Skip to main content
SpringerLink
Log in

Solute transport and energy transduction in bacteria

  • Research Articles
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

In bacteria two forms of metabolic energy are usually present, i.e. ATP and transmembrane ion-gradients, that can be used to drive the various endergonic reactions associated with cellular growth. ATP can be formed directly in substrate level phosphorylation reactions whereas primary transport processes can generate the ion-gradients across the cytoplasmic membrane. The two forms of metabolic energy can be interconverted by the action of ion-translocating ATPases. For fermentative organisms it has long been thought that ion-gradients could only be generated at the expense of ATP hydrolysis by the F0F1-ATPase. In the present article, an overview is given of the various secondary transport processes that form ion-gradients at the expense of precursor (substrate) and/or end-product concentration gradients. The metabolic energy formed by these chemiosmotic circuits contributes to the ‘energy status’ of the bacterial cell which is particularly important for anaerobic/fermentative organisms.

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

  • Ambudkar SV, Sonna LA & Maloney PC (1986) Variable stoichiometry of phosphate-linked anion exchange inStreptococcus lactis: implications for the mechanism of sugar phosphate transport by bacteria. Proc. Natl. Acad. Sci. USA 83: 280–284

    PubMed  Google Scholar 

  • Ambudkar SV & Rosen BP (1990) Ion-exchange systems in prokaryotes. In: Krulwich TA (Ed) The Bacteria, Vol XII (pp 247–271) Academic Press, New York

    Google Scholar 

  • Anantharam V, Allison MJ & Maloney PC (1989) Oxalate:formate exchange. The basis for energy coupling inOxalobacter. J. Biol. Chem. 264: 7244–7250

    PubMed  Google Scholar 

  • Beck BJ & Russell JB (1994) Electrogenic glutamine uptake byPeptostreptococcus anaerobicus and generation of a transmembrane potential. J. Bacteriol. 176: 1303–1308

    PubMed  Google Scholar 

  • Boenigk R, Dürre P & Gottschalk G (1989) Carrier-mediated acetate transport inAcetobacter woodii. Arch. Microbiol. 152: 589–593

    Google Scholar 

  • Bröer S & Krämer R (1990) Lysine uptake and exchange inCorynebacterium glutamicum. J. Bacteriol. 172: 7241–7248

    PubMed  Google Scholar 

  • Cunin R, Glansdorff N, Pierard A & Stalon V (1986) Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50: 314–352

    PubMed  Google Scholar 

  • Driessen AJM, Poolman B, Kiewiet R & Konings WN (1987) Arginine transport inStreptococcus lactis is catalyzed by a cationic exchanger. Proc. Natl. Acad. Sci. USA 84: 6093–6097

    Google Scholar 

  • Driessen AJM, Molenaar D & Konings WN (1989a) Kinetics and regulation of arginine:ornithine exchange in membrane vesicles ofLactococcus lactis. J. Biol. Chem. 264: 10361–10370

    PubMed  Google Scholar 

  • Driessen AJM, van Leeuwen R & Konings WN (1989b) Transport of basic amino acids by membrane vesicles ofLactococcus lactis. J. Bacteriol. 171: 1453–1458

    PubMed  Google Scholar 

  • Driessen AJM, Smid EJ & Konings WN (1988) Transport of diamines byEnterococcus faecalis is mediated by an agmatine-putrescine antiporter. J. Bacteriol. 170: 4522–4527

    PubMed  Google Scholar 

  • Eiglmeier K, Boos W & Cole ST (1987) Nucleotide sequence and transcriptional start point of theglpT gene ofEscherichia coli: extensive homology with components of the hexose-6-phosphate transport system. Mol. Microbiol. 1: 251–258

    PubMed  Google Scholar 

  • Elvin CM, Hardy CM & Rosenberg H (1985) P i exchange mediated by the GlpT-dependentsn-glycerol-3-phosphate transport system inEscherichia coli. J. Bacteriol. 161: 1054–1058

    Google Scholar 

  • Engel P, Krämer R & Unden G (1992) Anaerobic fumarate transport inEscherichia coli by anfnr-dependent dicarboxylate uptake system which is different from the aerobic dicarboxylate uptake system. J. Bacteriol. 174: 5533–5539

    PubMed  Google Scholar 

  • Foucaud C & Poolman B (1992) Lactose transport system ofStreptococcus thermophilus: functional reconstitution of the protein and characterization of the kinetic mechanism of transport. J. Biol. Chem. 267: 22087–22094

    PubMed  Google Scholar 

  • Gale EF (1946) The bacterial amino acid decarboxylases. Adv. Enzymol. 6: 1–32

    Google Scholar 

  • Heijthuijsen JHFG (1990) Growth and product formation in anaerobic methylotrophic non-methanogenic bacteria. Ph.D. thesis, University of Groningen

