Antonie van Leeuwenhoek

, Volume 65, Issue 4, pp 381–395 | Cite as

Bacterial sodium ion-coupled energetics

  • P. Dimroth
Research Articles

Abstract

For many bacteria Na+ bioenergetics is important as a link between exergonic and endergonic reactions in the membrane. This article focusses on two primary Na+ pumps in bacteria, the Na+-translocating oxaloacetate decarboxylase ofKlebsiella pneumoniae and the Na+-translocating F1F0 ATPase ofPropionigenium modestum. Oxaloacetate decarboxylase is an essential enzyme of the citrate fermentation pathway and has the additional function to conserve the free energy of decarboxylation by conversion into a Na+ gradient. Oxaloacetate decarboxylase is composed of three different subunits and the related methylmalonyl-CoA decarboxylase consists of five different subunits. The genes encoding these enzymes have been cloned and sequenced. Remarkable are large areas of complete sequence identity in the integral membrane-bound β-subunits including two conserved aspartates that may be important for Na+ translocation. The coupling ratio of the decarboxylase Na+ pumps depended on\(\Delta \tilde \mu Na^ + \) and decreased from two to zero Na+ uptake per decarboxylation event as\(\Delta \tilde \mu Na^ + \) increased from zero to the steady state level.

InP. modestum,\(\Delta \tilde \mu Na^ + \) is generated in the course of succinate fermentation to propionate and CO2. This\(\Delta \tilde \mu Na^ + \) is used by a unique Na+-translocating F1F0 ATPase for ATP synthesis. The enzyme is related to H+-translocating F1F0 ATPases. The F0 part is entirely responsible for the coupling of ion specificity. A hybrid ATPase formed by in vivo complementation of anEscherichia coli deletion mutant was completely functional as a Na+-ATP synthase conferring theE. coli strain the ability of Na+-dependent growth on succinate. The hybrid consisted of subunits a, c, b, δ and part of α fromP. modestum and of the remaining subunits fromE. coli. Studies on Na+ translocation through the F0 part of theP. modestum ATPase revealed typical transporter-like properties. Sodium ions specifically protected the ATPase from the modification of glutamate-65 in subunit c by dicyclohexylcarbodiimide in a pH-dependent manner indicating that the Na+ binding site is at this highly conserved acidic amino acid residue of subunit c within the middle of the membrane.

Key words

citrate fermentation F1F0 ATPase ion translocation mechanism Klebsiella pneumoniae Propionigenium modestum sodium translocating decarboxylases 

