Streptococcus cremoris cells that had been grown in a chemostat were starved for lactose. The viability of the culture remained essentially constant in the first hours of starvation and subsequently declined logarithmically. The viability pattern during starvation varied with the previously imposed growth rates. The death rates were 0.029, 0.076, and 0.298 h-' for cells grown at dilution rates of 0.07, 0.11 and 0.38 h-', respectively. In their natural habitats, microorganisms are to various extents exposed to fluctuations in the availability of substrates. Some organisms are better adapted to conditions of nutrient starvation than others. The oligotrophic and copiotrophic marine bacteria are examples of organisms with extreme longevity (1, 25). On the contrary, the facultative and obligate anaerobic chemoheterotrophs studied thus far, i.e., Streptococcus lactis (36), S. faecalis, and other Streptococcus species (31), Staphylococcus epidermidis (11), Peptococcus prevotii (30), Ruminococcus flavefaciens (45), and Selenomonas ruminantium (22,23) are more sensitive to nutrient starvation and lose their viability within a few days.Factors that have been implicated in the survival of microorganisms during nutrient starvation are the possession of storage compounds (5), the presence of substrates for endogenous metabolism (4), the growth-limiting nutrient before starvation (22,23,29), the adenylate energy charge (12, 14), the energy of maintenance requirement (5), the maintenance of a proton motive force (16), and diminution of cell size (13, 25), and various other environmental and organism-specific parameters.The cytoplasmic membrane is the major barrier for separating the interior of the organism from its environment. To maintain this osmotic barrier function, which is vital for various cellular processes, the cell requires metabolic energy. Several sources of metabolic energy can be involved in the transport of solutes across the cytoplasmic membrane. The driving force for most solutes is the proton motive force or one of its components. Some solutes are translocated by ATP-dependent transport systems, whereas the uptake of some sugars can be mediated by phosphoenolpyruvate (PEP)-dependent group translocation systems (15). In this study, S. cremoris was used to investigate the effect of lactose starvation on several energetic and membraneassociated functions. S. cremoris is a strictly fermentative lactic acid bacterium which can ferment only a few carbohydrates. Substrate-level phosphorylation yields ATP, which is used partly to generate the transmembrane electrochemical proton gradient. S. cremoris is unable to consume endogenous substrates or to invoke any specialized mechanism to survive periods of nutrient starvation. Survival of energy starvation by S. lactis has been attributed to the maintenance of a large PEP pool (5, 43). These organisms do not possess metabolic energy in other storage compounds, which allows an exact determination of the transition from growth to energy starvation. This paper shows that c...

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)

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