  • Heijthuijsen JHFG & Hansen TA (1989) Anaerobic degradation of betaine by marineDesulfovibrio strains. Arch. Microbiol. 152: 393–396

    Google Scholar 

  • Higuchi T, Hayashi H & Abe K (1993) ATP-generation coupled with amino acid decarboxylation by lactobacilli. FEMS Microbiol. Lett. 12: C39

  • Huber RE, Lytton J & Fung EB (1980) Efflux of β-galactosidase products fromEscherichia coli. J. Bacteriol. 141: 528–533

    PubMed  Google Scholar 

  • Ingvorsen K, Zehnder AJB & Jørgenson BB (1984) Kinetics of sulfate uptake and acetate uptake byDesulfobacter postgatei. Appl. Env. Microbiol. 47: 404–408

    Google Scholar 

  • Janssen PH & Harfoot CG (1990) Isolation of aCitrobacter sp. able to grow on malonate under strictly anaerobic conditions. J. Gen. Microbiol. 136: 1037–1042

    PubMed  Google Scholar 

  • Kashiwagi K, Miyamoto S, Suzuki F, Kobayashi H & Igarashi K (1992) Excretion of putrescine by the putrescine-ornithine antiporter encoded by thepotE gene ofEscherichia coli. Proc. Natl. Acad. Sci. USA 89: 4529–4533

    PubMed  Google Scholar 

  • Kelly DP (1988) Oxidation of sulphur compunds. In: Cole JA & Ferguson SJ (Eds) The nitrogen and sulphur cycle (pp 64–98) Soc. Gen. Microbiol., Cambridge Univ. Press, U.K.

    Google Scholar 

  • Kolb S, Otte H, Nagel B & Schink B (1992) Energy conservation in malolactic fermentation byLactobacillus planatarum andLactobacillus sake. Arch. Microbiol. 157: 457–463

    PubMed  Google Scholar 

  • Konings WN & Booth IR (1981) Do the stoichiometries of ion-linked transport systems vary? Trends Biochem. Sci. 6: 257–262

    Google Scholar 

  • Konings WN, Poolman B & Driessen AJM (1989) Bioenergetics and solute transport in lactococci. CRC Crit. Rev. Microbiol. 16: 419–476

    Google Scholar 

  • Konings WN & Rosenberg H (1978) Phosphate transport in membrane vesicles fromEscherichia coli. Biochim. Biophys. Acta 211: 158–168

    Google Scholar 

  • Kortstee GJJ, Appeldoorn KJ, Bonting CFC, Van Niel EWJ & Van Veen HW (1994) The biology of polyphosphate-accumulating bacteria involved in enhanced biological phophorus removal. FEMS Microbiol. Rev.: in press

  • Krämer R & Palmieri F (1992) Metabolite carriers in mitochondria. In: Ernster L (Ed) Molecular Mechanisms in Bioenergetics. Elsevier Science Publishers B.V., Amsterdam

    Google Scholar 

  • Kunkee R (1991) Some roles of malic acid in the malolactic fermentation in wine making. FEMS Microbiol. Rev. 88: 55–72

    Google Scholar 

  • Leblanc G, Rimon G & Kaback HR (1980) Glucose 6-phosphate transport in membrane vesicles isolated fromEscherichia coli: effect of imposed electrical potential and pH gradient. Biochem. 19: 2522–2528

    Google Scholar 

  • Maloney PC, Ambudkar SV, Anantharam V, Sonna LA & Varadhachary A (1990) Anion-exchange mechanisms in bacteria. Microb. Rev. 54: 1–17

    Google Scholar 

  • Maloney PC (1990) Microbes and membrane biology. FEMS Microbiol. Rev. 87: 91–102

    Google Scholar 

  • Maloney PC, Ambudkar SV, Thomas J & Schiller L (1984) Phosphate: hexose 6-phosphate antiport inStreptococcus lactis. J. Bacteriol. 158: 238–245

    PubMed  Google Scholar 

  • McInerney MJ & Beaty PS (1988) Anaerobic community structure from a nonequilibrium thermodynamic perspective. Can. J. Microbiol. 34: 487–493

    Google Scholar 

  • Meng S-Y & Bennett GN (1992) Nucleotide sequence of theEscherichia coli cad operon: a system for neutralization of low extracellular pH. J. Bacteriol. 174: 2659–2669

    PubMed  Google Scholar 

  • Michel TA & Macy JM (1990) Generation of a membrane potential by sodium-dependent succinate efflux inSelenomonas ruminantium. J. Bacteriol. 172: 1430–1435

    PubMed  Google Scholar 

  • Michels PAM, Michels JPJ, Boonstra J & Konings WN (1979) Generation of an electrochemical proton gradient in bacteria by the extrusion of metabolic end products. FEMS Microbiol. Lett. 5: 357–364

    Google Scholar 

  • Mitchell P (1968) Chemiosmotic coupling and energy transduction, Glynn Research Ltd., Bodmin, England

    Google Scholar 

  • Molenaar D, Bosscher JS, Ten Brink B, Driessen AJM & Konings WN (1993) Generation of a proton motive force by histidine decarboxlylation and electrogenic histidine/histamine antiport inLactobacillus buchneri. J. Bacteriol. 175: 2864–2870.

