Ribose and glucose-galactose receptors: Competitors in bacterial chemotaxis

• Published in: Journal of molecular biology Vol. 227; no. 2; pp. 418 - 440
• Main Author: Mowbray, Sherry L.
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 20.09.1992; Elsevier
• Subjects: Amino Acid Sequence; bacterial chemotaxis; bacterial transport; Bacteriology; Binding Sites; Binding, Competitive; Biological and medical sciences; Carrier Proteins - chemistry; Carrier Proteins - metabolism; chemotaxis; Escherichia coli; Escherichia coli - metabolism; Escherichia coli Proteins; Fundamental and applied biological sciences. Psychology; galactose; Galactose - metabolism; glucose; Glucose - metabolism; Hydrogen Bonding; Microbiology; Models, Molecular; Molecular Sequence Data; Periplasmic Binding Proteins; Permeability, membrane transport, intracellular transport; Protein Conformation; receptors; Receptors, Cell Surface - chemistry; Receptors, Cell Surface - metabolism; ribose; Ribose - metabolism; Salmonella typhimurium; Salmonella typhimurium - metabolism; Sequence Homology, Amino Acid; X-ray crystallography; X-ray diffraction; X-ray crystallography; bacterial transport; receptors; bacterial chemotaxis; periplasmic-binding proteins; Binding protein; Membrane receptor; Molecular structure; Membrane transport; Escherichia coli; Bacteria; Carbohydrate; Chemotaxis; Salmonella typhimurium; Biological activity; Comparative study; Enterobacteriaceae
• ISSN: 0022-2836; 1089-8638
• DOI: 10.1016/0022-2836(92)90898-T

The periplasmic ribose and glucose-galactose receptors (binding proteins) of Gram-negative bacteria compete for a common inner membrane receptor in bacterial chemotaxis, as well as being the essential primary receptors for their respective membrane transport systems. The high-resolution structures of the periplasmic receptors for ribose (from Escherichia coli) and glucose or galactose (from both Salmonella typhimurium and E. coli) are compared here to outline some features that may be important in their dual functions. The overall structure of each protein consists of two similar domains, both of which are made up of two non-contiguous segments of amino acid chain. Each domain is composed of a core of β-sheet flanked on both sides with α-helices. The two domains are related to each other by an almost perfect intramolecular axis of symmetry. The ribose receptor is smaller as a result of a number of deletions in its sequence relative to the glucose-galactose receptor, mostly occurring in the loop regions; as a result, this protein is also more symmetrical. Many structural features, including some hydrophobic core interactions, a buried aspartate residue and several unusual turns, are conserved between the two proteins. The binding sites for ligand are in similar locations, and built along similar principles, although none of the specific interactions with the sugars is conserved. A comparison shows further that slightly different rotations relate the domains to each other in the three proteins, with the ribose receptor being the most closed, and the Salmonella glucose-galactose receptor the most open. The primary axis of relative rotation is almost perpendicular to that which describes the intramolecular symmetry in each case. These relative rotations of the domains are accompanied by the sliding of some helices as the structures adjust themselves to relieve strain. The hinges which are responsible for most of these relative domain rotations are very similar in the three proteins, consisting of a symmetrical arrangement of β-strands and α-helices and two conserved water molecules that are critical to the hydrogen bonding in the important interdomain region. A region of high sequence and structural similarity between the ribose and glucose-galactose receptors is also located around the intramolecular symmetry axis, on the opposite side of the proteins from the hinge region. This region is that which is altered most by the relative rotations, and is the location of most of the known mutations which affect chemotaxis and transport in the ribose receptor.