Skip to main content
NCBI home page
Plant Physiology logoLink to Plant Physiology
. 1990 Nov;94(3):1116–1123. doi: 10.1104/pp.94.3.1116

Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum1

I. Regulation of Carbon Metabolism and Succinate as a Fermentation Product

Greg C Vanlerberghe 1, Regina Feil 1, David H Turpin 1
PMCID: PMC1077350  PMID: 16667805

Abstract

The onset of anaerobiosis in darkened, N-limited cells of the green alga Selenastrum minutum (Naeg.) Collins elicited the following metabolic responses. There was a rapid decrease in energy charge from 0.85 to a stable lower value of 0.6 accompanied by rapid increases in pyruvate/phosphoenolpyruvate and fructose-1,6-bisphosphate/fructose-6-phosphate ratios indicating activation of pyruvate kinase and 6-phosphofructokinase, respectively. There was also a large increase in fructose-2,6-bisphosphate, which, since this alga lacks pyrophosphate dependent 6-phosphofructokinase, can be inferred to inhibit gluconeogenic fructose-1,6-bisphosphatase activity. These changes resulted in an approximately twofold increase in the rate of starch breakdown indicating a Pasteur effect. The Pasteur effect was accompanied by accumulation of d-lactate, ethanol and succinate as fermentation end-products, but not malate. Accumulation of succinate was facilitated by reductive carbon metabolism by a partial TCA cycle (GC Vanlerberghe, AK Horsey, HG Weger, DH Turpin [1989] Plant Physiol 91: 1551-1557). An initial stoichiometric decline in aspartate and increases in succinate and alanine suggests that aspartate catabolism provides an initial source of carbon for reduction to succinate under anoxic conditions. These observations allow us to develop a model for the regulation of anaerobic carbon metabolism and a model for short-term and long-term strategies for succinate accumulation in a green alga.

