Inorganic polyphosphate in the yeast Saccharomyces cerevisiae with a mutation disturbing the function of vacuolar ATPase

Tomaschevsky, A. A.; Ryasanova, L. P.; Kulakovskaya, T. V.; Kulaev, I. S.

doi:10.1134/s0006297910080158

Cited by 12 publications

(10 citation statements)

References 8 publications

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“…An alternative hypothesis is that the decrease in volutin formation is a pleiotropic effect due to an intrinsic physiological change in the vacuole, similar to what is seen when vacuoles are treated with an agent that raises vacuole pH [36], mutations that perturb energy balance [5], or vacuolar physiology [37]. This alternate hypothesis explains our data, as volutin granules are formed in all mutants tested.…”

Section: Deletion Strain Analysissupporting

confidence: 54%

Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>

Marshall¹,

Rosa²,

Sanchez³

et al. 2014

AiM

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The budding yeast Saccharomyces cerevisiae serves as an effective model organism for many cellular pathways including phosphate transport, accumulation, and storage. In S. cerevisiae, phosphate is actively transported across the plasma membrane via several phosphate carriers and is then transported into the acidic vacuole (roughly equivalent to the mammalian lysosome with degradative functions but with additional storage functions, such as calcium) where it is synthesized into volutin, a storage form of polyphosphate, found in many organisms. We have been studying volutin granule formation in wild type cells to determine the physiological requirements for formation and in mutants to determine the pathway by which the volutin biosynthetic proteins are transported to the vacuole. Undertaking an analysis of volutin formation in yeast vacuoles by blocking vacuole function with pharmacological agents, such as ionomycin and CCCP, we see that vacuole pH as well as vacuolar calcium seems critical for volutin formation. Different blocks in vacuolar protein sorting have differential effects on volutin granule accumulation, with volutin granule formation seen in all mutant strains thus far tested, except for vps33, a mutant cell strain lacking all vacuolar structure. Our data are consistent with pleiotrophic effects of vacuolar physiological function blocks leading to a decrease in volutin formation.

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Section: Deletion Strain Analysissupporting

confidence: 54%

Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>

Marshall¹,

Rosa²,

Sanchez³

et al. 2014

AiM

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“…The HMW polyP content was higher in S. coelicolor and in the ppk mutant compared to the wild type S. lividans at 42 h and 60 h. This higher content might be linked to their active oxidative phosphorylation (see discussion). Indeed, several authors proposed that the synthesis of polyP, as that of ATP, directly involves oxidative phosphorylation 31, 32 . The content of MMW polyP of S. coelicolor and the ppk mutant decreased abruptly in the 42 h–60 h and 60 h–80 h periods, respectively (Fig.…”

Section: Resultsmentioning

confidence: 99%

Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145

Esnault

Dulermo

Smirnov

et al. 2017

Sci Rep

133

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The Streptomyces genus is well known for its ability to produce bio-active secondary metabolites of great medical interest. However, the metabolic features accompanying these bio-productions remain to be defined. In this study, the comparison of related model strains producing differing levels of actinorhoddin (ACT), showed that S. lividans, a weak producer, had high TriAcylGlycerol (TAG) content indicative of a glycolytic metabolism. In contrast, the strong producer, S. coelicolor, was characterized by low TAG content, active consumption of its polyphosphate (PolyP) stores and extremely high ATP/ADP ratios. This indicated highly active oxidative metabolism that was correlated with induction of ACT biosynthesis. Interestingly, in conditions of phosphate limitation, the ppk mutant had TAG content and ACT production levels intermediary between those of S. lividans and S. coelicolor. This strain was characterized by high ADP levels indicating that Ppk was acting as an Adenosine Di Phosphate Kinase. Its absence resulted in energetic stress that is proposed to trigger an activation of oxidative metabolism to restore its energetic balance. This process, which is correlated with ACT biosynthesis, requires acetylCoA to fuel the Krebs cycle and phosphate for ATP generation by the ATP synthase coupled to the respiratory chain, resulting in low TAG and polyP content of the ACT producing strains.

