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Different Mechanisms of Energy Coupling for the Active Transport of Proline and Glutamine in Escherichia Coli

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Different Mechanisms of Energy Coupling for the Active Transport of Proline and Glutamine in Escherichia Coli Proc. Nat. Acad. Sci. USA Vol. 70, No. 5, pp. 1514-1518, May 1973 Different Mechanisms of Energy Coupling for the Active Transport of Proline and Glutamine in Escherichia coli (inhibitors/mutants/ATP/energized membrane state/starvation) EDWARD A. BERGER Section of Biochemistry, Molecular and Cell Biology, Wing Hall, Cornell University, Ithaca, New York 14850 Communicated by Leon A. Heppel, March 15, 1973 ABSTRACT The ability of either glucose or D-lactate to the ATPase inhibitor NN-dicyclohexylcarbodiimide (4), to energize active transport of amino acids in E. coli was as well as the loss of thiomethyl- studied in starved cells blocked at specific sites of energy from cyanide-resistant metabolism. Proline uptake could be driven by either galactoside uptake in an ATPase mutant (5). oxidative or substrate-level processes. The oxidative path- Energy for active transport can thus be derived indepen- way was sensitive to cyanide but not to arsenate, and dently from either respiration or ATP hydrolysis. The ob- operated normally in a mutant deficient in the Ca, Mg- servations (4, 7) that uptake driven by either pathway is dependent ATPase. The substrate-level pathway, which was active with glucose but not with D-lactate as the car- sensitive to uncouplers of oxidative phosphorylation has led bon source, was sensitive to arsenate but not to cyanide, several workers (4-8) to propose that a high-energy membrane and required a functional ATPase. Uncouplers prevented state is the immediate energy donor for bacterial transport, the utilization of energy for proline uptake by either path- though other models have recently been formulated (3, 9). way. Since this conclusion is based upou studies with only a few Energy coupling for glutamine uptake was quite differ- ent. The oxidative pathway was sensitive to cyanide and uptake systems, it is necessary to identify the energy donors uncouplers and, in contrast with proline, required an for the active transport of other metabolites before any active ATPase. The glycolytic component was resistant to generalizations can be applied. cyanide and uncouplers, and functioned normally in the In this study, the ability of different carbon sources to ATPase mutant: Arsenate abolished glutamine transport provide energy for active transport was investigated in energized by either pathway. The results suggest that proline transport is driven starved E. coli cells blocked at specific sites of energy me- directly by an energy-rich membrane state, which can be tabolism. By the judicious choice of energy sources and in- generated by either electron transport or ATP hydrolysis. hibitors, it is possible to distinguish whether respiration per se, Glutamine uptake, on the other hand, is apparently the energized membrane state, or phosphate-bond energy is driven directly by phosphate-bond energv formed by way of oxidative or substrate-level phosphorylations. the obligatory energy donor for a particular system. For example, glucose can provide ATP by either oxidative phos- Early investigations of bacterial active transport have im- phorylation, which requires both electron transport and a plicated the high-energy phosphate bond in the energy- functional Ca,Mg-ATPase, or by the substrate-level phos- coupling process (1, 2). Recent evidence, however, suggests phorylations of glycolysis, which require neither process. that the role of ATP is probably indirect. The extensive Glucose can also give rise to an energy-rich membrane state studies of Kaback and his colleagues (3) demonstrated that by two pathways: through hydrolysis of glycolytic ATP by membrane vesicles incapable of oxidative phosphorylation can ATPase in the presence or absence of respiration, or through still use respiration to drive the uptake of a wide variety of the oxidations of the respiratory chain, which may occur in amino acids and sugars. Klein and Boyer recently showed (4) the absence of ATPase. Alternatively, D-lactate is oxidized that aerobic proline transport in intact cells of Escherichia directly by a membrane-bound dehydrogenase coupled to the coli is retained under conditions where intracellular ATP and cytochrome chain (3), and can provide energy only in the phosphoenolpyruvate levels are drastically reduced by presence of electron transport. The synthesis of ATP re- arsenate. Furthermore, a functional Ca,Mg-dependent quires an active ATPase, whereas the generation of the ATPase is not required for aerobic accumlation of thiomethyl- energized membrane state does not. galactoside (5) or proline (4, 6), confirming that transport The results presented here confirm the suggestions of can proceed independently of oxidative phosphorylation. others (4, 6) that proline uptake is driven by the energized While it is clear that the respiration-linked uptake of certain membrane state. Glutamine transport, on the other hand, is substrates does not involve the formation or use of high-energy