Catabolism of Adenosine 5'-Monophosphate by Extracts of the Marine Bacterium Beneckea natriegens

Niven, Donald F.; Collins, P.; Knowles, Christopher J.

doi:10.1099/00221287-100-1-5

Cited by 10 publications

(6 citation statements)

References 23 publications

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“…Under conditions of starvation, there is in most bacteria a decrease in total adenylates, due primarily to removal of AMP from the adenylate pool by the enzymes adenosine monophosphate nucleosidase (17) or adenylate deaminase (11) or both. These mechanisms allow for the stabilization of the adenylate energy charge during unfavorable conditions.…”

Section: Resultsmentioning

confidence: 99%

Stability of the Adenosine 5′-Triphosphate Pool in Coxiella burnetii : Influence of pH and Substrate

Hackstadt

Williams

1981

J Bacteriol

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The ability of Coxiella burnetii to couple oxidation of metabolic substrates to adenosine 5'-triphosphate (ATP) synthesis in axenic reaction buffers was examined. Pyruvate, succinate, and glutamate were catabolized and incorporated at the highest rates of 11 substrates tested. Glutamate oxidation, however, resulted in the greatest stability of the ATP pool and highest intracellular ATP levels over a 48-h period. At pH 4.5, the optimum for metabolism by C. burnetii, glutamate oxidation resulted in maintenance of the ATP pool at a concentration of approximately 0.7 nmol of ATP per mg of dry weight over a 96-h period. In the absence of substrate, ATP declined by 96 h to less than 0.01 nmol/mg of dry weight. When cells were maintained at pH 7.0 in the presence or absence of glutamate, ATP pools were considerably more stable, presumably due to the miniimal metabolic activity displayed by C. burnetii at pH 7. The stability of the ATP pool reflected viability as there was greater than an 8-log decrease in viable C. burnetii after incubation for 7 days at pH 4.5 in the absence of glutamate. Viability was retained in the presence of glutamate at pH 4.5 or 7.0 in the absence of any added substrate. The stability of the ATP pool was due to endogenous synthesis of ATP coupled to substrate oxidation as shown by depression of ATP levels in the presence of inhibitors of electron transport or oxidative phosphorylation. In addition, the adenylate energy charge increased from an initial value of 0.57 to 0.73 during glutamate oxidation with a concomitant rise in the total adenylate pool size. C. burnetii therefore appears able to regulate endogenous ATP levels in response to substrate availability and pH, thus effecting a conservation of metabolic energy in neutral or alkaline environments. Such a mechanism has been proposed to play a role in the resistance of C. burnetii to environmental conditions and subsequent activation upon entry into the phagolysosome in which this organism replicates.

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Section: Resultsmentioning

confidence: 99%

Stability of the Adenosine 5′-Triphosphate Pool in Coxiella burnetii : Influence of pH and Substrate

Hackstadt

Williams

1981

J Bacteriol

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“…In succinate-limited cultures, the energy charge immediately dropped to 0-6 at the start of the stationary phase (Andersen & von Meyenburg, 1977). In contrast to these results, glucose-or succinate-limitation of B. natriegens did not cause a measurable decrease in energy charge and there was a slight increase in the adenylate pool size (Niven et al, 1977~). During growth on glucose, but not on succinate, volatile acids were produced.…”

Section: Introductionmentioning

confidence: 92%

“…Culture samples (0.8 ml) were collected rapidly into 0-2 ml 25 % (w/v) HClO, precooled to 4 "C in a spring-loaded syringe unit (Niven et al, 1977~). The supernatants from filtration (0.45 pm pore size filters) were also analysed.…”

Section: E T H O D Smentioning

confidence: 99%

“…296 N. N A Z L Y , I. S. C A R T E R A N D C. J. KNOWLES The effect of termination of growth on the adenine nucleotide composition of batch cultures, due to depletion of carbon or NH$+ from the medium, has been examined in E. coli strain B (Chapman et al, 1971 ;Walker-Simmons & Atkinson, 1977) and Beneckea natriegens (Niven et al, 1977~). (For simplicity, we will refer to these as 'carbon-limited' and ' nitrogen-limited ' cultures.)…”

Section: Introductionmentioning

confidence: 98%

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Adenine Nucleotide Pools During Starvation of Beneckea natriegens

