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Review
. 1999 Mar;63(1):230-62.
doi: 10.1128/MMBR.63.1.230-262.1999.

Osmosensing by bacteria: signals and membrane-based sensors

J M Wood  1
Affiliations
Review

Osmosensing by bacteria: signals and membrane-based sensors

J M Wood. Microbiol Mol Biol Rev. 1999 Mar.

Abstract

Bacteria can survive dramatic osmotic shifts. Osmoregulatory responses mitigate the passive adjustments in cell structure and the growth inhibition that may ensue. The levels of certain cytoplasmic solutes rise and fall in response to increases and decreases, respectively, in extracellular osmolality. Certain organic compounds are favored over ions as osmoregulatory solutes, although K+ fluxes are intrinsic to the osmoregulatory response for at least some organisms. Osmosensors must undergo transitions between "off" and "on" conformations in response to changes in extracellular water activity (direct osmosensing) or resulting changes in cell structure (indirect osmosensing). Those located in the cytoplasmic membranes and nucleoids of bacteria are positioned for indirect osmosensing. Cytoplasmic membrane-based osmosensors may detect changes in the periplasmic and/or cytoplasmic solvent by experiencing changes in preferential interactions with particular solvent constituents, cosolvent-induced hydration changes, and/or macromolecular crowding. Alternatively, the membrane may act as an antenna and osmosensors may detect changes in membrane structure. Cosolvents may modulate intrinsic biomembrane strain and/or topologically closed membrane systems may experience changes in mechanical strain in response to imposed osmotic shifts. The osmosensory mechanisms controlling membrane-based K+ transporters, transcriptional regulators, osmoprotectant transporters, and mechanosensitive channels intrinsic to the cytoplasmic membrane of Escherichia coli are under intensive investigation. The osmoprotectant transporter ProP and channel MscL act as osmosensors after purification and reconstitution in proteoliposomes. Evidence that sensor kinase KdpD receives multiple sensory inputs is consistent with the effects of K+ fluxes on nucleoid structure, cellular energetics, cytoplasmic ionic strength, and ion composition as well as on cytoplasmic osmolality. Thus, osmoregulatory responses accommodate and exploit the effects of individual cosolvents on cell structure and function as well as the collective contribution of cosolvents to intracellular osmolality.

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Figures

FIG. 1
FIG. 1
Phases of the osmotic stress response for E. coli K-12. Structural and physiological responses triggered by osmotic shifts (up or down) imposed at time zero proceed in parallel along the indicated, approximate timescales. The evidence supporting this scheme is discussed in the text.
FIG. 2
FIG. 2
Chemosensing versus osmosensing. Many biosensors are molecules whose conformations change between an “off” and an “on” conformation in response to a change in the biosensor environment. Chemosensors detect the biochemistry of cellular environments, including changes in nutrient supplies and signals with biological origins. The proportion of chemosensor molecules in the “on” conformation increases when the appropriate ligand binds to a specific site on the chemosensor surface. Osmosensors detect changes in extracellular water activity (direct osmosensing) or resulting changes in cell composition or structure (indirect osmosensing). At least some osmosensors are expected to change their conformations in response to solvent changes. The proportion of osmosensor molecules in the “on” conformation would then increase when the sensor surface was exposed to a suitably altered solvent (depicted here by a change from a white to a shaded background). Alternatively, sensing could involve a change in oligomeric state (for example, ligand- or solvent-induced dimerization).
FIG. 3
FIG. 3
Solvent effects on macromolecular conformation. If different forms (conformations) of a macromolecule (or osmosensor) interact differently with their solvent, solvent changes will alter the distribution of the macromolecule (or sensor) population among those forms. Such effects could constitute a basis for osmosensing, as illustrated in Fig. 2. Simultaneous exposure of membrane-based osmosensors to multiple solvent environments would further enhance the scope for modulation of their structure by solvent changes. Three aspects of solvent-macromolecule interactions that have been demonstrated to influence macromolecular conformation are illustrated in this figure. For preferential exclusion, if water and cosolvent interact differently with the macromolecular surface, a change in cosolvent composition can trigger a change in macromolecular conformation and/or oligomerization. For example, an increased concentration of one or more cosolvents (indicated by a darker grey background) that are preferentially excluded from the sensor surface (indicated by a halo) favors a conformational change that results in a decreased sensor surface area (indicated by a change from square to round). For hydration changes, if entry of cosolvent molecules to macromolecule-associated solvent pools is restricted (as indicated by the relative sizes of the grey cosolvent molecules and the water-filled cleft on the macromolecular surface), an increase in cosolvent concentration will cause macromolecule-associated solvent to be extracted and macromolecular conformation to be altered (closing the water-filled cleft and possibly also causing a more generalized conformational change, indicated by a change from square to round). For macromolecular crowding or confinement within matrices, in crowded solutions (those containing high concentrations or networks of macromolecules) compact or globular conformations of a test macromolecule (or osmosensor) are favored. Changes in crowding of the bacterial cytoplasm, where macromolecules occupy as much as 50% of the available volume (indicated as a change in the concentration of oblong, grey molecules comparable in size to the test macromolecule), may therefore favor changes in conformation of osmosensor molecules (again indicated as a change from square to round).
FIG. 4
FIG. 4
Solvent effects on membranes. Membrane strain is the relative displacement of membrane constituents in response to an imposed stress. Such strain may be communicated to osmosensors by the phospholipid bilayer. (A) Intrinsic membrane strain arises because phospholipid monolayers that have an intrinsic tendency to be curved must flatten in order to associate and form phospholipid bilayers in aqueous solution (satisfying the requirements of the hydrophobic effect). This phenomenon has a number of potential consequences including the possible existence of a lateral pressure, exerted in the bilayer plain, that is higher in the membrane core than at the membrane surface (see the text for a discussion of this phenomenon). (B) Changes in cosolvent composition (indicated in grey) may modulate intrinsic membrane strain by acting in the ways illustrated in Fig. 3. Such changes could be transmitted to (and modify the conformations of) osmosensors that are integral membrane proteins. (C) Since biomembranes are fluid, topologically closed, and differentially permeable to water and cosolvents, changes of intra- or extracellular water activity cause changes in membrane shape. Such changes may alter mechanically imposed membrane strain in ways that change the conformations of osmosensors that are integral membrane proteins.
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