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References

  1. Amann R, Ludwig W, Laubinger W, Dimroth P & Schleifer KH (1988) Cloning and sequencing of the gene encoding the β-subunit of the sodium ion translocating ATP synthase ofPropionigenium modestum. FEMS Microbiol. Lett. 65: 253–260Google Scholar
  2. Antranikian G & Giffhorn F (1987) Citrate metabolism in anaerobic bacteria. FEMS Microbiol. Rev. 46: 175–198Google Scholar
  3. Beatrix B, Bendrat K, Rospert S & Buckel W (1990) The biotin-dependent sodium ion pump glutaconyl-CoA decarboxylase fromFusobacterium nucleatum. Arch. Microbiol. 154: 362–369PubMedGoogle Scholar
  4. Buckel W & Semmler (1983) Purification, characterization and reconstitution of glutaconyl-CoA decarboxylase, a biotin-dependent sodium pump from anaerobic bacteria. Eur. J. Biochem. 136: 427–434PubMedGoogle Scholar
  5. Dibrov PA, Kostyrko VA, Lazarova RL, Skulachev VP & Smirnova IA (1986) Na+-dependent motility and modes of membrane energization in the marine alkalotolerantVibrio alginolyticus. Biochim. Biophys. Acta 850: 449–457PubMedGoogle Scholar
  6. Dimroth P & Hilpert W (1984) Carboxylation of pyruvate and acetyl-CoA by reversal of the Na+ pumps oxaloacetate decarboxylase and methylmalonyl-CoA decarboxylase. Biochemistry 23: 5360–5366Google Scholar
  7. Dimroth P & Thomer A (1983) Subunit composition of oxaloacetate decarboxylase and characterization of the α-chain as carboxyl-transferase. Eur. J. Biochem. 137: 107–112PubMedGoogle Scholar
  8. Dimroth P & Thomer A (1986) Citrate transport inKlebsiella pneumoniae. Biol. Chem. Hoppe-Seyler 367: 813–823PubMedGoogle Scholar
  9. Dimroth P & Thomer A (1989) A primary respiratory Na+ pump of an anaerobic bacterium: the Na+-dependent NADH: quinone oxidoreductase ofKlebsiella pneumoniae. Arch. Microbiol. 151: 439–444PubMedGoogle Scholar
  10. Dimroth P & Thomer A (1990) Solubilization and reconstitution of the Na+-dependent citrate carrier ofKlebsiella pneumoniae. J. Biol. Chem. 265: 7721–7724PubMedGoogle Scholar
  11. Dimroth P & Thomer A (1992) The sodium ion pumping oxaloacetate decarboxylase ofKlebsiella pneumoniae. Metal ion content, inhibitors and proteolytic degradation studies. FEBS Lett. 300: 67–70PubMedGoogle Scholar
  12. Dimroth P & Thomer A (1993) On the mechanism of sodium ion translocation by oxaloacetate decarboxylase ofKlebsiella pneumoniae. Biochemistry 31: 1734–1739Google Scholar
  13. Dimroth P (1980) A new sodium transport system energized by the decarboxylation of oxoaloacetate. FEBS Lett. 122: 234–236PubMedGoogle Scholar
  14. Dimroth P (1982a) The robe of biotin and sodium in the decarboxylation of oxaloacetate by the membrane-bound oxaloacetate decarboxylase fromKlebsiella aerogenes. Eur. J. Biochem. 121: 435–441PubMedGoogle Scholar
  15. Dimroth P (1982b) The generation of an electrochemical gradient of sodium ions upon decarboxylation of oxaloacetate by the membrane-bound and Na+-activated oxaloacetate decarboxylase fromKlebsiella aerogenes. Eur. J. Biochem. 121: 443–449PubMedGoogle Scholar
  16. Dimroth P (1987) Sodium ion transport decarboxylases and other aspects of sodium cycling in bacteria. Microbiol. Rev. 51: 320–340PubMedGoogle Scholar
  17. Dimroth P (1988) The role of vitamines and their carrier proteins in citrate fermentation. In: Kleinkauf H, Döhren H & Jaenicke L (Eds) The Roots of Modern Biochemistry (pp 191–204) Walter de Gruyter, BerlinGoogle Scholar
  18. Dimroth P (1990) Mechanisms of sodium transport in bacteria. Phil. Trans. R. Soc. Lond. B 326: 465–477Google Scholar
  19. Dimroth P (1993) Na+ extrusion coupled to decarboxylation reactions: In: Bakker EP (Ed) Akali Cation Transport Systems in Prokaryotes (pp 77–100) CRC Press, Boca RatonGoogle Scholar
  20. Dimroth P (1993) The Na+-translocating ATP-synthetase fromPropionigenium modestum. In: Bakker EP (Ed) Akali Cation Transport Systems in Prokaryotes (pp 139–154) CRC Press, Boca RatonGoogle Scholar
  21. Efiok BJS & Webster DA (1990) A cytochrome that can pump sodium ion. Biochem. Biophys. Res. Commun. 173: 370–375Google Scholar
