Bacterial PEP-Dependent Carbohydrate: Phosphotransferase Systems Couple Sensing and Global Control Mechanisms

Abstract

The PEP-dependent carbohydrate:phosphotransferase systems (PTSs) of enteric bacteria constitute a complex sensory system which involves as its central element a PEP-dependent His-protein kinase (Enzyme I). As a unit, the PTS comprises up to 20 different transporters per cell which correspond to its chemoreceptors for PTS carbohydrates, and several targeting subunits, which include in the low [G+C] Gram-positive bacteria an ancillary Ser/Thr-protein kinase. The PTS senses the presence of carbohydrates, in particular glucose, in the medium and the energy state of the cell, in the form of either the intracellular PEP-to-pyruvate ratio or the D-fructose-bisphosphate levels. This information is subsequently communicated to cellular targets, in particular those involved in the chemotactic response of the cell towards PTS carbohydrates, and in sensing glucose in the medium, using cAMP and several targeting subunits as intermediates. Peptide targeting subunits ensure the fast, transient, and yet accurate communication of the PTS with its more than hundred different targets, avoiding at the same time unwanted cross-talk. Many elements of this sensory system are simultaneously elements of specific and global regulatory networks. Thus, the PTS controls, besides the immediate (in the ms to s range) chemotactic responses, the activity of the various carbohydrate transporters and enzymes involved in carbon and energy metabolism through inducer exclusion, and in a delayed response (in the min to h range) the synthesis of these transporters and catabolic enzymes through catabolite repression. Indirect consequences of this program are phenomena related to cell surface rearrangements, which include flagella synthesis, as well as memory, adaptation, and learning effects. The analogy between the PTS and other prokaryotic systems, and more complex sensory systems from eukaryotic organisms which share elements with regulatory systems is obvious.

The compartmentalized vessel

“…7 The chemotaxis system enables navigation of bacterial cells along gradients, with carbon source gradients having a major impact. 8,9 Together, these systems can be regarded as a microbrain or as the bacterial metabolic nervous system. 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.…”

Phosphoenolpyruvate Phosphotransferase System Components Modulate Gene Transcription and Virulence of Borrelia burgdorferi

“…Although genome sequence analysis indicated the presence of numerous homologs of carbohydrate transporters, B. burgdorferi actually uses very few carbohydrates to support its growth, including glucose, mannose, N-acetylglucosamine, maltose, chitobiose, and glycerol (20). In many bacteria, the highly conserved phosphoenolpyruvate phosphotransferase system (PEP-PTS) plays an important dual role in both carbohydrate transport and the regulation of gene expression based on carbohydrate availability (21)(22)(23)(24). The PEP-PTS consists of multiple components, including the common cytoplasmic components enzyme I (EI) and histidine protein (HPr), the sugarspecific cytoplasmic components enzyme IIA (EIIA) and enzyme IIB (EIIB), and the sugar specific membrane-associated component(s) enzyme IIC (EIIC).…”

Lipid dependencies, biogenesis and cytoplasmic micellar forms of integral membrane sugar transport proteins of the bacterial phosphotransferase system

“…The prokaryotic phosphoenolpyruvate (PEP)-sugar phosphotransferase system (PTS) is an unusual system for taking up sugars as it couples sugar uptake to phosphorylation (Kaback, 1968(Kaback, , 1970Lengeler & Jahreis, 2009;Postma et al, 1993;Simoni et al, 1967). It serves as an enzyme-coupled transport system that modifies its substrate sugars by phosphorylation concomitant with transport (Meadow et al, 1990).…”

“…The proteins of the PTS catalyse two vectorial reactions, one unidirectional and irreversible (reaction 1) and one bidirectional and fully reversible (reaction 2) (Lengeler & Jahreis, 2009;Saier et al, 1977a, b).…”