Generation of an electrochemical proton gradient in Streptococcus cremoris by lactate efflux.

Abstract

Recently an energy-recycling model was proposed that postulates the generation of an electrochemical gradient in fermentative bacteria by carrier-mediated excretion of metabolic end products in symport with protons. In this paper experimental support for this model is given. In batch cultures of Streptococcus Uptake studies with the lipophilic cation tetraphenylphosphonium demonstrated that lactate efflux increased the electrical potential across the membrane by 51 mV. The generation of an electrical potential by lactate efflux and the demonstration of a potassium efflux-induced uptake of lactate indicates that lactate is translocated across the membrane by a symport system with more than one proton.The energy-recycling model recently proposed by Michels et al. (1) is an extension of the chemosmotic model given by Mitchell (2-4). The energy-recycling model postulates that carrier-mediated excretion of metabolic end products can lead to the generation of an electrochemical gradient across the cytoplasmic membrane, thus providing metabolic energy to the cell. The proposed model is based on the following considerations.The driving force for translocation of solute A across the cytoplasmic membrane by a solute-proton symport system (2) is the sum of the electrochemical gradient and the solute gradient (5):Z log(A-/A-t) + (n -1)A' -nZApH, in which AiT is the electrical potential and ApH is the pH gradient across the cytoplasmic membrane, n is the number of protons transported in symport with A-; Z is 2.3RT/F (R, gas constant; T, absolute temperature; F, Faraday constant); and A-and A-t are the concentrations of A-in the cell and the external medium, respectively. A steady-state level of accumulation is reached when this driving force is zero, thus when (n -1)AT -nZApH =-Z log(Aj-/A-t). According to this equation accumulation of solute A-will occur when [(n -1)AT -nZApH] > -Z log(Aj-/A-t). However, excretion of solute will occur when [(n -1)AT -nZApH] < -Z log(A-/A-,) and the energy of the solute gradient then will be converted into energy of the electrochemical proton gradient.During fermentation, excretion of metabolic end products via a carrier in symport with proton(s) can occur only when the outwardly directed driving force supplied by the chemical end product gradient exceeds the inwardly directed driving force supplied by the electrochemical gradient. The excretion of end products will then lead to the generation of an electrochemical gradient. Michels et al. (1)

A theoretical evaluation of growth yields of yeasts

“…Acids, however, may uncouple energy generation from biomass formation (Baronofsky et al 1984;Tuttle & Dugan 1976;Verduyn et al 1990b), although this probably depends to a major extent on the culture pH. Alternatively, export of acids may yield energy under certain conditions, as shown for lactate efflux by Streptococcus cremoris (Otto et al 1980). In contrast, yeasts only form two main fermentation products under anaerobic conditions, ethanol and glycerol, which are neutral and leave the cell by passive diffusion.…”

Lactic acid excretion by Streptococcus mutans

“…Konings and colleagues (Michels et al, 1979;Otto et al, 1980Otto et al, , 1982ten Brink & Konings, 1980) have provided evidence for an ' energy recycling model ' in Lactococcm lactis where the lactate ion, which is impermeable to the cell membrane, leaves the cell via a membrane carrier in symport with more than one proton. The energy recycling model is an extension of the chemiosmotic model presented by Mitchell (1963) and postulates that carriermediated excretion of end-products can lead to the generation of an electrochemical gradient across the cell membrane, thereby providing energy to the cell.…”

The generation of metabolic energy by solute transport

“…The generally accepted view is that in these organisms, the pmf and/or smf is generated by the action of the membrane-bound ATPase. However, recent studies have revealed that primary metabolic energy generation is not the only process by which a pmf or smf can be generated (Otto et al 1980;Poolman 1990;Konings et al 1994). In fermentative bacteria, a pmf or smf can be generated by secondary transport processes and, by analogy, these processes are called 'secondary metabolic energy generation' (Fig.…”