Skip to main content
SpringerLink
Log in

Permeability of ammonia, methylamine and ethylamine in the cyanobacterium,Synechococcus R-2 (Anacystis nidulans) PCC 7942

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Permeabilities of ammonia (NH3), methylamine (CH3NH2) and ethylamine (CH3CH2NH2) in the cyanobacterium (cyanophyte)Synechococcus R-2 (Anacystis nidulans) have been measured. Based on net uptake rates of DCMU (dichlorophenyldimethylurea) treated cells, the permeability of ammonia was 6.44±1.22 μm sec−1 (n=13). The permeabilities of methylamine and ethylamine, based on steady-state14C labeling were more than ten times that of ammonia (P methylamine=84.6±9.47 μm sec−1 (76),P ethylamine=109±11 μm sec−1 (55)). The apparent permeabilities based on net uptake rates of methylamine and ethylamine uptake were significantly lower, but this effect was partially reversible by ammonia, suggesting that net amine fluxes are rate limited by proton fluxes to an upper limit of about 700 nmol m−2 sec−1. Increasing concentrations of amines in alkaline conditions partially dissipated the pH gradient across the cell membrane, and this property could be used to calculate the relative permeabilities of different amines. The ratio of ethylamine to methylamine permeabilities was not significantly different from that calculated from the direct measurements of permeabilities; ammonia was much less effective in dissipating the pH gradient across the cell membrane than methylamine or ethylamine. An apparent permeability of ammonia of 5.7±0.9 μm sec−1 could be calculated from the permeability ratio of ammonia to methylamine and the experimentally measured permeability of methylamine. The permeability properties of ammonia and methylamine are very different; this poses problems in the interpretation of experiments where14C-methylamine is used as an ammonia analogue.

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

  • Allen, M.M. 1968. Simple conditions for growth of unicellular blue-green algae.J. Phycol. 4:1–3

    Google Scholar 

  • Atkins, G.L. 1969. Multicompartment Models in Biological Systems. Methuen, London

    Google Scholar 

  • Barr, C.E., Koh, M.S., Ryan, T.E. 1974. NH3 efflux as a means for measuring H+ extrusion inNitella.In: Membrane Transport in Plants. U. Zimmermann and J. Dainty, editors. pp. 180–185. Springer-Verlag, New York-Heidlberg-Berlin

    Google Scholar 

  • Beilby, M.J., Smith, F.A., Walker, N.A. 1980. The processes transporting CH3NH2 and CH3NH 3+ across theChara plasmalemma.In: Plant Membrane Transport: Current Conceptual Issues. R.M. Spanswick, W.J. Lucas, and J. Dainty, editors. pp. 601–602. Elsevier/North Holland Biomedical, Amsterdam

    Google Scholar 

  • Boussiba, S., Dilling, W., Gibson, J. 1984a. Methylammonium transport inAnacystis nidulans R-2.J. Bacteriol. 160:204–210

    Google Scholar 

  • Boussiba, S., Gibson, J. 1985. The role of glutamine synthetase activity in ammonium and methylammonium transport inAnacystis nidulans.FEBS Lett. 180:13–16

    Google Scholar 

  • Boussiba, S., Resch, C.M., Gibson, J. 1984b. Ammonia uptake and retention in some cyanobacteria.Arch. Microbiol. 138:287–292

    Google Scholar 

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

    Google Scholar 

  • Butler, T.C., Waddell, W.J., Poole, D.T. 1967. Intracellular pH based on the distribution of weak electrolytes.Fed. Proc. 26:1327–1332

    Google Scholar 

  • Collander, R. 1954. The permeability ofNitella cells to nonelectrolytes.Physiol. Plant. 7:420–445

    Google Scholar 

  • Crofts, A.R. 1966a. Uptake of ammonium ion by chloroplasts, and the mechanism of amine uncoupling.Biochem. Biophys. Res. Commun. 24:127–134

    Google Scholar 

  • Crofts, A.R. 1966b. Uptake of ammonium by chloroplasts and its relation to photophosphorylation.Biochem. Biophys. Res. Commun. 24:725–731

    Google Scholar 

  • Crofts, A.R. 1967. Amine uncoupling of energy transfer in chloroplasts.J. Biol. Chem. 242:3352–3359

    Google Scholar 

  • Gaensslen, R.E., McCarty, R.E. 1971. Amine uptake in chloroplasts.Arch. Biochem. Biophys. 147:55–65