driven directly by phosphate-bond energy formed by either phosphates, these same transport systems can apparently be oxidative phosphorylation or glycolysis. energized by an alternate nonoxidative mechanism that MATERIALS AND METHODS uses ATP. E. coli is able to accumulate various substrates anaerobically (4, 7), and it has been shown for proline that Bacterial Strains. E. coli ML 308-225 and its derivative anaerobic uptake is abolished by arsenate (4). The essential DL-54 were the generous gifts of Dr. Robert D. Simoni. role of the Ca, Mg-ATPase in the use of ATP for transport is DLh54 is missing more than 95% of the Ca,Mg-ATPase inferred from the sensitivity of anaerobic proline accumulation activity and is unable to grow on carbon sources that re- quire oxidative phosphorylation for ATP formation (6). Abbreviation: FCCP, carbonyl cyanide-p-trifluoromethoxy- Chemicals. L- [ U_14C]proline and - [ U-'4C]glutamine were phenylhydrazone. purchased from New England Nuclear Corp. The isotopes 1514 Downloaded by guest on October 1, 2021 Proc. Nat. Acad. Sci. USA 70 (1973) Energy Coupling Mechanisms for Active Transport 1515 were diluted with nonradioactive amino acids to final specific the endogenous rates of proline uptake in unstarved cells activities of 20-25 Ci/mol. 2,4-Dinitrophenol was purchased were so high as to partially or completely mask the effects from Sigma. Carbonyl cyanide-p-trifluoromethoxyphenyl- of glucose or D-lactate. Glutamine uptake in the absence of hydrazone (FCCP) was a gift from Dr. Efraim Racker. All added carbon source was not as high, suggesting that the two other compounds were analytical grade. transport systems might be using different energy stores. Several starvation methods were examined for their ability Growth of Cells. Bacteria were grown in a synthetic, phos- to deplete endogenous energy reserves. Vigorous overnight phate-buffered minimal medium (10) supplemented with 11 aeration of the cells at 370 in the presence or absence of thio- mM glucose as a carbon source. Optical density at 600 nm methylgalactoside failed to reduce endogenous rates of was monitored with a Gilford spectrophotometer model 240 proline transport significantly. Incubation with a-methyl- (OD600 of 1 corresponded to 109 cells per ml). Cultures were glucoside in the presence of sodium azide (14) was more innoculated to an OD of about 0.2 and were allowed to grow effective, though the inhibitory effects of azide on transport at 370 on a gyratory shaker for about two generations. The could not be completely reversed by washing. The most cells were harvested by centrifugation, washed twice with satisfactory results were obtained with the uncoupler dini- minimal medium at 230, and suspended in 20 ml of minimal trophenol. Table 1B shows that incubation of ML 308-225 medium per g wet weight of cells. This suspension was used with 5 mM dinitrophenol for 10 hr at 370, followed by ex- directly for transport experiments with unstarved cells. tensive washing, reduced the endogenous rates of proline Starvation of Cells. Washed cells were suspended in minimal uptake sufficiently to permit large stimulations by added medium containing 5 mM dinitrophenol at a density of 1 g energy sources. Furthermore, the transport rates in the (wet weight) of cells per 200 ml. The suspension was incubated presence of glucose and D-lactate were very similar to those at 370 with shaking for 10 hr for ML 308-225, or for 1 hr. with observed with unstarved cells (Table 1A). DL-54. The cells were then isolated by centrifugation, washed DL-54 was much more sensitive to this starvation procedure three times in minimal medium, and suspended in 20 volumes than the wild type. Incubations as short as 30 min greatly of minimal medium per g of cells for transport assays. reduced endogenous rates of proline uptake in this strain, while they had little effect on ML 308-225. If the dinitro- Transport Assay. A reaction flask containing cells (100-200 phenol treatment was continued beyond 2 hr with the mutant, ,ug of protein), chloramphenicol (80,4g/ml), and inhibitors- endogenous uptake rates were reduced below detectable where designated-was incubated at 370 for 5 min. 11 mM limits, but the rates with added energy sources also began Glucose or 10 mM D-lactate were added and the incubation to decline. A 1-hr incubation was therefore chosen for D1h54, was continued for 10 min. The flask was brought to room since as shown in Table 1B, endogenous proline transport temperature and the transport reaction was initiated by the was adequately depleted and the rates of glucose- and D- addition of labeled amino acid to a concentration of 10 AM. lactate-supported uptake of both proline and glutamine were The final volume of the mixture was 0.5 ml. At various times, similar to those in unstarved cells. 0.2-ml aliquots were withdrawn, filtered on 25-mm nitro- The dinitrophenol starvation procedure thus permitted cellulose filters (0.45 Mm, Matheson-Higgins), and washed assessment of the ability of different energy sources to stimu- with 10 ml of a solution containing 0.01 M Tris HCl (pH late transport, and starved cells were used in the remainder 7.3)-0.15 M NaCl-0.5 mM MgCl2 (11) at 230.
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