Turgor-controlled K+ fluxes and their pathways in Escherichia coli

Abstract

Escherichiu coli like most gram-negative bacteria with walls maintains a cytoplasmic osmolarity exceeding that of the medium ; the resulting hydrostatic pressure (turgor pressure) pushes the cytoplasmic membrane against the peptidoglycan and creates a tension in the two envelopes.Potassium is the only cation wich takes part in the regulation of cellular osmolarity. The adaptation of intracellular K ' concentration to external osmolarity involves K + turgor-controlled fluxes. When the medium osmolarity is raised an osmodependent influx of K can be observed; this is carried out by the K f transport system TrkA which can also taken up rubidium. A specific and unidirectional pathway allows K + ions to flow out of the cell when the medium osmolarity is decreased; this pathway reveals two characteristics: it has no affinity for rubidium and it can be blocked by the blockers of eukaryotic K + channels. Osmodependent fluxes are turned on immediately after the medium osmolarity is disturbed; in contrast, they are turned off gradually as the rate of K t fluxes approach zero. The rate of K' influx seems to depend on the level of internal osmolarity and not on the extent of the increase in medium osmolarity. The rate of the efflux is directly proportional to the decrease in medium osmolarity and is independent on the level of internal osmolarity.Algal cells and higher plant cells have developed osmoregulatory mechanisms in order to withstand osmotic stress and to maintain a constant turgor pressure which is assumed to exert a dual function in initiation of growth and enlargement of cell [l, 21. This regulation is mediated by fluxes of water and organic or inorganic water-soluble molecules and also by the biosynthesis of metabolites of low molecular mass Cells that lack cell walls, such as erythrocytes [4] and certain algae [5], maintain their volume at a constant value over a wide range of external osmotic pressures. Their response to disturbances of the cxternal osmolarity is biphasic [I]; first, water fluxes instantaneously modify the cell volume but not the absolute number of solute molecules, then the cell volume is slowly shifted back to its original value by means of controlled loss or uptake of osmotically active solute molecules and/or stimulation of metabolic turnover of osmoactive solutes. In contrast, walled cells are able to maintain internal osmolarity and pressure higher than in the medium, creating a turgor pressure which is the macroscopic parameter that is regulated during the biphasic response to osmotic stress. The solute transport processes involved in regulation of turgor pressure are identical to those observed in the volume regulation of non-walled-cells [l]. Turgor pressure has been found to be maintained within narrow limits over a wide range of external osmolarities in marine algal cells [I]; its absolute value varies from 2-20 bar according to the species.Bacteria seem to share in some properties of eukaryotic cells since they show a biphasic response to osmotic stress 16, 71 and a turgor pressure...

Regulation of compatible solute accumulation in Salmonella typhimurium: evidence for a glycine betaine efflux system

“…Thus, when the activity of the Prop system was studied in osmo-adapting cells and compared with the activity of the turgor-regulated TrkA system it was found that the Prop system was active when the activity of the TrkA system had subsided ( Fig. 3; see also Meury et al, 1985). Further, Prop activity was unaffected by achievement of steady state accumulation of glycine betaine.…”

“…8). However, early experiments to demonstrate activation of K+ efflux by high turgor created by downshock were similarly unsuccessful (Meury et al, 1985). It has been reported that osmotic pressure controls the amount of proline that is excreted into the medium by mutants of S. typhimurium that are osmotolerant due to overproduction of proline (Csonka, 1988).…”

“…Such transport systems should increase their activity under conditions of stress and their activity should decline once the stress is alleviated. The best examples of this type of activity have emerged from the study of K+ transport in Escherichia coli (Rhoads & Epstein, 1978;Meury et al, 1985). The activity of K+-uptake systems is under negative-feedback control from high turgor pressure (and possibly from high internal K+ concentrations).…”

Evidence for the involvement of a common genetic determinant in the control of thallium-resistant (Tl+-R) phenotype and salinity-tolerant phenotype in the cyanobacterium Nostoc muscorum.

“…The salinity inducible K ϩ uptake and accumulation is the primary signal essential for an overaccumulation of secondary osmolytes, such as glycine betaine or proline, that protect the bacterial systems against salinity stress (Csonka and Hanson, 1991;Meury et al, 1985). Studies on the role of K ϩ as a primary osmolyte in cyanobacterial salinity adaptation have shown that upshock treatment leads to an immediate uptake of Na ϩ during the first 2 min, followed by uptake of K ϩ during the next 20 min, during which Na ϩ is extruded (Reed and Stewart, 1985).…”

The distribution of homologues of the Escherichia coli KefC K+-efflux system in other bacterial species

“…In Escherichia coli control over K+ accumulation is the major mechanism of turgor regulation (Epstein, 1986) and the size of the cytoplasmic K+ pool is determined primarily by the osmotic pressure of the environment (Epstein & Schultz, 1965). Regulation of both influx and efflux processes for K+ has been demonstrated (Rhoads & Epstein, 1978;Meury et al, 1985;Bakker et al, 1987), which allows the cell to adapt to both low and high turgor. K+ uptake is accomplished by at least three systems, Kdp, Kup and Trk (Bossemeyer et al, 1989a;Epstein, 1986).…”