Skip to main content
Log in

Accumulation of glycinebetaine and its synthesis from radioactive precursors under salt-stress in the cyanobacterium Aphanothece halophytica

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Growth in salt-stressed (2.0 M NaCl) Aphanothece halophytica was initially delayed during the first two days of cultivation and eventually attained the same growth rate as the control (0.5 M NaCl) cells. Glycinebetaine accumulation increased slightly in control cells but a dramatic increase of glycinebetaine occurred in salt-stressed cells during a growth period of six days. There was no apparent increase in the synthesis of [14C] glycinebetaine in the control cells, in contrast to the marked increase in its synthesis in the salt-stressed cells. Increasing NaCl concentration in the growth medium induced both the accumulation and the synthesis of glycinebetaine. Time course experiments provided evidence that [14C] choline was first oxidized to [14C] betaine aldehyde which was further oxidized to [14C] glycinebetaine in A. halophytica. The supporting data for such a pathway were obtained from the presence of choline and betaine aldehyde dehydrogenase activities found in the membrane and cytoplasmic fractions, respectively. The activities of these two enzymes were also enhanced upon increasing NaCl concentration in the growth medium from 0.5 M to 2.0 M. Under this condition an increaseof approximately 1.5-fold was observed for choline dehydrogenase activity as compared to 2.5-fold for betaine aldehyde dehydrogenase activity, suggesting a preferable induction of the latter enzyme by salt stress. A. halophytica was able to utilize [14C] ethanolamine and [14C] glycine for the synthesis of [14C] glycinebetaine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ameyama M, Shinagawa E, Matsushita K, Takimoto K, Nakashima K, Adachi O (1985) Mammalian choline dehydrogenase is a quinoprotein. Agric. biol. Chem. 49: 3623–3626.

    CAS  Google Scholar 

  • Borowitzka MA, Borowitzka LJ, Kessly D (1990) Effects of salinity increase on carotenoid accumulation in the green alga Dunaliella salina. J. appl. Phycol. 2: 111–119.

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Brouquisse R, Weigel P, Rhodes D, Yocum CF, Hanson AD (1989) Evidence for a ferredoxin-dependent choline monooxygenase from spinach chloroplast stroma. Plant Physiol. 90: 322–329.

    PubMed  CAS  Google Scholar 

  • Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J. gen. Microbiol. 72: 589–591.

    PubMed  CAS  Google Scholar 

  • Castenholz RW (1988) Culturing methods for cyanobacteria. Meth. Enzymol. 167: 68–93.

    CAS  Google Scholar 

  • Choquet CG, Ahonkhai I, Klein M, Kushner DJ (1991) Formation and role of glycinebetaine in the moderate halophile Vibrio costicola. Arch. Microbiol. 155: 153–158.

    Article  CAS  Google Scholar 

  • Coughlan SJ, Wyn Jones RG (1982) Glycinebetaine biosynthesis and its control in detached secondary leaves of spinach. Planta 154: 6–17.

    Article  CAS  Google Scholar 

  • Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: Genetics and physiology. Annu. Rev. Microbiol. 45: 569–606.

    Article  PubMed  CAS  Google Scholar 

  • Fan LL, Masters BSS (1974) Properties of purified kidney microsomal NADPH-cytochrome c reductase. Arch. Biochem. Biophys. 165: 665–671.

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Hall JL, Ward ME (1978) Salt tolerance in the halophyte, Suaeda maritima (L.) Dum: properties of malic enzyme and PEP carboxylase. Ann. Bot. 42: 1065–1074.

    CAS  Google Scholar 

  • Hanson AD, Hitz WD (1982) Metabolic responses of mesophytes to plant water deficits. Annu. Rev. Plant Physiol. 33: 163–203.

    Article  CAS  Google Scholar 

  • Hanson AD, Nelson CE (1978) Betaine accumulation and [14C] formate metabolism in water-stressed barley leaves. Plant Physiol. 62: 305–312.

    PubMed  CAS  Google Scholar 

  • Hanson AD, Rhodes D (1983) 14C Tracer evidence for synthesis of choline and betaine via phosphoryl bases intermediates in salinized sugar beet leaves. Plant Physiol. 71: 692–700.

    PubMed  CAS  Google Scholar 

  • Hanson AD, Scott NA (1980) Betaine synthesis from radioactive precursors in attached, water-stressed barley leaves. Plant Physiol. 66: 342–348.

    PubMed  CAS  Google Scholar 

  • Hitz WD, Rhodes D, Hanson AD (1981) Radiotracer evidence implicating phosphoryl and phosphatidyl bases as intermediates in betaine synthesis by water-stressed barley leaves. Plant Physiol. 68: 814–822.

    PubMed  CAS  Google Scholar 

  • Incharoensakdi A, Kum-arb U (1998) Betaine aldehyde dehydrogenase from a halotolerant cyanobacterium Aphanothece halophytica: purification, properties and regulation by salinity. J. Sci. Soc. Thailand 24: 231–240.