    PubMed  Google Scholar 

  • Poolman B & Konings WN (1993) Secondary solute transport in bacteria. Biochim. Biophys. Acta 1183: 5–39

    Google Scholar 

  • Poolman B, Molenaar D, Smid, EJ, Ubbink T, Abee T, Renault PP & Konings WN (1991) Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J. Bacteriol. 173: 6030–6037

    PubMed  Google Scholar 

  • Poolman B, Molenaar D & Konings WN (1994) Diversity of transport mechanisms in bacteria. In: Shinitzky M (Ed) Handbook of Biomembranes, Vol 2 (pp 329–379) Balaban Publishers, Rehovot, Israel

    Google Scholar 

  • Poolman B (1990) Precursor/product antiport in bacteria. Molec. Microbiol. 4: 1629–1636

    Google Scholar 

  • Poolman B, Driessen AJM & Konings WN (1987a) Regulation of arginine-ornithine exchange and the arginine deiminase pathway inStreptococcus lactis. J. Bacteriol. 169: 5597–5604

    Google Scholar 

  • Poolman B, Driessen AJM & Konings WN (1987b) Regulation of solute transport in streptococci by the external and internal pH values. Microbiol. Rev. 51: 498–508

    PubMed  Google Scholar 

  • Poolman B, Royer TJ, Mainzer SE & Schmidt BF (1989) Lactose transport system ofStreptococcus thermophilus: a hybrid protein with homology to the melibiose carrier and enzyme III of phosphoenol-pyruvate-dependent phosphotransferase systems. J. Bacteriol. 171: 244–253

    Google Scholar 

  • Otto R, Lageveen RG, Veldkamp H & Konings WN (1982) Lactate efflux induced electrical potential in membrane vesicles ofStreptococcus cremoris. J. Bacteriol. 146: 733–738

    Google Scholar 

  • Otto R, Sonnenberg ASM, Veldkamp H & Konings WN (1980) Generation of an electrochemical proton gradient inStreptococcus cremoris by lactate efflux. Proc. Natl. Acad. Sci., U.S.A. 77: 5502–5506

    Google Scholar 

  • Ramos A, Poolman B, Santos H, Lolkema JS & Konings WN (1994) Uniport of anionic citrate and proton consumption in citrate metabolism generate a proton motive force inLeuconostocoenos. J. Bacteriol. in press

  • Reichard P (1957) Ornithine carbamoyl transferase from rat liver. Acta Chem. Scand. 11: 523–536

    Google Scholar 

  • Reizer J & Saier MH (1987) Mechanism and regulation of phosphate transport inStreptococcus pyogenes. J. Bacteriol. 169: 297–301

    Google Scholar 

  • Rice SL & Koehler PE (1976) Tyrosine and histidine decarboxylase activities ofPediococcus cerevisiae andLactobacillus sp. and the production of tyramine in fermented sausages. J. Milk Food Technol. 39: 166–169

    Google Scholar 

  • Ruan Z-S, Anantharam V, Crawford IT, Ambudkar SV, Rhee SY, Allison MJ & Maloney PC (1992) Identification, purification, and reconstitution of OxlT, the oxalate: formate antiport protein ofOxalobacter formigenes. J. Biol. Chem. 267: 10537–10543

    PubMed  Google Scholar 

  • Salema M, Poolman B, Lolkema JS, Loureiro Dias MC & Konings WN (1994) Uniport of monoanionic L-malate in membrane vesicles fromLeuconostoc oenos. Eur. J. Biochem. submitted for publication

  • Schonheit P, Kristjansson JK & Thauer RK (1982) Kinetic mechanism for the ability of sulfate reducers to outcompete methanogens for acetate. Arch. Microbiol. 132: 285–288

    Google Scholar 

  • Simpson SJ, Bendall MR, Egan AF & Rogers PJ (1983a) High field phosphorous NMR studies of the stoichiometry of the lactate/proton carrier ofStreptococcus faecalis. Eur. J. Biochem. 136: 63–69

