Proton-linked sugar transport systems in bacteria

Abstract

The cell membranes of various bacteria contain proton-linked transport systems for D-xylose, L-arabinose, D-galactose, D-glucose, L-rhamnose, L-fucose, lactose, and melibiose. The melibiose transporter of E. coli is linked to both Na+ and H+ translocation. The substrate and inhibitor specificities of the monosaccharide transporters are described. By locating, cloning, and sequencing the genes encoding the sugar/H+ transporters in E. coli, the primary sequences of the transport proteins have been deduced. Those for xylose/H+, arabinose/H+, and galactose/H+ transport are homologous to each other. Furthermore, they are just as similar to the primary sequences of the following: glucose transport proteins found in a Cyanobacterium, yeast, alga, rat, mouse, and man; proteins for transport of galactose, lactose, or maltose in species of yeast; and to a developmentally regulated protein of Leishmania for which a function is not yet established. Some of these proteins catalyze facilitated diffusion of the sugar without cation transport. From the alignments of the homologous amino acid sequences, predictions of common structural features can be made: there are likely to be twelve membrane-spanning alpha-helices, possibly in two groups of six; there is a central hydrophilic region, probably comprised largely of alpha-helix; the highly conserved amino acid residues (40-50 out of 472-522 total) form discrete patterns or motifs throughout the proteins that are presumably critical for substrate recognition and the molecular mechanism of transport. Some of these features are found also in other transport proteins for citrate, tetracycline, lactose, or melibiose, the primary sequences of which are not similar to each other or to the homologous series of transporters. The glucose/Na+ transporter of rabbit and man is different in primary sequence to all the other sugar transporters characterized, but it is homologous to the proline/Na+ transporter of E. coli, and there is evidence for its structural similarity to glucose/H+ transporters in Plants. In vivo and in vitro mutagenesis of the lactose/H+ and melibiose/Na+ (H+) transporters of E. coli has identified individual amino acid residues alterations of which affect sugar and/or cation recognition and parameters of transport. Most of the bacterial transport proteins have been identified and the lactose/H+ transporter has been purified. The directions of future investigations are discussed.

Secondary solute transport in bacteria

“…1-4). Electrogenic uptake of neutral solutes in bacteria has been shown for sugars and amino acids [11,16,[36][37][38][39]. Electrogenic cationic solute-proton (or sodium ion) symport has been observed for the uptake of arginine and lysine in a number of bacteria [11,[40][41][42].…”

“…E. coli uses both protons and sodium ions as coupling ions for the uptake of sugars, amino acids and other nutrients [e.g., lactose-H + (LacY), galactose-H + (GalP), arabinose-H + (AraE), xylose-H + (XylE), proline-H + (ProP), proline-Na + (PutP), serine-Na +, glutamate-Na + (GItS), glutamate-H + (GltP), a-ketoglutarate-H + (KgtP), pantothenate-Na + (PanF)] [11,16,[46][47][48][49][50][51]. Unique examples are the melibiose carrier (MelB) of E. coli and the alanine carrier protein (Acp) of thermophilic bacterium PS3 which can choose among protons and sodium ions for the uphill movement of solutes [13,52,53], and these may actually represent intermediate stages in the evolution from H + to Na ÷ energetics or vice versa.…”

“…The molecular masses of most of these proteins fall in the range 40-55 kDa [16]. Hydropathy analyses of the primary sequences has indicated that the secondary carriers consist of a hydrophobic polypeptide which traverses the cytoplasmic membrane in a zig-zag manner.…”

“…Hydropathy analyses of the primary sequences has indicated that the secondary carriers consist of a hydrophobic polypeptide which traverses the cytoplasmic membrane in a zig-zag manner. It has been proposed that the generic secondary structure of the carrier proteins consists of 2 times 6 (or 5) transmembrane a-helices that are separated by a relatively large cytoplasmic loop [16,106,107] (Fig. 3).…”

“…Although a number of reviews on secondary transport proteins have appeared in the past few years, many of these writings are restricted to discussing properties of a single (type of) carrier molecule [11][12][13][14][15], while others focus on structural information and evolutionary relationships between polypeptides on basis of sequence similarities [16][17][18][19] or specific aspects of carrier functions [20,21]. The present paper serves as a comprehensive review on the diversity of secondary carrier mechanisms in the bacterial kingdom.…”