    Google Scholar 

  • Gibson, J. 1981. Movement of acetate across the cytoplasmic membrane of the unicellular cyanobacteriaSynechococcus andAphanocapsa.Arch. Microbiol. 130:175–179

    Google Scholar 

  • Gibson, J. 1984. Nutrient transport by anoxygenic and oxygenic photosynthetic bacteria.Annu. Rev. Microbiol. 38:135–59

    Google Scholar 

  • Gordon, J.K., Moore, R.A. 1981. Ammonium and methylammonium transport by the nitrogen-fixing bacteriumAzotobacter vinelandii.J. Bacteriol. 148:435–442

    Google Scholar 

  • Hackette, S.L., Skye, G.E., Burton, C.U., Segel, H.I. 1970. Characterisation of an ammonium transport system in filamentous fungi with methylammonium-14C as substrate.J. Biol. Chem. 245:4241–4250

    Google Scholar 

  • Heldt, H.W., Werdan, K., Milovancev, M., Geller, G. 1973. Alkalization of the chloroplast stroma caused by light dependent proton flux into the thylacoid space.Biochim. Biophys. Acta 314:224–241

    Google Scholar 

  • Hind, G., Whittingham, C.P. 1963. Reduction of ferricyanide by choloroplasts in the presence of nitrogenous bases.Biochim. Biophys. Acta 75:194–202

    Google Scholar 

  • Hope, A.B., Walker, N.A. 1975. The Physiology of Giant Algal Cells. Cambridge University Press, Cambridge

    Google Scholar 

  • Howitz, K.T., McCarty, R.E. 1985. Kinetic characteristics of the chloroplast envelope glycolate transporter.Biochemistry 24:2645–2652

    Google Scholar 

  • Ihlenfeldt, M.J.A., Gibson, J. 1975. CO2 fixation and its regulation inAnacystis nidulans (Synechococcus).Arch Microbiol. 102:13–21

    Google Scholar 

  • Kallas, T., Dahlquist, F.W. 1981. Phosphorous-31 nuclear magnetic resonance analysis of internal pH during photosynthesis in the cyanobacteriumSynechococcus.Biochemistry 20:5900–5907

    Google Scholar 

  • Kleiner, D. 1981. The transport of NH3 and NH 4+ across biological membranes.Biochim. Biophys. Acta 639:41–52

    Google Scholar 

  • Kleiner, D. 1985a. Energy expenditure for cyclic retention of NH3/NH 4+ during N2 fixation byKlebsiella pneumoniae.FEBS Lett. 187:237–239

    Google Scholar 

  • Kleiner, D. 1985b. Bacterial ammonium transport.FEMS Microbiol. Rev. 32:87–100

    Google Scholar 

  • Krulwich, T.A. 1986. Bioenergetics of alkalophilic bacteria.J. Membrane Biol. 89:113–125

    Google Scholar 

  • Masamoto, K., Nishimura, M. 1978. Estimation of the internal pH in cells of blue-green algae in dark and under illumination.J. Biochem. 82:483–487

    Google Scholar 

  • McCarty, R.E., Coleman, C.H. 1970. Effect of hydrocarbon chain length on the uncoupling of photophosphorylation by amines.Arch. Biochem. Biophys. 141:198–206

    Google Scholar 

  • Meister, A. 1974. Glutamine synthetase of mammals.In: The Enzymes. Vol. 10 (3rd Ed.) pp. 699–754. P.D. Boyer, editor. Academic, New York-London

    Google Scholar 

  • Mewes, H.-H.W., Rafael, J. 1981. The 2-(dimethylaminostyryl)-1-methylpyridinium cation as indicator of the mitochondrial membrane potential.FEBS Lett. 131:7–10

    Google Scholar 

  • Miller, A.G., Turpin, D.H., Canvin, D.T. 1984. Na+ requirement for growth, photosynthesis, and pH regulation in the alkalotolerant cyanobacteriumSynechococcus leopoliensis.J. Bacteriol. 159:100–106

    Google Scholar 

  • Mitchell, P. 1966. Chemiosmotic Coupling in Oxidative and Photosynthetic Phosphorylation. Glynn Research Laboratories, Bodmin, Cornwall, England

    Google Scholar 

  • Mitchell, P., Moyle, J. 1969. Estimation of membrane potential and pH difference across the cristae of rat liver mitochondria.Eur. J. Biochem. 7:471–484

    Google Scholar 

  • Nicholls, D.G. 1982. Bioenergetics: An Introduction to the Chemiosmotic Theory. Academic, London

    Google Scholar 

  • Nobel, P.S. 1983. Introduction to Biophysical Plant Physiology, Freeman, San Francisco

