Skip to main content
SpringerLink
Log in

A glycine betaine transport system in Aphanothece halophytica and other glycine betaine-synthesising cyanobacteria

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Uptake of exogenous 14C-glycine betaine has been followed in the cyanobacterium Aphanothece halophytica and other species able to synthesise glycine betaine in response to osmotic stress. At 1 mmol dm−3 uptake was rapid (flux rate=29.50 nmol m−2 s−1), equilibrating at an internal concentration of 120 mmol dm−3 within 30 min. This rapid uptake, coupled with high internal accumulation, was characteristic of glycine betaine-synthesising cyanobacteria only. The 14C-glycine betaine transported was not catabolised. Kinetic studies indicated a Michaelis-Menten type relationship (K m=2.0 μmol dm−3, V max=45 nmol min−1 mm−3 cell volume), with a pH optimum of 8.0–8.5. Darkness dramatically decreased the flux rate. Higher 14C-glycine betaine levels occurred in cells growth in medium of elevated osmotic strength, and glycine betaine uptake was sensitive to changes in external salinity. A relationship between Na+ availability and glycine betaine uptake was observed, with >80 mmol dm−3 Na+ required for optimal stimulation of uptake in seawater-grown cells. Severe hyperosmotic stress (1000 mmol dm−3 NaCl) reduced the rate of glycine betaine uptake but increased internal glycine betaine concentration at equilibrium. Hypo-osmotic stress caused a decline in the internal glycine betaine concentration due to an increased rate of loss, indicating that the efflux system was also sensitive to ambient salinity changes. It is envisaged that this active transport system may be an adaptive mechanism in halophilic glycine betaine-synthesising cyanobacteria.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aitken DM, Brown AD (1972) Properties of halophil nicotinamideadenine dinucleotide phosphate-specific isocitrate dehydrogenase. Biochem J 130:645–662

    PubMed  Google Scholar 

  • Batterton JG, Van Baalen C (1971) Growth responses of cyanobacteria to sodium chloride concentrations. Arch Mikrobiol 76:151–165

    PubMed  Google Scholar 

  • Baumann P, Baumann L (1981) The marine Gram negative eubacteria. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer, Berlin Heidelberg, New York, pp 1302–1331

    Google Scholar 

  • Bernard T, Pocard JA, Perround B, Le Rudulier D (1986) Variations in the response of salt stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364

    Google Scholar 

  • Blunden G, El-Barouni MM, Gordon SM, Maclean WFH, Rogers DJ (1981) Extraction, purification and characterisation of Dragendorff-positive compounds from some British marine algae. Bot Marina 24:451–456

    Google Scholar 

  • Borowitzka LJ (1980) Solute accumulation and regulation of cell water activity. In: Paleg LB, Aspinall D (eds) The physiology and biochemistry of drought resistance in plants. Academic Press, Syndney Australia, pp 97–130

    Google Scholar 

  • Bouillard L, Le Rudulier D (1983) Nitrogen fixation under osmotic stress: enhancement of nitrogenase biosynthesis in Klebsiella pneumoniae by glycine betaine. Physiol Veg 21:447–457

    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  Google Scholar 

  • Cairney JC, Booth IR, Higgins CF (1985a) Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1218–1223

    PubMed  Google Scholar 

  • Cairney JC, Booth IR, Higgins CF (1985b) Osmoregulation of gene expression in Salmonella typhimurium: pro U encodes an osmotically-induced betaine transport system. J Bacteriol 164:1224–1232

    PubMed  Google Scholar 

  • Chudek JA, Foster R, Moore DJ, Reed RH (1987) Identification and quantification of methylated osmolytes in algae using proton nuclear magnetic resonance spectroscopy. Brit Phycol J 22 (in press)

  • Galinski E, Trüper HG (1982) Betaine, a compatible solute in the extremely halophilic phototrophic bacterium Ectothiorhodospira halochloris FEMS Microbiol Lett 13:357–360

    Article  Google Scholar 

  • Garlick S, Oren A, Padan E (1971) Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. J Bacteriol 129:623–629

    Google Scholar 

  • Hellebust JA (1976) Effect of salinity on photosynthesis and mannitol synthesis in the green flagellate Platymonas suecica. Can J Bot 54:1735–1741

    Google Scholar 

  • Ikuta S, Matuura K, Imamura S, Misaki H, Hariuti Y (1977) Oxidative pathway of choline to betaine in the soluble fraction prepared from Arthrobacter globiformis. J Biochem 82:157–163

    PubMed  Google Scholar 

  • Imhoff JF, Rodriguez-Valera F (1984) Betaine is the main compatible solute of halophilic eubacteria. J Bacteriol 160:478–479

    PubMed  Google Scholar 

  • Kratz WA, Myers J (1955) Nutrition and growth of several blue green algae. Am J Bot 42:282–287

    Google Scholar 

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

    PubMed  Google Scholar 

  • Lanyi JK (1979) The role of Na+ in transport processes of bacterial membranes. Biochim Biophys Acta 559:377–379

    PubMed  Google Scholar 

  • Le Rudulier D, Bernard T, Goas G, Hamelin J (1984) Osmoregulation in Klebsiella pneumoniae: enhancement of anaerobic growth and nitrogen fixation under stress by proline betaine, butyrobetaine, and other related compounds. Can J Microbiol 30:299–305

    PubMed  Google Scholar 

  • Le Rudulier D, Bernard T, Pocard JA, Goas G (1983) Accroissement de l'osmotolérance chez Rhizobium meliloti par la glycine bétaine et la proline bétaine. CR Acad Sci Paris 297:155–160

    Google Scholar 

  • Le Rudulier D, Bouillard L (1983) Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae. Appl Env Microbiol 46:152–159

