Energy metabolism in Streptococcus cremoris during lactose starvation

Otto, R.; Vije, J; Tenbrink, B; Klont, B.; Konings, Wn

doi:10.1007/bf00428848

Cited by 24 publications

(23 citation statements)

References 16 publications

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“…Starving cells degrade their proteins in one to two hours following the onset of carbohydrate starvation. After this period the polypeptide pool is stable with half-lifes of more than 40 h. Since the pool of energy-rich intermediates ("PEP-pool", A T P and proton motive force) gradually decreases to "zero" (levels below the detection limits) in the first one to two hours of starvation (Otto et al 1985;Poolman et al 1987a), it is most likely that the degradation (turnover) of proteins is an energy-requiring process. The metabolic energy for protein degradation may be required for the unfolding of the polypeptides, the activation of proteases and/or the cleavage ofpeptide-bonds (Hershko and Ciechanover 1982;Olden and Goldberg 1978; W a x m a n and Goldberg 1986).…”

Section: Discussionmentioning

confidence: 99%

“…In the first hour(s) of lactose starvation ofL. lactis, when culture is still fully viable, ATP levels fall to concentrations below 0.1 mM, and the membrane potential (A ~) and pH gradient (ApH) collapse (Otto et al 1985;Poolman et al 1987b). In the initial phase of starvation a transient increase in "PEP-pool" intermediates (3-phosphoglycerate, 2-phosphoglycerate and phosphoenolpyruvate) has been observed (Mason et al i981;Otto et al 1985;Poolman et al 1987a; Thompson and Thomas 1977).…”

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confidence: 99%

“…lactis, when culture is still fully viable, ATP levels fall to concentrations below 0.1 mM, and the membrane potential (A ~) and pH gradient (ApH) collapse (Otto et al 1985;Poolman et al 1987b). In the initial phase of starvation a transient increase in "PEP-pool" intermediates (3-phosphoglycerate, 2-phosphoglycerate and phosphoenolpyruvate) has been observed (Mason et al i981;Otto et al 1985;Poolman et al 1987a; Thompson and Thomas 1977). The decrease of the PEP-pool intermediates during later phases of starvation has been attributed to the inhibition of pyruvate kinase by inorganic phosphate (Mason et al 1981; Thompson and Thomas 1977;Thompson 1978, Thompson andTorchia 1984) and the decrease of fructose 1,6-diphosphate (activator of pyruvate kinase; feedforward control of glycolysis) (Konings et al 1989;Poolman et al 1987a;Thompson 1978).…”

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Physiological responses of Lactococcus lactis ML3 to alternating conditions of growth and starvation

et al. 1993

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Abstract.Lactococcus lact& species can survive periods of carbohydrate starvation for relatively long periods of time. In the first hours of starvation, however, the maximal glycolytic and arginine deiminase (ADI) pathway activities decline rapidly. The rate of decrease of the pathway activities diminishes as soon as the cells become depleted of energy-rich intermediates. Loss of glycolytic activity is associated with loss of glyceraldehyde 3-phosphate dehydrogenase, phosphoglycerate mutase and pyruvate kinase activities. Upon addition of sugar to starved cultures these enzymatic, and thus the glycolytic, activities can be restored to 100% values. The recovery of enzymatic activities is inhibited by chtoramphenicol, indicating that protein synthesis is involved. In contrast, restoration of ADI pathway activity does not require de novo synthesis of proteins. General protein degradation and synthesis have been studied in growing and starving cells using [35S]methionine-labeling of proteins and twodimensional gel analysis. The breakdown of bulk proteins in exponentially growing cells shows first-order rate kinetics (t~ of approximately 5 h). Following an initial breakdown of proteins with a tz ~ of 5 h during the first hour(s) of starvation, bulk proteins are degraded very slowly in starving energy-depleted cells. The breakdown of proteins during starvation appears to be (largely) nonspecific. The rate of synthesis of proteins decreases rapidly in the first hour(s) of starvation. From the onset of starvation on at least 45 proteins are no longer synthesized. During starvation relative induction of fourteen to fifteen proteins can be observed.

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Physiological responses of Lactococcus lactis ML3 to alternating conditions of growth and starvation

et al. 1993

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“…Within 10 h of lactose starvatioi maximal rate of glycolysis had fallen to less than 10% ( activity in the growing culture. The decreased activi glycolysis is expressed as a diminished rate of ATP syni (28) and consequently as a decreased ability to regenei proton motive force. The capacity to generate a A& ZApH is given as the time required to reach steady values.…”

Section: Methodsmentioning

confidence: 99%

“…There have been conflicting reports on the role of Pi in the regulation of pyruvate kinase (20,28,44). The increase in the PEP pool in streptococci when the starvation phase was entered has been attributed to the inhibition of pyruvate kinase by Pi (20,44).…”

Section: Methodsmentioning

confidence: 99%

Bioenergetic consequences of lactose starvation for continuously cultured Streptococcus cremoris

Poolman¹,

Smid²,

Veldkamp³

et al. 1987

J Bacteriol

112

104

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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...

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