Full text

PDF
1116

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Botha F. C., Turpin D. H. Fructose 1,6-Bisphosphatase in the Green Alga Selenastrum minutum: I. Evidence for the Presence of Isoenzymes. Plant Physiol. 1990 Aug;93(4):1460–1465. doi: 10.1104/pp.93.4.1460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Botha F. C., Turpin D. H. Molecular, Kinetic, and Immunological Properties of the 6-Phosphofructokinase from the Green Alga Selenastrum minutum: Activation during Biosynthetic Carbon Flow. Plant Physiol. 1990 Jul;93(3):871–879. doi: 10.1104/pp.93.3.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Effer W. R., Ranson S. L. Respiratory metabolism in buckwheat seedlings. Plant Physiol. 1967 Aug;42(8):1042–1052. doi: 10.1104/pp.42.8.1042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Englander S. W., Calhoun D. B., Englander J. J. Biochemistry without oxygen. Anal Biochem. 1987 Mar;161(2):300–306. doi: 10.1016/0003-2697(87)90454-4. [DOI] [PubMed] [Google Scholar]
  5. Gfeller R. P., Gibbs M. Fermentative Metabolism of Chlamydomonas reinhardtii: I. Analysis of Fermentative Products from Starch in Dark and Light. Plant Physiol. 1984 May;75(1):212–218. doi: 10.1104/pp.75.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Givan C. V. Short-term Changes in Hexose Phosphates and ATP in Intact Cells of Acer pseudoplatanus L. Subjected to Anoxia. Plant Physiol. 1968 Jun;43(6):948–952. doi: 10.1104/pp.43.6.948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hirt G., Tanner W., Kandler O. Effect of Light on the Rate of Glycolysis in Scenedesmus obliquus. Plant Physiol. 1971 Jun;47(6):841–843. doi: 10.1104/pp.47.6.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Huppe H. C., de Lamotte-Guéry F., Jacquot J-P, Buchanan B. B. The ferredoxin-thioredoxin system of a green alga, Chlamydomonas reinhardtii: identification and characterization of thioredoxins and ferredoxin-thioredoxin reductase components. Planta. 1990;180:341–351. [PubMed] [Google Scholar]
  9. Husic D. W., Tolbert N. E. Anaerobic Formation of d-Lactate and Partial Purification and Characterization of a Pyruvate Reductase from Chlamydomonas reinhardtii. Plant Physiol. 1985 Jun;78(2):277–284. doi: 10.1104/pp.78.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kobr M. J., Beevers H. Gluconeogenesis in the castor bean endosperm: I. Changes in glycolytic intermediates. Plant Physiol. 1971 Jan;47(1):48–52. doi: 10.1104/pp.47.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kruger N. J., Beevers H. Synthesis and degradation of fructose 2,6-bisphosphate in endosperm of castor bean seedlings. Plant Physiol. 1985 Feb;77(2):358–364. doi: 10.1104/pp.77.2.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lin M., Turpin D. H., Plaxton W. C. Pyruvate kinase isozymes from the green alga, Selenastrum minutum. II. Kinetic and regulatory properties. Arch Biochem Biophys. 1989 Feb 15;269(1):228–238. doi: 10.1016/0003-9861(89)90104-5. [DOI] [PubMed] [Google Scholar]
  13. Mendelssohn I. A., McKee K. L., Patrick W. H., Jr Oxygen Deficiency in Spartina alterniflora Roots: Metabolic Adaptation to Anoxia. Science. 1981 Oct 23;214(4519):439–441. doi: 10.1126/science.214.4519.439. [DOI] [PubMed] [Google Scholar]
  14. Menegus F., Cattaruzza L., Chersi A., Fronza G. Differences in the Anaerobic Lactate-Succinate Production and in the Changes of Cell Sap pH for Plants with High and Low Resistance to Anoxia. Plant Physiol. 1989 May;90(1):29–32. doi: 10.1104/pp.90.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Smith R. G., Vanlerberghe G. C., Stitt M., Turpin D. H. Short-Term Metabolite Changes during Transient Ammonium Assimilation by the N-Limited Green Alga Selenastrum minutum. Plant Physiol. 1989 Oct;91(2):749–755. doi: 10.1104/pp.91.2.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Stitt M. Fructose 2,6-bisphosphate and plant carbohydrate metabolism. Plant Physiol. 1987 Jun;84(2):201–204. doi: 10.1104/pp.84.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Stitt M. Product inhibition of potato tuber pyrophosphate:fructose-6-phosphate phosphotransferase by phosphate and pyrophosphate. Plant Physiol. 1989 Feb;89(2):628–633. doi: 10.1104/pp.89.2.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Streeter J. G., Thompson J. F. Anaerobic Accumulation of gamma-Aminobutyric Acid and Alanine in Radish Leaves (Raphanus sativus, L.). Plant Physiol. 1972 Apr;49(4):572–578. doi: 10.1104/pp.49.4.572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Turpin D. H., Botha F. C., Smith R. G., Feil R., Horsey A. K., Vanlerberghe G. C. Regulation of Carbon Partitioning to Respiration during Dark Ammonium Assimilation by the Green Alga Selenastrum minutum. Plant Physiol. 1990 May;93(1):166–175. doi: 10.1104/pp.93.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Vanlerberghe G. C., Horsey A. K., Weger H. G., Turpin D. H. Anaerobic Carbon Metabolism by the Tricarboxylic Acid Cycle : Evidence for Partial Oxidative and Reductive Pathways during Dark Ammonium Assimilation. Plant Physiol. 1989 Dec;91(4):1551–1557. doi: 10.1104/pp.91.4.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Vanlerberghe G. C., Schuller K. A., Smith R. G., Feil R., Plaxton W. C., Turpin D. H. Relationship between NH(4) Assimilation Rate and in Vivo Phosphoenolpyruvate Carboxylase Activity : Regulation of Anaplerotic Carbon Flow in the Green Alga Selenastrum minutum. Plant Physiol. 1990 Sep;94(1):284–290. doi: 10.1104/pp.94.1.284. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES