Osmosensing by Bacteria: Signals and Membrane-Based Sensors

Abstract

SUMMARY 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.

Structural Evidence for Functional Lipid Interactions in the Betaine Transporter BetP

“…To date, it is not known whether this regulatory restriction from the membrane results in upregulation or downregulation of the transport activity, which is attributed to the fact that mutations in the ionic network of loop 2 are not tolerated. However, having key components in the functional conformational changes directly accessible by the membrane may prove to be beneficial to communicate changes in the state of the membrane due to osmotic stress, an important factor in osmoregulation (Wood, 1999), through the core of the protein.…”

The transcriptional regulator, CosR, controls compatible solute biosynthesis and transport, motility and biofilm formation in Vibrio cholerae

“…All microorganisms must cope with variable environments and one important condition that microbial cells must adapt to is osmolarity. Many bacteria adapt to increased osmolarity by importing or producing compatible solutes to counteract osmotic pressure (Wood, 1999). Compatible solutes are small, highly soluble organic molecules that act to stabilize intracellular levels of water and turgor pressure without disturbing cellular function (Brown, 1976).…”

Potassium glutamate as a transcriptional inhibitor during bacterial osmoregulation

“…Escherichia coli must adapt to increases in osmotic pressure to survive its passage along the human GI tract (Foster and Spector, 1995). The consequence of lack of osmotic adaptation is the loss of water and turgor pressure needed for metabolism and cell division (Wood, 1999). Survival depends on the accumulation of small molecule osmoprotectants that prevent loss of water and are also compatible with normal biochemical events.…”

“…When growing E. coli are subject to osmotic shock, wholesale changes in growth, metabolism and gene expression occur (Wood, 1999). Many of these are common to all forms of hyperosmotic shock and some are unique changes caused by specific external osmolytes.…”