic membrane, where they transiently create large pores in a controlled manner. Mechanosensitive channel research has benefited from advances in electrophysiology, genomics and molecular genetics as well as from the application of biophysical techniques. Most recently, new analytical methods have been used to complement existing knowledge and generate insights into the molecular interactions that take place between mechanosensitive channel proteins and the surrounding membrane lipids. This article reviews the latest developments.

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Figure 1: Physiological function of mechanosensitive channels in bacteria.
Figure 2: Measuring the conductance and pressure sensitivity of MscS and MscL.
Figure 3: Structures of MscL-Mt and MscS-Ec.
Figure 4: Helix packing and proposed gating movement in MscS-Ec.
Figure 5: Defining the interactions that might prevent mechanosensation.

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Acknowledgements

The authors acknowledge the generous support of their research collaborators and colleagues, but in particular P. Blount, J. Bowie, J. Naismith, T. Rasmussen, A. Rasmussen, W. Bartlett, C. Kung, B. Martinac, D. Rees, E. Perozo, T. Lee and S. Sukharev. Research on MS channels is supported by The Wellcome Trust (GR077564MA), the Biotechnology and Biological Sciences Research Council (BBSRC), MRC and the University of Aberdeen, UK.

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Authors and Affiliations

  1. School of Medical Sciences, Institute of Medical Sciences, University of Aberdeen, Aberdeen, AB25 2ZD, UK

    Ian R. Booth, Michelle D. Edwards, Susan Black, Ulrike Schumann & Samantha Miller

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  1. Ian R. Booth
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DATABASES

Entrez Genome Project

Arabidopsis thaliana

Escherichia coli

Lactococcus lactis

Mycobacterium tuberculosis

Staphylococcus aureus

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Glossary

Patch clamp

A technique whereby a small glass electrode tip is tightly sealed onto a patch of cell membrane, thereby making it possible to record the flow of current through individual ion channels or pores in the patch.

Conductance

Calculated from the increase in current when a single channel is fully open, under known conditions of applied transmembrane voltage.

Open dwell time

The average time a single channel remains in the fully open state under conditions of constant transmembrane pressure and voltage; this parameter can only be determined statistically based on the analysis of many single openings of channels that occur over several minutes in a patch-clamp recording.

Pressure sensitivity

The pressure required to open channels is most often quoted relative to another channel. For example, the pressure required to open MscL-Ec is often quoted as a ratio by reference to the pressure required to achieve the first openings of MscS-Ec in the same membrane patch. Absolute measures of sensitivity to membrane tension can be achieved only by measuring the curvature of the patch under pressure using video microscopy and by applying Laplace's law, which relates the tension in the bilayer to the transmembrane pressure through the radius of the curvature of the patch.

Protonmotive force

The protonmotive force is created when protons are expelled from the cell during respiratory and photosynthetic electron flow or by the action of an ATPase. The protonmotive force consists of the proton gradient (ΔpH) and a gradient of charge (ΔΨ). Proton (and Na+) ions enter the cell, driven by the protonmotive force, to do useful work such as ATP synthesis, flagellar rotation and membrane transport.

Inactivation

(also known as desensitization). MscS-Ec has been observed to undergo spontaneous loss of channel activity when held under constant pressure; activity can be restored to the majority of channels in a patch by resting the membrane (re-setting the pressure to zero) for a short period before re-imposing pressure.

Electron paramagnetic resonance

Observation of the transitions between spin states of an unpaired electron in a magnetic field.

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Booth, I., Edwards, M., Black, S. et al. Mechanosensitive channels in bacteria: signs of closure?. Nat Rev Microbiol 5, 431–440 (2007). https://doi.org/10.1038/nrmicro1659

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