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“…Interestingly, in mammalian cells the inhibition of the ATP synthase and/or the disruption of the proton gradient, correlated with a lower polyP content [ 29 ]. Similarly, in the yeast Saccharomyces cerevisiae , inhibition of a vacuolar ATPase known to be involved in H + gradient formation, was also correlated with a lower polyP content [ 30 ]. In both cases the authors proposed that the synthesis of polyP, as that of ATP, directly involves oxidative phosphorylation.…”

Section: Discussionmentioning

confidence: 99%

“…We thus propose that this higher ATP content might, at least in part, be due to the de-repression of oxidative phosphorylation in the phoP mutant. High oxidative phosphorylation activity might also have a direct (as hypothesized in [ 29 ] and [ 30 ]) or indirect (via ATP synthesis and polymerization by Ppk) positive impact on HMW polyP synthesis. However, we rather believe that the greater abundance of HMW polyP in the mutant is due to the less efficient degradation of these polymers into shorter forms and Pi.…”

Section: Discussionmentioning

confidence: 99%

Phosphate Homeostasis in Conditions of Phosphate Proficiency and Limitation in the Wild Type and the phoP Mutant of Streptomyces lividans

et al. 2015

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Phosphate, as a constituent of the high energy molecules, ATP/GTP and polyphosphate, plays a crucial role in most of the metabolic processes of living organisms. Therefore, the adaptation to low Pi availability is a major challenge for bacteria. In Streptomyces, this adaptation is tightly controlled by the two component PhoR/PhoP system. In this study, the free intracellular Pi, ATP, ADP and polyP content of the wild type and the phoP mutant strain of S. lividans TK24 were analyzed at discrete time points throughout growth in Pi replete and limited media. PolyP length and content was shown to be directly related to the Pi content of the growth medium. In Pi repletion, ATP and high molecular weight (HMW) polyP contents were higher in the phoP mutant than in the WT strain. This supports the recently proposed repressive effect of PhoP on oxidative phosphorylation. High oxidative phosphorylation activity might also have a direct or indirect positive impact on HMW polyP synthesis. In Pi sufficiency as in Pi limitation, the degradation of these polymers was shown to be clearly delayed in the phoP mutant, indicating PhoP dependent expression of the enzymes involved in this degradation. The efficient storage of Pi as polyphosphate and/or its inefficient degradation in Pi in the phoP mutant resulted in low levels of free Pi and ATP that are likely to be, at least in part, responsible for the very poor growth of this mutant in Pi limitation. Furthermore, short polyP was shown to be present outside the cell, tightly bound to the mycelium via electrostatic interactions involving divalent cations. Less short polyP was found to be associated with the mycelium of the phoP mutant than with that of the WT strain, indicating that generation and externalization of these short polyP molecules was directly or indirectly dependent on PhoP.

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Inorganic polyphosphate in the yeast Saccharomyces cerevisiae with a mutation disturbing the function of vacuolar ATPase

Cited by 12 publications

References 8 publications

Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>

Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>

Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145

Phosphate Homeostasis in Conditions of Phosphate Proficiency and Limitation in the Wild Type and the phoP Mutant of Streptomyces lividans

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Inorganic polyphosphate in the yeast Saccharomyces cerevisiae with a mutation disturbing the function of vacuolar ATPase

Cited by 12 publications

References 8 publications

Analysis of Volutin Granule Formation in &lt;i&gt;Saccharomyces cerevisiae&lt;/i&gt;

Analysis of Volutin Granule Formation in &lt;i&gt;Saccharomyces cerevisiae&lt;/i&gt;

Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145

Phosphate Homeostasis in Conditions of Phosphate Proficiency and Limitation in the Wild Type and the phoP Mutant of Streptomyces lividans

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Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>

Analysis of Volutin Granule Formation in <i>Saccharomyces cerevisiae</i>