Planta

, Volume 201, Issue 2, pp 173–178 | Cite as

Characterization of mannitol metabolism in the mangrove red algaCaloglossa leprieurii (Montagne) J.Agardh

  • Ulf Karsten
  • Kevin D. Barrow
  • Oliver Nixdorf
  • John A. West
  • Robert J. King
Article

Abstract

A metabolic pathway, known as the mannitol cycle in fungi, has been identified as a new entity in the eulittoral mangrove red algaCaloglossa leprieurii (Montagne) J. Agardh. Three specific enzymes, mannitol-1-phosphate dehydrogenase (Mt1PDH; EC 1.1.1.17), mannitol-1-phosphatase (MtlPase; EC 3.1.3.22), mannitol dehydrogenase (MtDH; EC 1.1.1.67) and one nonspecific hexokinase (HK; EC 2.7.1.1) were determined and biochemically characterized in cell-free extracts. Mannitol-1-phosphate dehydrogenase showed activity maxima at pH 7.0 [fructose-6-phosphate (F6P) reduction] and pH 8.5 [oxidation of mannitol-1-phosphate (Mt1P)], and a very high specificity for both carbohydrate substrates. TheKm values were 1.4 mM for F6P, 0.09 mM for MOP, 0.020 mM for NADH and 0.023 mM for NAD+. For the dephosphorylation of MOP, MtlPase exhibited a pH optimum at 7.2, aKm value of 1.2 mM and a high requirement of Mg2+ for activation. Mannitol dehydrogenase had activity maxima at pH 7.0 (fructose reduction) and pH 9.8 (mannitol oxidation), and was less substrate-specific than Mt1PDH and MtlPase, i.e. it also catalyzed reactions in the oxidative direction with arabitol (64.9%), sorbitol (31%) and xylitol (24.8%). This enzyme showedKm values of 39 mM for fructose, 7.9 mM for mannitol, 0.14 mM for NADH and 0.075 mM for NAD+. For the non-specific HK, only theKm values for fructose (0.19 mM) and glucose (7.5 mM) were determined. The activities of the anabolic enzymes Mt1PDH and MtlPase were always at least two orders of magnitude higher than those of the degradative enzymes, indicating a net carbon flow towards a high intracellular mannitol pool. The function of mannitol metabolism inC. leprieurii as a biochemical adaptation to the environmental extremes in the mangrove habitat is discussed.

Key words

Caloglossa Hexokinase Mannitol-1-phosphate dehydrogenase Mannitol-1-phosphatase Mannitol dehydrogenase Osmolyte metabolism 