  22. Esser U, Krumholz LR & Simoni RD (1990) Nucleotide sequence of the F0 subunits of the sodium dependent F1F0 ATPase ofPropionigenium modestum. Nucleic Acids Res. 18: 5887Google Scholar
  23. Gerike U & Dimroth P (1993) N-terminal amino acid sequences of the subunits of the Na+-translocating F1F0 ATPase fromPropionigenium modestum. FEBS Lett. 316: 89–92PubMedGoogle Scholar
  24. Heise R, Müller V & Gottschalk G (1992) Presence of a sodium-translocating ATPase in membrane vesicles of the homoacetogenic bacteriumAcetobacterium woodii. Eur. J. Biochem. 206: 553–557Google Scholar
  25. Hilpert W, Schink B & Dimroth P (1984) Life by a new decarboxylation-dependent energy conservation mechanism with Na+ as coupling ion. EMBO J. 3: 1665–1670Google Scholar
  26. Hilpert W & Dimroth P (1983) Purification and characterization of a new sodium transport decarboxylase. Methylmalonyl-CoA decarboxylase fromVeillonella alcalescens. Eur. J. Biochem. 132: 579–587Google Scholar
  27. Hilpert W & Dimroth P (1984) Reconstitution of Na+ transport from purified methylmalonyl-CoA decarboxylase and phospholipid vesicles. Eur. J. Biochem 138: 579–583PubMedGoogle Scholar
  28. Hilpert W & Dimroth P (1991) On the mechanism of sodium ion translocation by methylmalonyl-CoA decarboxylase fromVeillonella alcalescens. Eur. J. Biochem. 195: 79–86PubMedGoogle Scholar
  29. Hirota H & Imae Y (1983) Na+-driven flagellar motors of an alkaliphilic Bacillus strain YN-1. J. Biol. Chem. 258: 10577–10581PubMedGoogle Scholar
  30. Huder J & Dimroth P (1993) Sequence of the sodium ion pump methylmalonyl-CoA decarboxylase fromVeillonella parvula. J. Biol. Chem. 268: 24564–24571Google Scholar
  31. Kaim G, Ludwig W, Dimroth P & Schleifer KH (1990) Sequence of subunits a and b of the sodium ion translocating adenosine triphosphate synthase ofPropionigenium modestum. Nucleic Acids Res. 18: 6697PubMedGoogle Scholar
  32. Kaim G, Ludwig W, Dimroth P & Schleifer KH (1992) Cloning, sequencing andin vivo expression of genes encoding the F0 part of the sodium-ion-dependent ATP synthase ofPropionigenium modestum inEscherichia coli. Eur. J. Biochem. 207: 463–470PubMedGoogle Scholar
  33. Kaim G & Dimroth P (1993) Formation of a functionally active sodium-translocating hybrid F1F0 ATPase inEscherichia coli by homologous recombination. Eur. J. Biochem. 218: 937–944Google Scholar
  34. Ken-Dror S, Lanyi JK, Schobert B, Silver B & Avi-Dor Y (1986) An NADH: quinone oxidoreductase of the halotolerant bacterium Ba1 is specifically dependent on sodium ions. Arch. Biochem. Biophys. 244: 766–772Google Scholar
  35. Kluge C & Dimroth P (1992) Studies on Na+ and H+ translocation through the F0 part of the Na+-translocating F1F0 ATPase fromPropionigenium modestum: discovery of a membrane potential dependent step. Biochemistry 31: 12665–12672Google Scholar
  36. Kluge C & Dimroth P (1993a) Kinetics of inactivation of the F1F0 ATPase ofPropionigenium modestum by dicyclohexylcarbodiimide in relationship to H+ and Na+ concentration: probing the binding site for the coupling ions. Biochemistry 31: 10378–10386Google Scholar
  37. Kluge C & Dimroth P (1993b) Specific protection by Na+ or Li+ of the F1F0 ATPase ofPropionigenium modestum from the reaction with dicyclohexylcarbodiimide. J. Biol. Chem. 268: 14557–14560PubMedGoogle Scholar
  38. Kluge G, Laubinger W & Dimroth P (1992) The Na+-translocating ATPase ofPropionigenium modestum. Trans. Biochem. Soc. 20: 572–577Google Scholar
  39. Laubinger W, Deckers-Hebestreit G, Alterndorf K & Dimroth P (1990) A hybrid adenosinetriphosphatase composed of F1 ofEscherichia coli and F0 ofPropionigenium modestum is a functional sodium ion pump. Biochemistry 29: 5458–5463PubMedGoogle Scholar
  40. Laubinger W & Dimroth P (1987) Characterization of the Na+-stimulated ATPase ofPropionigenium modestum as an enzyme of the F1F0 type. Eur. J. Biochem. 168: 475–480PubMedGoogle Scholar
  41. Laubinger W & Dimroth P (1988) Characterization of the ATP synthase ofPropionigenium modestum as a primary sodium pump. Biochemistry 27: 7531–7537Google Scholar
  42. Laubinger W & Dimroth P (1989) The sodium ion translocating adenosinetriphosphatase ofPriopionigenium modestum pumps protons at low sodium ion concentrations. Biochemistry 28: 7194–7198PubMedGoogle Scholar