    Google Scholar 

  • O'Hara, G.W., Riley, I.T., Glenn, A.R., Dilworth, M.J. 1985. The ammonium permease ofRhizobium leguminosarum MNF 3841.J. Gen. Microbiol. 131:757–764

    Google Scholar 

  • Padan, E., Zilberstein, D., Rottenberg, H. 1976. The proton electrochemical gradient inEscherichia coli cells.Eur. J. Biochem. 63:533–541

    Google Scholar 

  • Raven, J.A., Farquhar, G.D. 1981. Methylammonium transport inPhaseolus vulgaris leaf slices.Plant Physiol. 67:859–863

    Google Scholar 

  • Reed, R.H., Rowell, P., Stewart, W.D.P. 1980. Components of the proton electrochemical potential gradient inAnabaena varibilis.Biochem. Soc. Trans. 8:707–708

    Google Scholar 

  • Reed, R.H., Rowell, P., Stewart, W.D.P. 1981a. Uptake of potassium and rubidium ions by the cyanobacteriumAnabaena variabilis.FEMS Microbiol. Lett. 11:233–236

    Google Scholar 

  • Reed, R.H., Rowell, P., Stewart, W.D.P. 1981b. Characterisation of the transport of potassium ions in the cyanobacteriumAnabaena variabilis Kutz.Eur. J. Biochem. 116:323–330

    Google Scholar 

  • Reid, R.J., Walker, N.A. 1983. Adenylate concentrations inChara: Variability, effects of inhibitors and the relationship to protoplasmic streaming.Aust. J. Plant Physiol. 10:373–383

    Google Scholar 

  • Ritchie, R.J. 1985. Energetic considerations of ion transport inEnteromorpha intestinalis (L.) Link.New Phytol. 100:5–24

    Google Scholar 

  • Ritchie, R.J. 1987. The permeability of ammonia, methylamine and ethylamine in the charophyte,Chara corallina (C. australis).J. Exp. Bot. (in press)

  • Segel, I.H. 1976. Biochemical Calculations. John Wiley & Sons, New York

    Google Scholar 

  • Slayman, C.L. 1970. Movement of ions and electrogenesis in microrganisms.Am. Zool. 10:377–392

    Google Scholar 

  • Smith, F.A., Raven, J.A. 1976. H+ transport and regulation of cell pH.In: Encyclopedia of Plant Physiology. (New Series) Vol. 2, part A: Cells, pp. 317–346. U. Luttge and M.G. Pitman, editors. Springer-Verlag, Berlin

    Google Scholar 

  • Smith, F.A., Walker, N.A. 1978. Entry of methylammonium ions intoChara internodal cells.J. Exp. Bot. 29:107–120

    Google Scholar 

  • Solorzano, L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method.Limnol. Oceanogr. 14:799–801

    Google Scholar 

  • Spanswick, R.M. 1981. Electrogenic ion pumps.Annu. Rev. Plant Physiol. 32:267–289

    Google Scholar 

  • Walker, N.A., Pitman, M.G. 1976. Measurements of fluxes across membranes.In: Encyclopedia of Plant Physiology. (New Series) Vol. 2, Part A: Cells. pp. 93–126. (U. Luttge and M.G. Pitman, editors) Springer-Verlag, Berlin

    Google Scholar 

  • Walker, N.A., Smith, F.A., Beilby, M.J. 1979. Amine uniport at the plasmalemma of charophyte cells. II. Ratio of matter to charge transported and permeability of free base.J. Membrane Biol. 49:283–296

    Google Scholar 

  • Walter, A., Gutknecht, J. 1986. Permeability of small nonelectrolytes through lipid bilayer membranes.J. Membrane Biol. 90:207–217

    Google Scholar 

  • West, I.A. 1980. Energy coupling in secondary active transport.Biochim. Biophys. Acta 604:91–126

    Google Scholar 

  • Zar, J.H. 1974. Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, N.J.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Biochemistry, Molecular and Cell Biology, Division of Biological Sciences, Cornell University, 14853, Ithaca, New York

    Raymond J. Ritchie & Jane Gibson

Authors
  1. Raymond J. Ritchie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jane Gibson
    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

Ritchie, R.J., Gibson, J. Permeability of ammonia, methylamine and ethylamine in the cyanobacterium,Synechococcus R-2 (Anacystis nidulans) PCC 7942. J. Membrain Biol. 95, 131–142 (1987). https://doi.org/10.1007/BF01869158

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869158

Key Words

Search

Navigation