Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri

Abstract

Lactobaciflus buchneri ST2A vigorously decarboxylates histidine to the biogenic amine histamine, which is excreted into the medium. Cells grown in the presence of histidine generate both a transmembrane pH gradient, inside alkaline, and an electrical potential (A*), inside negative, upon addition of histidine. Studies of the mechanism of histidine uptake and histamine excretion in membrane vesicles and proteoliposomes devoid of cytosolic histidine decarboxylase activity demonstrate that histidine uptake, histamine efflux, and histidine/ histamine exchange are electrogenic processes. Histidine/histamine exchange is much faster than the unidirectional fluxes of these substrates, is inhibited by an inside-negative A* and is stimulated by an inside positive A*. These data suggest that the generation of metabolic energy from histidine decarboxylation results from an electrogenic histidine/histamine exchange and indirect proton extrusion due to the combined action of the decarboxylase and carrier-mediated exchange. The abundance of amino acid decarboxylation reactions among bacteria suggests that this mechanism of metabolic energy generation and/or pH regulation is widespread.Several precursor/product antiport mechanisms have been shown or were anticipated to be involved in generation of metabolic energy (16). Metabolic energy can be obtained from these mechanisms by substrate level phosphorylation (5,17) or by the formation of transmembrane ion gradients (ion and proton motive force). Characteristic for all of these precursor/product antiport mechanisms is that the product is structurally similar to the precursor. Transport of precursor and product can be catalyzed by one membrane transport protein which binds both precursor and product with high affinity. The usual mode in which these carrier proteins function is that of exchange: i.e., reorientation of the substrate binding site to either side of the membrane takes place while a substrate is bound. When the product is more positively charged than the precursor, this antiport generates an inside-negative electrical potential gradient across the membrane. Two examples of such carriers which have been studied in detail are the oxalate/formate antiporter of Oxalobacter formigenes (22) and the malate/lactate carrier of Lactococcus lactis (18). Because the metabolic conversion from oxalate to formate or from malate to lactate is a decarboxylation whereby the carboxylic group leaves the cytoplasm as neutral carbon dioxide or dihydrogen carbonate, the net effect of metabolism and electrogenic precursor/ product antiport is the extrusion of one proton. Consequently, a proton motive force is generated from the free energy of decarboxylation.A different mechanism by which metabolic energy is generated from a decarboxylation reaction is found in the Na'-translocating oxaloacetate decarboxylase (3). In this system, decarboxylation is catalyzed by a membrane-bound protein which uses the free energy directly to translocate sodium ions across the membrane. In this study, it will b...

Excretion and Uptake of Putrescine by the PotE Protein in Escherichia coli

“…These proteins play important roles in the generation of a proton motive force (45), neutralization of low extracellular pH (44), and supply of carbon dioxide (46). In this study, we clarified that the ornithine-putrescine antiporter also functions as a putrescine uptake system that is dependent on the membrane potential.…”

Secondary solute transport in bacteria

“…Since the decarboxylation of lysine, which results in cadaverine and carbon dioxide, also consumes a proton (intracellularly), this system may actually be analogous to oxalate/formate exchange-oxalate decarboxylation in Oxalobacter formigenes [82], malate/lactate exchange-malolactic fermentation in lactic acid bacteria [43], and histidine/histamine exchange-histidine decarboxylation in L. buchneri [95], and thus be involved in metabolic energy generation.…”

“…Some exchange processes actually contribute to the production of metabolic energy. Examples are oxalate/formate exchange (oxalate fermentation) in Oxalobacter formigenes [82], malate/lactate exchange (malolactic fermentation) in L. lactis [43], histidine/ histamine exchange in Lactobacillus buchneri [95], and aspartate/alanine exchange in Lactobacillus sp. (Abe, K., personal communication).…”

Energy transduction in lactic acid bacteria

“…are able to convert aspartate into alanine and gain metabolic energy from this reaction most likely as a result of aspartate/alanine exchange in combination with the decarboxylation (K. Abe, unpublished results). The energetic consequences of electrogenic transport in combination with precursor decarboxylation can be calculated from the standard free energy (AGo) of the decarboxylation reaction, pCO 2 values and assuming that the reaction proceeds to equilibrium [11]. For malolactic fermentation at pH 7, a pCO 2 of 1 bar and about equal concentrations of dianionic malate and lactate, a Ap of -275 mV is thermodynamically leasable (The AG~ of the malate decarboxylation reaction at pH 7.0 and CO 2 at 1 bar is approximately -26.5 kJ mol i [69]; for the lysine to 13¢~ cadaverine convcrsion thc ..IG~'~ is approximatcly -25 kJ tool t [11].…”