Abbreviations

F6P

fructose-6-phosphate

HK

hexokinase

Mt1P

mannitol-1-phosphate

Mt1PDH

mannitol-1-phosphate dehydrogenase

Mt1Pase

mannitol-1-phosphatase

MtDH

mannitol dehydrogenase

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. In: Neufeld EF, Gipsburg V (eds) Methods in enzymology. Academic Press, New York, pp 115–118Google Scholar
  2. Bisson MA, Kirst GO (1995) Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 82: 461–471Google Scholar
  3. Dills SS, Appweson A, Schmidt MR, Saier MH (1980) Carbohydrate transport in bacteria. Microbiol Rev 44: 385–418Google Scholar
  4. Horikoshi K, Iida S, Ikeda Y (1965) Mannitol and mannitol dehydrogenase in conidia ofAspergillus oryzae. J Bacteriol 89: 326–330Google Scholar
  5. Hult K, Gatenbeck S (1979) Enzyme activities of the mannitol cycle and some connected pathways inAlternaria alternata, with comments on the regulation of the cycle. Acta Chem Scand 33: 239–243Google Scholar
  6. Ikawa T, Watanabe T, Nisizawa K (1972) Enzymes involved in the last steps of the biosynthesis of mannitol in brown algae. Plant Cell Physiol 13: 1017–1029Google Scholar
  7. Jensen M, Feige GB, Waterkotte A (1991) Mannitol-1-phosphate dehydrogenase inPseudevernia furfuracea. Lichenologist 23: 187–196Google Scholar
  8. Karsten U, West JA (1993) Ecophysiological studies on six species of the mangrove red algal genusCaloglossa. Aust J Plant Physiol 20: 729–739Google Scholar
  9. Karsten U, West JA, Mostaert AS, King RJ, Barrow KD, Kirst GO (1992) Mannitol in the red algal genusCaloglossa (Harvey) J. Agardh. J Plant Physiol 140: 292–297Google Scholar
  10. Karsten U, Barrow KD, Nixdorf O, King RJ (1996) The compability of unusual organic osmolytes from mangrove red algae with enzyme activity. Aust J Plant Physiol 23: 577–582Google Scholar
  11. King RJ, Puttock CF (1995) Morphology and taxonomy ofCaloglossa (Delesseriaceae, Rhodophyta). Aust Syst Bot 7: 89–124Google Scholar
  12. Kirst GO (1980) Low mw carbohydrates and ions in Rhodophyceae: quantitative measurement of floridoside and digeneaside. Phytochemistry 19: 1107–1110Google Scholar
  13. Kiser RC, Niehaus WG (1981) Purification and kinetic characterization of mannitol-1-phosphate dehydrogenase fromAspergillus niger. Arch Biochem Biophys 211: 613–621Google Scholar
  14. Klungsoyr L (1966) Mannitol kinase in cell-free extracts ofEscherichia coli. Biochim Biophys Acta 122: 361–364Google Scholar
  15. Kremer BP (1978) Patterns of photoassimilatory products in Pacific Rhodophyceae. Can J Bot 56: 1655–1659Google Scholar
  16. Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiol Plant 70: 553–557Google Scholar
  17. Morton N, Dickerson AG, Hammond JBW (1985) Mannitol metabolism inAgaricus bisporus: purification and properties of mannitol dehydrogenase. J Gen Microbiol 131: 2885–2890Google Scholar
  18. Mostaert AS, Karsten U, King RJ (1995) Physiological responses ofCaloglossa leprieurii (Ceramiales, Rhodophyta) to salinity stress. Phycol Res 43: 215–222Google Scholar
  19. Mostaert AS, Orlovich DA, King RJ (1996) Ion compartmentation in the red algaCaloglossa leprieurii (Montagne) J. Agardh in response to salinity changes: freeze substitution and X-ray microanalysis. New Phytol 132: 513–519Google Scholar
  20. Niehaus WG, Dilts RP (1982) Purification and characterization of mannitol dehydrogenase fromAspergillus parasiticus. J Bacteriol 151: 243–250Google Scholar
  21. Noeldner PKM, Coleman MJ, Faulks R, Oliver RP (1994) Purification and characterization of mannitol dehydrogenase from the fungal tomato pathogenCladosporium fulvum (syn.Fulvia fulva). Physiol Mol Plant Pathol 45: 281–289Google Scholar
  22. Richter DFE, Kirst GO (1987) Mannitol dehydrogenase and mannitol-1-phosphate dehydrogenase inPlatymonas subcordiformis: some characteristics and their role in osmotic adaptation. Planta 170: 528–534Google Scholar
  23. Rumpho ME, Edwards GE, Loescher WH (1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves. Plant Physiol 73: 869–873Google Scholar
  24. Schmatz DM (1989) The mannitol cycle — a new metabolic pathway in the coccidia. Parasitol Today 5: 205–208Google Scholar
  25. Singh SP, Rogers PJ (1993) Isolation and characterization of mannitol-1-phosphate dehydrogenase fromBrochothrix thermosphacta. J Gen Appl Microbiol 39: 327–337Google Scholar
  26. Strandberg GM (1969) Mannitol metabolism inAspergillus candidus. J Bacteriol 97: 1305–1309Google Scholar
  27. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259: 508–510Google Scholar
  28. Teschner W, Serre MC, Garel JR (1990) Enzymatic properties, renaturation and metabolic role of mannitol-1-phosphate dehydrogenase fromEscherichia coli. Biochemie 72: 33–40Google Scholar
  29. Turner JF, Copeland L (1981) Hexokinase II of pea seeds. Plant Physiol 68: 1123–1127Google Scholar
  30. Wegmann K (1986) Osmoregulation in eucaryotic algae. FEMS Microbiol Rev 39: 129–135Google Scholar
  31. Wolff JB, Kaplan NO (1955) Mannitol-1-phosphate dehydrogenase fromEscherichia coli. J. Biol Chem 218: 849–869Google Scholar
  32. Yamada H, Okamoto K, Kodama K, Noguchi F, Tanaka S (1961) Enzymic studies on mannitol formation byPiricularia oryzae. J Biochem 49: 404–410Google Scholar

Copyright information

© Springer-Verlag 1997

Authors and Affiliations

  • Ulf Karsten
    • 1
  • Kevin D. Barrow
    • 2
  • Oliver Nixdorf
    • 3
  • John A. West
    • 4
  • Robert J. King
    • 1
  1. 1.School of Biological ScienceUniversity of New South WalesSydneyAustralia
  2. 2.School of Biochemistry and Molecular GeneticsUniversity of New South WalesSydneyAustralia
  3. 3.Department of Biology, Marine BotanyUniversity of BremenBremenGermany
  4. 4.School of BotanyUniversity of MelbourneParkvilleAustralia

Personalised recommendations