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Bioenergetic characterization of transient state phosphate uptake by the cyanobacterium Anacystis nidulans

Theoretical and experimental basis for a sensory mechanism adapting to varying environmental phosphate levels

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Abstract

A force flow relationship based on nonequilibrium thermodynamics was derived to analyze the variable transient state phosphate uptake phenomena of cyanobacteria seen under different growth conditions and external phosphate concentrations. This relationship postulates the following basic properties of the uptake system: First, a threshold value exists, below which incorporation is energetically impossible. Second, threshold values are influenced by the activity of the phosphate uptake system, such that a decrease of the activity increases the threshold level. Third, near the thermodynamic equilibrium the uptake rate is linearly dependent on the free energy of polyphosphate formation and the pH-gradient at the thylakoid membrane. Experiments performed with Anacystis nidulans showed that phosphate uptake characteristics conformed to the properties predicted by the linear force-flow relationship. Linearity extented into regions far form thermodynamic equilibrium, e.g. to high phosphate concentrations, when algae were preconditioned to high phosphate levels. Under phosphate limited growth linearity was confined to a small concentration range, threshold values decreased below 10 nM, and the external concentration approached threshold. The data suggest that the uptake system responds to changes in the external phosphate concentration in the same way as sensory systems to input stimuli by amplifying signals and adapting to them.

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Abbreviations

chl:

chlorophyll

H +e , H +C , H +T :

protons in the external medium, the cytoplasmic and thylakoid space respectively

Pc :

phosphate in the cytoplasmic space

Pe :

phosphate in the external medium

Pn, Pn+1 :

polyphosphates

ΔpHT :

pH-gradient across the thylakoid membrane

References

  • Falkner G, Werdan K, Horner F, Heldt HW (1976) pH-changes in the cytoplasm of the blue green alga Anacystis nidulans caused by light-dependent proton flux into the thylakoid space. Plant Physiol 58:717–718

    Google Scholar 

  • Falkner G, Horner F, Simonis W (1980) The regulation of the energy-dependent phosphate uptake by the blue-green alga Anacystis nidulans. Planta 149:138–143

    Google Scholar 

  • Falkner G, Strasser P, Graffius D (1984) Phosphate uptake by blue green algae in vitro and in a lake during an algal bloom: Useful application of a force-flow relationship. Hydrobiologia 108:265–271

    Google Scholar 

  • Healey FP (1982) Phosphate. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Botanical monographs, vol 19. Blackwell, Oxford London Edinburgh Boston Melbourne, pp 105–124

    Google Scholar 

  • Kedem O, Caplan SR (1965) Degree of coupling and its relation to efficiency of energy conversion. Trans Faraday Soc 61:1897–1911

    Google Scholar 

  • Koshland DE jr, Goldbeter A, Stock JB (1982) Amplification and adaptation in regulatory and sensory systems. Science 217:220–225

    Google Scholar 

  • Kuenzler EJ, Ketchum BH (1962) Rate of phosphorus uptake by Phaeodactylum tricornutum. Biol Bull Woods Hole 123:134–145

    Google Scholar 

  • Kuhl A (1974) Phosphorus. In: Stewart WDP (ed) Algal physiology and biochemistry. Botanical monographs, vol 10. University of California Press, Berkeley Los Angeles, pp 636–654

    Google Scholar 

  • Kulaev IS, Vagabov VM (1983) Polyphosphate metabolism in micro organisms. Adv Microbial Physiol 24:83–171

    Google Scholar 

  • Lawry NH, Jensen TE (1979) Deposition of condensed phosphate as an effect of varying sulfur deficiency in the cyanobacterium Synechoccus sp (Anacystis nidulans). Arch Microbiol 120:1–7

    Google Scholar 

  • MacKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322

    Google Scholar 

  • Nielsen SO, Lehninger AL (1955) Phosphorylation coupled to the oxidation of ferrocytochrome c. J Biol Chem 215:555–570

    Google Scholar 

  • Odum HT, Pinkerton RC (1955) Time's speed regulator: The optimum efficiency for maximum power output in physical and biological systems. Am Sci 43:331–343

    Google Scholar 

  • Rigler FH (1956) A tracer study of phosphorus cycle in lake water. Ecology 37:550–562

    Google Scholar 

  • Riegman R (1985) Phosphate-phytoplankton interactions. Academisch Proefschrift (Thesis) University of Amsterdam

  • Robertson BR, Button DK (1979) Phosphate limited continuous culture of Rhodotorula rubra: Kinetics of transport, leakage and growth. J Bacteriol 138:884–895

    Google Scholar 

  • Simonis W, Urbach W (1973) Photophosphorylation in vivo. Ann Rev Plant Physiol 24:89–114

    Google Scholar 

  • Stucki JW, Compiani M, Caplan SR (1983) Efficiency of energy conversion in model biological pumps. Optimization by linear nonequilibrium thermodynamic relations. Bipohysical Chemistry 18:101–109

    Google Scholar 

  • Thellier M (1970) An electrokinetic interpretation of the functioning of biological systems and its application to the study of mineral salts absorption. Ann Bot 34:983–1009

    Google Scholar 

  • Trevorrow K, Haynes DH (1984) The thermodynamic efficiency of the Ca2+−Mg2+-ATPase is one hundred percent. J Bioenerg Biomembr 16:53–59

    Google Scholar 

  • Ullrich-Eberius CI, Novacky A, van Bel AJE (1984) Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta 161:46–52

    Google Scholar 

  • Yoshida A (1955) Studies on metaphosphate. II. Heat of hydrolysis of metaphosphate extracted from yeast cells. J Biochem (Tokyo) 42:163–168

    Google Scholar 

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Falkner, G., Falkner, R. & Schwab, A.J. Bioenergetic characterization of transient state phosphate uptake by the cyanobacterium Anacystis nidulans . Arch. Microbiol. 152, 353–361 (1989). https://doi.org/10.1007/BF00425173

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  • DOI: https://doi.org/10.1007/BF00425173

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