The molecular composition of the volutin granule of yeast

Jacobson, Lewis A.; Halmann, M.; Yariv, J.

doi:10.1042/bj2010473

Cited by 38 publications

(28 citation statements)

References 17 publications

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“…For C. utilis cells this number ranges from 20-40 which is consistent with previous reports upon vacuolar PP in yeasts (Urech et al 1978). PP with mol.wt, up to 250,000 yields relatively sharp 3 ~p NMR resonances (Jacobson et al 1982). Hence, it is likely that all polyphosphate in yeast is observed by 3 ~p NMR unless it is immobilized by complexation into rigid, high molecular weight structures.…”

Section: Discussionsupporting

confidence: 78%

Phosphorus-31 nuclear magnetic resonance studies of intracellular pH, phosphate compartmentation and phosphate transport in yeasts

et al. 1982

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Abstract. 31p NMR spectra were obtained from suspensions of Candida utilis, Saccharomyces cerevisiae and Zygosaccharomyces bailii grown aerobically on glucose. Direct introduction of substrate into the cell suspension, without interruption of the measurements, revealed rapid changes in pH upon addition of the energy source. All 3 ~p NMR spectra of the yeasts studied indicated the presence of two major intracellular inorganic phosphate pools at different pH environments. The pool at the higher pH was assigned to cytoplasmic phosphate from its response to glucose addition and iodoacetate inhibition of glycolysis. After addition of substrate the pH in the compartment containing the second phosphate pool decreased. A parallel response was observed for a significant fraction of the terminal and penultimate phosphates of the polyphosphate observed by 3 ~p NMR. This suggested that the inorganic phosphate fraction at the lower pH and the polyphosphates originated from the same intracellular compartment, most probably the vacuole. In this vacuolar compartment, pH is sensitive to metabolic conditions. In the presence of energy source a pH gradient as large as 0.8 to 1.5 units could be generated across the vacuolar membrane. Under certain conditions net transport of inorganic phosphate across the vacuolar membrane was observed during glycolysis: to the cytoplasm when the cytoplasmic phosphate concentration had become very low due to sugar phosphorylation, and into the vacuole when the former concentration had become high again after glucose exhaustion.

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Section: Discussionsupporting

confidence: 78%

Phosphorus-31 nuclear magnetic resonance studies of intracellular pH, phosphate compartmentation and phosphate transport in yeasts

et al. 1982

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“…Long chain polyphosphates have also commonly been extracted from fungal tissue. They usually co-exist with polyphosphates of shorter chain lengths (Harold, 1966;Bennett & Scott, 1971;Callow et al, 1978;Beever &;Burns, 1980;Jacobson, Halmann & Yariv, 1982;Kulaev & Vagabov, 1983;Straker & Mitchell, 1985). The occurrence of a short chain polyphosphate in the vacuoles of Pisolithus tinctorius is consistent w-ith the demonstrated acid solubility of metachromatic vacuolar granules in chemically-fixed Pisolithus tinctorius sections by 5 % cold TCA Orlovich & Ashford, 1993); only polyphosphates of low molecular weight are labile with this treatment (Dawes & Senior, 1973).…”

Section: Discussionmentioning

confidence: 99%

Demonstration of a short chain polyphosphate in Pisolithus tinctorius and the implications for phosphorus transport

1994

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SUMMARYPolyphosphate was extracted from an Australian isolate oi Pisolithus tinctorius (Pers.) Coker & Couch, known to he mycorrhizal with Eucalyptus pilularis. It was separated from RNA and characterized hy PAGE and ^^F NMR spectroscopy. A broad pink hand, which showed y-metachromasy with toiuidine blue, ran faster on acrylamide gels than a number of purple-blue bands (various RNA fractions) and did not stain with ethidium bromide, was identified as polyphosphate. The major pink band co-migraied with a synthetic polyphosphate standard of a chain length of about 1 5 phosphate (PJ subunits, and analysis by ^^P nuclear magnetic resonance (NMR) spectroscopy confirmed that polyphosphate was a major fraction in the extract. Polyphosphate was extracted from mycelium grown at both high and low levels of P,, but the amount extracted from cultures grown with 10 mM P, (added as ammonium phosphate) was significantly greater, Polyphosphate was a substantial fraction of the phosphorus present in the hyphae and it is proposed that polyphosphate is transported along the hyphae by the motile tubule and vacuole system present in this fungus.

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“…Their metachromatic nature is attributable to the reaction of the polyphosphate (polyP) 1 present in the granules with certain basic dyes, such as toluidine blue, which induces a characteristic shift in their absorption spectrum to a higher wavelength (10). They have been described as devoid of internal structure or limiting membrane (11) and have also been found in unicellular eukaryotes (12)(13)(14)(15)(16). In recent years, volutin granules of unicellular eukaryotes such as Chlamydomonas reinhardtii (17), Dictyostelium discoideum (18), and a number of human pathogens, including malaria parasites, Toxoplasma gondii, and trypanosomatids (19), were found to be surrounded by a membrane with a number of pumps and exchangers and were named acidocalcisomes.…”

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confidence: 99%

Identification of Organelles in Bacteria Similar to Acidocalcisomes of Unicellular Eukaryotes

Seufferheld

Vieira

Ruiz

et al. 2003

Journal of Biological Chemistry

166

141

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Acidocalcisomes are acidic calcium storage compartments described in several unicellular eukaryotes, including trypanosomatid and apicomplexan parasites, algae, and slime molds. In this work, we report that the volutin granules of Agrobacterium tumefaciens possess properties similar to the acidocalcisomes. Transmission electron microscopy revealed that each intracellular granule was surrounded by a membrane. X-ray microanalysis of the volutin granules showed large amounts of phosphorus, magnesium, potassium, and calcium. Calcium in the volutin granules increased when the bacteria were incubated at high extracellular calcium concentration. Immunofluorescence and immunoelectron microscopy, using antisera raised against peptide sequences conserved in the A. tumefaciens proton pyrophosphatase, indicated localization in intracellular vacuoles. Purification of the volutin granules using iodixanol density gradients indicated a preferential localization of the pyrophosphatase activity in addition to high concentrations of phosphate, pyrophosphate, short-and long-chain polyphosphate, but lack of markers of the plasma membrane. The pyrophosphatase activity was potassium-insensitive and inhibited by the pyrophosphate analogs, amynomethylenediphosphonate and imidodiphosphate, by dicyclohexylcarbodiimide, and by the thiol reagent N-ethylmaleimide. Polyphosphate was also localized to the volutin granules by 4,6-diamino-2-phenylindole staining. The organelles were acidic, as demonstrated by staining with LysoSensor blue DND-167, a dye especially used to detect very acidic compartments in cells, and cycloprodigiosin, a compound isolated from a marine bacterium that has been shown to uncouple proton pyrophosphatase activity acting as a chloride/proton symport. The results suggest that acidocalcisomes arose before the prokaryotic and eukaryotic lineages diverged.

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The molecular composition of the volutin granule of yeast

Cited by 38 publications

References 17 publications

Phosphorus-31 nuclear magnetic resonance studies of intracellular pH, phosphate compartmentation and phosphate transport in yeasts

Phosphorus-31 nuclear magnetic resonance studies of intracellular pH, phosphate compartmentation and phosphate transport in yeasts

Demonstration of a short chain polyphosphate in Pisolithus tinctorius and the implications for phosphorus transport

Identification of Organelles in Bacteria Similar to Acidocalcisomes of Unicellular Eukaryotes

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