    Google Scholar 

  • Le Rudulier D, Valentine RC (1982) Genetic engineering in agriculture: osmoregulation. Trends Biochem Sci 7:431–433

    Google Scholar 

  • Macleod RA (1968) On the role of inorganic ions in the physiology of marine bacteria. Adv Microbiol Sea 1:95–126

    Google Scholar 

  • Macleod RA (1980) Observations on the role of inorganic ions in the physiology of marine bacteria. In: Morishita H, Masui M (eds) Saline environment. Organising Committee of the Japanese Conference on Halophilic Microbiology, Osaka, pp 5–29

  • Macleod RA (1985) Marine microbiology far from the sea. Ann Rev Microbiol 39:1–20

    Google Scholar 

  • Measures JC (1975) Role of amino acids in osmoregulation of nonhalophilic bacteria. Nature 257:398–400

    PubMed  Google Scholar 

  • Miller DM, Jones JH, Yopp JH, Tindall DH, Schmid WT (1976) Ion metabolism in a halophilic blue green alga Aphanothece halophytica. Arch Microbiol 111:145–149

    PubMed  Google Scholar 

  • Mohammad FAA, Reed RH, Stewart WDP (1983) The halophilic cyanobacterium Synechocystis DUN 52 and its osmotic responses. FEMS Microbiol Lett 16:287–290

    Google Scholar 

  • Moore DJ, Reed RH, Stewart WDP (1985) Responses of cyanobacteria to low level osmotic stress: implications for the use of buffers. J Gen Microbiol 131:1267–1272

    Google Scholar 

  • Perroud B, Le Rudulier D (1985) Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol 161:393–401

    PubMed  Google Scholar 

  • Reed RH, Chudek JA, Foster R, Stewart WDP (1984b) Osmotic adjustment in cyanobacteria from hypersaline environments. Arch Microbiol 198:333–337

    Google Scholar 

  • Reed RH, Collins JC, Russell G (1980) The effects of salinity upon cellular volume of the marine red alga Porphyra purpurea (Roth) C. Ag. J Exp Bot 31:1521–1537

    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

    Google Scholar 

  • Reed RH, Richardson DL, Warr SRC, Stewart WDP (1984a) Carbohydrate accumulation and osmotic stress in cyanobacteria. J Gen Microbiol 130:1–4

    Google Scholar 

  • Reed RH, Warr SRC, Kerby NW, Stewart WDP (1986) Osmotic shock-induced release of low molecular weight metabolities from free-living and immobilised cyanobacteria. Enzyme Microb Technol 8:101–104

    Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Roth WG, Lecki MP, Dietzler DN (1985) Osmotic stress drastically inhibits active transport of carbohydrates by Escherichia coli. Biochem Biophys Res Comm 126:434–441

    PubMed  Google Scholar 

  • Sauvage D, Hamelin J, Larher F (1983) Glycine betaine and other structurally-related compounds improve the salt tolerance of Rhizobium meliloti. Plant Sci Lett 31:291–302

    Google Scholar 

  • Schobert B (1980) Proline catabolism, relaxation of osmotic strain and membrane permeability in the diatom Phaeodactylum tricormutum. Physiol Plant 50:37–40

    Google Scholar 

  • Stewart LMD, Booth IR (1983) Na+ involvement in proline transport in Escherichia coli. FEMS Microbiol Lett 19:161–164

    Google Scholar 

  • Stewart WDP (1983) Natural environments—challenges to microbial success and survival. Symp Soc Gen Microbiol 34:1–35

    Google Scholar 

  • Storey R, Wyn-Jones RG (1975) Betaine and choline levels in plants and their relationship to NaCl stress. Plant Sci Lett 4:161–168

    Google Scholar 

  • Tel-Or E, Harel MH (1981) Adaptation to salt of the photosynthetic apparatus in cyanobacteria. In: Akoyunoglou G (ed) Photosynthesis and productivity, photosynthesis and environment: Photosynthesis VI. Balaban International Science Series, Philadelphia, pp 455–462

  • Walsby AE, Van Rijn J, Cohen Y (1983) The biology of a new gasvacuolate cyanobacterium Dactylococcopsis salina sp. nov. in Solar Lake. Proc R Soc Lond B 217:417–447

    Google Scholar 

  • Wong PTS, Thompson J, Macleod RA (1969) Nutrition and metabolism of marine bacteria. XVII. Ion dependent retention of amino isobutyric acid and its relation to Na+-dependent transport in a marine pseudomonad. J Biol Chem 244:1016–1025

    PubMed  Google Scholar 

  • Wyn-Jones RG, Storey R, Leight RA, Ahmad N, Pollard A (1977) A hypothesis or cytoplasmic osmoregulation. In: Marré E, Ciferri O (eds) Regulation of cell membrane activities in plants. Elsevier, Amsterdam, pp 121–135

    Google Scholar 

  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems Science 217:1214–1222

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. D. J. Moore

    Present address: Department of Microbiology, University of Edinburgh, West Mains Road, EH9 3JG, Edinburgh, UK

Authors and Affiliations

  1. Department of Biological Sciences, University of Dundee, DD1 4HN, Dundee, UK

    D. J. Moore, R. H. Reed & W. D. P. Stewart

Authors
  1. D. J. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. H. Reed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. D. P. Stewart
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moore, D.J., Reed, R.H. & Stewart, W.D.P. A glycine betaine transport system in Aphanothece halophytica and other glycine betaine-synthesising cyanobacteria. Arch. Microbiol. 147, 399–405 (1987). https://doi.org/10.1007/BF00406140

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00406140

Key words

Search

Navigation