1980

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The marine bacterium Beneckea natriegens was grown in batch culture on a glucose/ NH,+/salts medium; growth terminated due to either carbon or nitrogen depletion from the medium. Nitrogen-limited cultures converted part of the excess glucose into glycogen whereas the carbon-limited cultures formed little glycogen. Glycogen-rich cultures survived longer than glycogen-poor cultures during starvation. Little protein was utilized during starvation and RNA was degraded as the primary endogenous source of energy. Glycogen was consumed only when the RNA content had decreased to about a third of the growth value.The adenine nucleotide content of nitrogen-limited cultures increased at the start of the stationary phase but the energy charge remained at the growth value of 0.9 to 0.95. The maximum size of the adenine nucleotide pool depended on the concentration of glucose remaining in the medium at the start of the stationary phase but a limiting value of about 60 pmol ATP (g protein)-l was attained, compared with 12 to 14 pmol ATP (g protein)-l in exponentially growing cultures. During extended starvation of both glycogen-rich and glycogen-poor cultures, there was a large decrease in adenine nucleotide content, but the energy charge remained above 0-6 even when viability was very low. I N T R O D U C T I O NThere are many factors that can cause loss of viability of bacteria (Dawes, 1976). During long-term starvation, endogenous metabolites such as non-essential RNA, protein and reserve polymers (glycogen, poly-P-hydroxybutyrate, triacylglycerols and polyphosphate) act as energy sources permitting essential maintenance processes to occur, thereby preserving viability (Dawes & Senior, 1973). Under these circumstances loss of viability may be related to the inability to regenerate ATP due to depletion of endogenous metabolites and reserve polymers. This would be seen as a decrease in the adenine nucleotide content or as a decrease in the ATP : ADP and ATP : AMP ratios, which may be measured as a decrease in energy charge (Atkinson, 1968(Atkinson, , 1978Chapman & Atkinson, 1977;Knowles, 1977Knowles, ,1979.There have been few studies on the adenylate pools of starving bacteria. Chapman et uZ. (1 97 1) showed that, following nitrogen depletion from a glucose-containing growth medium, there was a gradual decrease in the intracellular energy charge of Escherichia cofi strain B from a growth value of about 0-8 to between 0.6 and 0-5 after 60 to 80 h, without loss of viability. The intracellular adenine nucleotide content also decreased during this period. After 60 to 80 h, a rapid decrease in energy charge occurred, coincident with a loss of viability. Montague & Dawes (1974) showed a similar relationship of decrease in energy charge and loss of viability during starvation of Peptococcus pre'votii, which does not form reserve polymers but utilizes RNA as the sole endogenous source of energy. 7 Present address: The College of the Resurrection, Mirfield, West Yorkshire WF14 OBN.

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“…Vibrio natriegens is a marine bacterium capable of rapid growth (generation time of 25-30 min in a succinate-salts medium) and which maintains an energy charge level of at least 0.90 for prolonged periods under conditions of starvation (Niven et al 1977a;Nazly et al 1980). AMP catabolism by extracts of V .…”

Section: Introductionmentioning

confidence: 99%

AMP metabolism by the marine bacterium Vibrio (Beneckea) natriegens: purification and properties of adenylate kinase

Ramotar¹,

Pickard²

1981

Can. J. Microbiol.

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Adenylate kinase (EC 2.7.4.3) has been purified 484-fold from extracts of Vibrio natriegens to a specific activity of 1350 μmol ADP formed∙min−1∙mg protein−1. The preparation was 97% pure as judged by gel electrophoresis and exhibited molecular weight values of 29 000 by gel filtration and 32 000 by SDS–gel electrophoresis. The isoelectric point was at pH 4.7. Only ATP (Km 0.067 mM), ADP (Km 0.45 mM), and AMP (Km 0.12 mM) exhibited high activity as substrates, though dATP or dAMP could serve as cosubstrates with AMP or ATP, respectively, at reduced rates. The equilibrium constant in the direction of ATP formation was 1.09, and the pH optimum in both directions was broad, from pH 7.2 to pH 7.6. Enzyme activity was sensitive to the thiolalkylating agents iodacetamide and p-chloromercuriphenyl sulfonate.

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Catabolism of Adenosine 5'-Monophosphate by Extracts of the Marine Bacterium Beneckea natriegens

Cited by 10 publications

References 23 publications

Stability of the Adenosine 5′-Triphosphate Pool in Coxiella burnetii : Influence of pH and Substrate

Stability of the Adenosine 5′-Triphosphate Pool in Coxiella burnetii : Influence of pH and Substrate

Adenine Nucleotide Pools During Starvation of Beneckea natriegens

AMP metabolism by the marine bacterium Vibrio (Beneckea) natriegens: purification and properties of adenylate kinase

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