    PubMed  Google Scholar 

  • Simpson SJ, Vink R, Egan AF & Rogers PJ (1983b) Lactate efflux stimulate (32Pi)-ATP exchange inStreptococcus faecalis membrane vesicles. FEMS Microbiol. Lett. 5: 85–88

    Google Scholar 

  • Smith MR & Lequerica JL (1985)Methanosarcina mutant unable to produce methane or assimilate carbon from acetate. J. Bacteriol. 164: 618–625

    Google Scholar 

  • Smith DGE, Russell WC, Ingledew WJ & Thurkell T (1993) Hydrolysis of urea byUreaplasma urealyticum generates a transmembrane potential with resultant ATP synthesis. J. Bacteriol. 175: 3253–3258

    Google Scholar 

  • Sonna LA, Ambudkar SV & Maloney PC (1988) The mechanism of glucose 6-phosphate transport byEscherichia coli. J. Biol. Chem. 263: 6625–6630

    PubMed  Google Scholar 

  • Sonna LA & Maloney PC (1988) Identification and functional reconstitution of phosphate: sugar phosphate antiport ofStaphylococcus aureus. J. Membr. Biol. 101: 267–274

    PubMed  Google Scholar 

  • Ten Brink B, Damink C, Joosten HMLJ & Huis in 't Veld JHJ (1990) Occurrence and formation of biologically active amines in foods. Int. J. Food. Microbiol. 11: 73–84

    PubMed  Google Scholar 

  • Ten Brink B & Konings WN (1980) Generation of an electrochemical proton gradient by lactate efflux in membrane vesicles ofEscherichia coli. Eur. J. Biochem. 111: 59–66

    PubMed  Google Scholar 

  • Ten Brink B & Konings WN (1982) Electrochemical proton gradient and lactate concentration gradient inStreptococcus cremoris cells grown in batch culture. J. Bacteriol. 152: 682–686

    PubMed  Google Scholar 

  • Ten Brink B, Otto R, Hansen UP & Konings WN (1985) Energy recycling by lactate efflux in growing and nongrowing cells ofStreptococcus cremoris. J. Bacteriol. 162: 383–390

    PubMed  Google Scholar 

  • Thomas TD & Crow VL (1984) Selection of galactose-fermentingStreptococcus thermophilus in lactose-limited chemostat cultures. Appl. Env. Microbiol. 48: 186–191

    Google Scholar 

  • Thompson J (1987) Ornithine transport and exchange inStreptococcus lactis. J. Bacteriol. 169: 4147–4153

    PubMed  Google Scholar 

  • Van der Maarel MJEC, Quist P, Dijkhuizen L & Hansen TA (1993) Anaerobic degradation of dimethylsufoniopropionate by a marineDesulfovibrio strain. Arch. Microbiol. 160: 411–412

    Google Scholar 

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN & Zehnder AJB (1993a) Characterization of two phosphate transport systems inAcinetobacter johnsonii 210A. J. Bacteriol. 175: 200–206

    PubMed  Google Scholar 

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN & Zehnder AJB (1993b) Mechanism and energetics of the secondary phosphate transport system ofAcinetobacter johnsonii 210A. J. Biol. Chem. 268: 19377–19383

    PubMed  Google Scholar 

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN & Zehnder AJB (1994a) Substrate specificity of the two phosphate transport systems ofAcinetobacter johnsonii 210A in relation to phosphate speciation in its aquatic environment. J. Biol. Chem. in press

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN & Zehnder AJB (1994b) Generation of a proton motive force by the excretion of metal phosphate in the polyphosphate-accumulatingAcinetobacter johnsonii strain 210A. J. Biol. Chem. submitted

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN & Zehnder AJB (1994c) Translocation of metal phosphate via the inorganic phosphate transport system ofEscherichia coli. Biochem. 33: 1766–1770

    Google Scholar 

  • Verhoogt H, Smit H, Abee T, Gamper M, Driessen AJM, Haas D & Konings WN (1992)arcD, the first gene of thearc operon for anaerobic arginine catabolism inPseudomonas aeruginosa, encodes an arginine-ornithine exchanger. J. Bacteriol. 174: 156

    Google Scholar 

  • Winkler HH (1976) Rickettsial permeability. An ADD-ATP transport system. J. Biol. Chem. 251: 389–396

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Groningen, Biology Centre, Kerklaan 30, 9751 NN, Haren, The Netherlands

    Wil N. Konings, Bert Poolman & Hendrik W. van Veen

Authors
  1. Wil N. Konings
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bert Poolman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hendrik W. van Veen
    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

Konings, W.N., Poolman, B. & van Veen, H.W. Solute transport and energy transduction in bacteria. Antonie van Leeuwenhoek 65, 369–380 (1994). https://doi.org/10.1007/BF00872220

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00872220

Key words

Search

Navigation