Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli.

Abstract

Chemotactic responses in Escherichia coli are typically mediated by transmembrane receptors that monitor chemoeffector levels with periplasmic binding domains and communicate with the flagellar motors through two cytoplasmic proteins, CheA and CheY. CheA autophosphorylates and then donates its phosphate to CheY, which in turn controls flagellar rotation. E. coli also exhibits chemotactic responses to substrates that are transported by the phosphoenolpyruvate (PEP)-dependent carbohydrate phosphotransferase system (PTS). Unlike conventional chemoreception, PTS substrates are sensed during their uptake and concomitant phosphorylation by the cell. The phosphoryl groups are transferred from PEP to the carbohydrates through two common intermediates, enzyme I (El) and phosphohistidine carrier protein (HPr), and then to sugar-specific enzymes II. We found that in mutant strains HPr-like (4) and somehow sensed as chemoeffectors during the uptake process (5, 6). PTSs consist of membraneassociated substrate-specific enzymes II (EIIs) and a common cytoplasmic phosphodonor relay (Fig. 1). EIls are phosphorylated at the expense of PEP through enzyme I (El), a histidine kinase, and a phosphohistidine carrier protein (HPr). During transport of PTS carbohydrates, phosphate groups are transferred through El and HPr to the appropriate ElI and finally to the substrate molecule as it enters the cell (for review, see ref. 7). This phospho-relay activity generates a signal that suppresses clockwise flagellar rotation, thereby extending swimming runs that carry the organism toward higher substrate concentrations (8).The signaling connection between the PTS and MCP chemotactic pathways has long been a mystery. MCPs are not required for PTS chemotaxis, but CheA and CheY are required (9-11), suggesting that PTS signals elicit flagellar responses by modulating phospho-CheY levels, possibly through control of CheA activity (12). E. coli has at least 15 Ells, each of which serves as the "chemoreceptor" for its transport substrates (7). However, neither the binding of substrate to an ElI nor the generation of intracellular carbohydrate-phosphate nor its subsequent degradation is sufficient to trigger a chemotactic response (5,6,10,13,14). In contrast, the common phospho-relay components El and HPr are necessary for uptake of all PTS carbohydrates and for chemotactic responses to them. Conceivably, the flagellar signal derives from an uptake-driven change in phosphate flux through these shared PTS components (6,15). This article describes in vivo and in vitro studies that indicate that the unphosphorylated form of El may be the long-sought missing link between the PTS and MCP phospho-relay circuits. Its signaling target appears to be the CheA kinase.

Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides

“…In E. coli, sugars are sensed using the MCP-dependent or PTS system which integrate at the histidine protein kinase, CheA (Hazelbauer et al, 1990;Lengeler & Vogler, 1989;Rowsell et al, 1995;Lux et a/., 1995). Here we investigated the chemotactic responses of R. sphaeroides to various carbohydrates and the role of metabolism in this process.…”

The compartmentalized vessel

“…Obviously, the two systems need to communicate and indeed interaction between the general PTS protein EI and the chemotaxis histidine kinase CheA was suggested to occur. 10 How is the information on nutrients availability, which is obtained by receptors of two sensory systems, integrated to generate an optimal metabolic response? Based on recent evidence discussed below, the basis for this crosstalk appears to be the spatial organization of the two signaling systems.…”

Variation of swimming speed enhances the chemotactic migration of Escherichia coli

“…While detailed studies have focused on the molecular mechanism of sensing and adaptation via the Trg receptor (Hazelbauer and Engstrom 1980;Feng et al 1999;Li and Hazelbauer 2005), the latter is yet to be characterized in terms of the phenotypic response, namely, swimming speed and motor bias. In addition, glucose is also sensed through a PhosphoTransferase System (PTS) sugar uptake mechanism which operates in conjunction with the receptor mediated response through Trg (Adler and Epstein 1974;Lux et al 1995;Neumann et al 2012). Thus to study the response exclusively through the Trg receptor, we expose the two strains of cells, namely, wild type K12 and a mutant Dtrg, to varying concentrations and gradients of a non-metabolizable analogue of glucose, namely, 2-Deoxy-D-glucose (2Dg) (Adler and Epstein 1974).…”