    Article  CAS  Google Scholar 

  • Incharoensakdi A, Takabe T, Akazawa T (1986a) Effect of betaine on enzyme activity and subunit interaction of ribulose-1, 5-bisphosphate carboxylase/oxygenase from Aphanothece halophytica. Plant Physiol. 81: 1044–1049.

    PubMed  CAS  Google Scholar 

  • Incharoensakdi A, Takabe T, Akazawa T (1986b) Role of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in the activation process. Arch. Biochem. Biophys. 248: 62–70.

    Article  PubMed  CAS  Google Scholar 

  • Konishi K, Fujioka M (1987) Chemical modification of a functional arginine residue of rat liver glycine methyltransferase. Biochemistry 26: 8496–8502.

    Article  PubMed  CAS  Google Scholar 

  • Landfald B, Strom, AR (1986) Choline-glycinebetaine pathway confers a high level of osmotic tolerance in Escherichia coli. J. Bact. 165: 849–855.

    PubMed  CAS  Google Scholar 

  • Mackay MA, Norton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J. gen Microbiol. 130: 2177–2191.

    CAS  Google Scholar 

  • Manetas Y, Petropoulou Y, Karabourniotis G (1986) Compatible solutes and their effects on phosphoenolpyruvate carboxylase of C4-halophytes. Plant Cell Environ. 9: 145–151.

    Article  CAS  Google Scholar 

  • Montesinos ML, Herrero A, Flores E (1997) Amino acid transport in taxonomic diverse cyanobacteria and identification of two genes encoding elements of a neutral amino acid permease putatively involved in recapture of leaked hydrophobic amino acids. J. Bact. 179: 853–862.

    PubMed  CAS  Google Scholar 

  • Moore DJ, Reed RH, Stewart WDP (1987) A glycinebetaine transport system in Aphanothece halophytica and other glycinebetaine-synthesizing cyanobacteria. Arch. Microbiol. 147: 399–405.

    Article  CAS  Google Scholar 

  • Reed RH (1988) Osmotic adjustment: Organic solutes. Meth. Enzymol. 167: 528–534.

    Article  CAS  Google Scholar 

  • Reed RH, Chudek JA, Foster R, Stewart WDP (1984) Osmotic adjustment in cyanobacteria from hypersaline environments. Arch. Microbiol. 138: 333–337.

    Article  CAS  Google Scholar 

  • Reed RH, Richardson DL, Stewart WDP (1985) Na+ uptake and extrusion in the cyanobacterium Synechocystis PCC 6714 in response to hypersaline treatment. Evidence for transient changes in plasmalemma Na+ permeability. Biochim. biophys. Acta 814: 347–355.

    Article  CAS  Google Scholar 

  • Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 357–384.

    Article  CAS  Google Scholar 

  • Roberts MF, Lai M-C, Gunsalus RP (1992) Biosynthetic pathways of the osmolytes N-acetyl-?-lysine, ?-glutamine, and betaine in Methanohalophilus strain FDF1 suggested by nuclear magnetic resonance analyses. J. Bact. 174: 6688–6693.

    PubMed  CAS  Google Scholar 

  • Russell R, Scopes RK (1994) Use of hydrophobic chromatography for purification of membrane-located choline dehydrogenase from a Pseudomonas strain. Bioseparation 4: 279–284.

    PubMed  CAS  Google Scholar 

  • Smith LT, Pocard JA, Bernard T, Le Rudulier T (1988) Osmotic control of glycinebetaine biosynthesis and degradation in Rhizobium meliloti. J. Bact. 170: 3142–3149.

    PubMed  CAS  Google Scholar 

  • Storey R, Wyn Jone RG (1977) Quaternary ammonium compounds in plants in relation to salt stress. Phytochemistry 16: 447–453.

    Article  CAS  Google Scholar 

  • Takabe T, Incharoensakdi A, Arakawa K, Yokota S (1988) CO2 fixation rate and RuBisCO content increase in the halotolerant cyanobacterium, Aphanothece halophytica, grown in high salinities. Plant Physiol. 88: 1120–1124.

    Article  PubMed  CAS  Google Scholar 

  • Vonshak A, Kancharaksa N, Bunnag B, Tanticharoen M (1996) Role of light and photosynthesis on the acclimation process of the cyanobacterium Spirulina platensis to salinity stress. J. appl. Phycol. 8: 119–124.

    Article  Google Scholar 

  • Weretilnyk EA, Bednarek S, McCue KF, Rhodes D, Hanson AD (1989) Comparative biochemical and immnological studies of the glycinebetaine synthesis pathway in diverse families of dicotyledons. Planta 178: 342–352.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Incharoensakdi, A., Wutipraditkul, N. Accumulation of glycinebetaine and its synthesis from radioactive precursors under salt-stress in the cyanobacterium Aphanothece halophytica . Journal of Applied Phycology 11, 515–523 (1999). https://doi.org/10.1023/A:1008186309006

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008186309006

Navigation