  43. Laußermair E, Schwarz E, Oesterhelt D, Reinke H, Beyreuther K & Dimroth P (1989) The sodium ion translocating oxaloacetate decarboxylase ofKlebsiella pneumoniae. Sequence of the integral membrane-bound subunits β and γ. J. Biol. Chem. 264: 14710–14715PubMedGoogle Scholar
  44. Ludwig W, Kaim G, Laubinger W, Dimroth P, Hoppe J & Schleifer KH (1990) Sequence of subunit c of the sodiumion translsocating adenosine triphosphate synthase ofPropionigenium modestum. Eur. J. Biochem. 193: 395–399Google Scholar
  45. Mitchell P (1974) A chemiosmotic molecular mechanism for protontranslocating adenosine triphosphatases. FEBS Lett. 43: 189–194PubMedGoogle Scholar
  46. Müller V & Gottschalk G (1993) Na+ translocation in the course of methanogenesis from methanol or formaldehyde. In: Bakker EP (Ed) Alkali Cation Transport Systems in Prokaryotes (pp 155–177) CRC Press, Boca RatonGoogle Scholar
  47. Padan E & Suldiner S (1993) Na+ transport systems in prokaryotes. In: Bakker EP (Ed) Alkali Cation Transport Systems in Prokaryotes (pp 3–24) CRC Press, Boca RatonGoogle Scholar
  48. Pfenninger-Li XD & Dimroth P (1992) NADH formation by Na+-coupled reversed electron transfer inKlebsiella pneumoniae. Mol. Microbiol. 6: 1943–1948PubMedGoogle Scholar
  49. Schönheit P (1993) The role of Na+ in the first step of CO2 reduction to methane in methanogenic bacteria. In: Bakker EP (Ed) Alkali Cation Transport Systems in Prokaryotes (pp 179–202) CRC Press, Boca RatonGoogle Scholar
  50. Schuldiner S & Padan E (1993) Na+/H+ antiporters inEscherichia coli: In: Bakker EP (Ed) Alkali Cation Transport Systems in Prokaryotes (pp 25–51) CRC Press, Boca RatonGoogle Scholar
  51. Schwarz E, Oesterhelt D, Reinke H, Beyreuther K & Dimroth P (1988) The sodium translocating oxaloacetate decarboxylase ofKlebsiella pneumoniae. Sequence of the biotin-containing α-subunit and relationship to other biotin-containing enzymes. J. Biol. Chem. 263: 9640–9645Google Scholar
  52. Schwarz E & Oesterhelt D (1985) Cloning and expression ofKlebsiella pneumoniae genes coding for citrate transport and fermentation. EMBO J. 4: 1599–1603PubMedGoogle Scholar
  53. Speelmans G, Poolman B, Abee T & Konings WL (1993) Energy transduction in the thermophilic anaerobic bacteriumClostridium fervidus is exclusively coupled to sodium ions. Proc. Natl. Acad. Sci. USA 90: 7975–7979Google Scholar
  54. Thauer RK, Jungermann K & Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41: 100–180PubMedGoogle Scholar
  55. Tokuda H (1993) The Na+ cycle inVibrio alginolyticus. In: Bakker EP (Ed) Alkali Cation Transport Systems in Prokaryotes (pp 125–138) CRC Press, Boca RatonGoogle Scholar
  56. Tokuda H & Unemoto T (1984) Na+ is translocated at NADH: quinone oxidoreductase segment in the respiratory chain ofVibrio alginolyticus. J. Biol. Chem. 259: 7785–7790PubMedGoogle Scholar
  57. van der Rest M., Siewe R, Abee T, Schwarz E, Oesterhelt D & Konings WN (1992) Nucleotide sequence and functional properties of a sodium-dependent citrate transport system fromKlebsiella pneumoniae. J. Biol. Chem. 267: 8971–8976PubMedGoogle Scholar
  58. Wifling K & Dimroth P (1989) Isolation and characterization of oxaloacetate decarboxylase ofSalmonella typhimurium, a sodium ion pump. Arch. Microbiol. 152: 584–588PubMedGoogle Scholar
  59. Woehlke G, Laußermair E, Schwarz E, Oesterhelt D, Reinke H, Beyreuther K & Dimroth P (1992b) Sequence of the β-subunit of oxaloacetate decarboxylase fromKlebsiella pneumoniae: a correction of the C-terminal part. J. Biol. Chem. 267: 22804–22805Google Scholar
  60. Woehlke G, Wifling K & Dimroth P (1992a) Sequence of the sodium ion pump oxaloacetate decarboxylase fromSalmonella typhimurium J. Biol. Chem. 267: 22798–22803Google Scholar
  61. Yamato I & Anraku Y (1993) Na+/substrate symport in prokaryotes: In: Bakker EP (Ed) Akali Cation Transport Systems in Prokaryotes (pp 53–76) CRC Press, Boca RatonGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • P. Dimroth
    • 1
  1. 1.Mikrobiologisches InstitutEidgenössische Technische Hochschule, ETH-ZentrumZürichSwitzerland

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