Archives of Microbiology

, Volume 164, Issue 5, pp 363–369

Differential effects of sodium ions on motility in the homoacetogenic bacteriaAcetobacterium woodii andSporomusa sphaeroides

Original Paper

Abstract

The strictly anaerobic homoacetogenic bacteriaAcetobacterium woodii andSporomusa sphaeroides differ with respect to their energy metabolism. Since growth as well as acetate and ATP formation ofA. woodii is strictly dependent on Na+, but that ofS. sphaeroides is not, the question arose whether these organisms also use different coupling ions for mechanical work, i.e. flagellar rotation. During growth on fructose in the presence of Na+ (50 mM), cells ofA. woodii were vigorously motile, as judged by light microscopy. At low Na+ concentrations (0.3 mM), the growth rate decreased by only 15%, but the cells were completely non-motile. Addition of Na+ to such cultures restored motility instantaneously. Motility, as determined in swarm agar tubes, was strictly dependent on Na+; Li+, but not K+ partly substituted for Na+. Of the amilorides tested, phenamil proved to be a specific inhibitor of the flagellar motor ofA. woodii. Growth and motility ofS. sphaeroides was neither dependent on Na+ nor inhibited by amiloride derivatives. These results indicate that flagellar rotation is driven by\(\Delta \tilde \mu _{Na^ + } \) inA. woodii, but by\(\Delta \tilde \mu _{H^ + } \) inS. sphaeroides.

Key words

Homoacetogenic bacteria Flagellar rotation Na+ H+ Acetobacterium woodii Sporomusa sphaeroides 

Abbreviations

Amiloride

3,5-Diamino-6-chloropyrazinoylguanidine

Benzamil N10

benzyl amiloride

\(\Delta \tilde \mu _{H^ + } \)

Electrochemical proton potential

\(\Delta \tilde \mu _{Na^ + } \)

Electrochemical sodium ion potential

ETH2120 N, N, N′, N′

Tetracyclohexyl-1,2-phenylenedioxydiacetamide

SF6847

3,5-Di-tert-butyl-4-hydroxybenzylidenemalonitrile

Phenamil N10

phenyl amiloride

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References

  1. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628PubMedCrossRefGoogle Scholar
  2. Atsumi T, Sugiyama S, Cragoe EJ Jr, Imae Y (1990) Specific inhibition of the Na+-driven flagellar motors of alkalophilicBacillus strains by the amiloride analog phenamil. J Bacteriol 172:1634–1639PubMedGoogle Scholar
  3. Atsumi T, McCarter L, Imae Y (1992a) Polar and lateral flagellar motors of marineVibrio are driven by different ion-motive forces. Nature 355:182–184PubMedCrossRefGoogle Scholar
  4. Atsumi T, Maekawa Y, Tokuda H, Imae Y (1992b) Amiloride at pH 7.0 inhibits the Na+-driven flagellar motors ofVibrio alginolyticus but allows cell growth. FEBS Lett 314:114–116PubMedCrossRefGoogle Scholar
  5. Becher B, Müller V (1994)\(\Delta \tilde \mu _{Na^ + } \) drives the synthesis of ATP via an\(\Delta \tilde \mu _{Na^ + } \)-translocating F1F0-ATP synthase in membrane vesicles of the archaeonMethanosarcina mazei Göl. J Bacteriol 176:2543–2550PubMedGoogle Scholar
  6. Bryant MP (1972) Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr 25:1324–1328PubMedGoogle Scholar
  7. Dangel W, Schulz H, Diekert G, König H, Fuchs G (1987) Occurrence of corrinoid-containing membrane proteins in anaerobic bacteria. Arch Microbiol 148:52–56CrossRefGoogle Scholar
  8. Dibrov PA, Kostyrko VA, Lazarova RJ, Skulachev VP, Smironova IA (1986) The sodium ion cycle. 1. Na+-dependent motility and modes of membrane energization in the marine alkalotolerantVibrio alginolyticus. Biochim Biophys Acta 850:449–457PubMedCrossRefGoogle Scholar
  9. Diekert G, Wohlfarth G (1994) Metabolism of homoacetogens. Antonie Van Leeuwenhoek 66:209–221PubMedCrossRefGoogle Scholar
  10. Fuchs G (1986) CO2 fixation in acetogenic bacteria: variations on a theme, FEMS Microbiol Rev 39:181–213CrossRefGoogle Scholar
  11. Geerligs G, Schönheit P, Diekert G (1989) Sodium-dependent acetate formation from CO2 inPeptostreptococcus productus (strain Marburg). Arch Microbiol 148:305–313CrossRefGoogle Scholar
  12. Heise R, Müller V, Gottschalk G (1989) Sodium dependence of acetate formation by the acetogenic bacteriumAcetobacterium woodii. J Bacteriol 171:5473–5478PubMedGoogle Scholar
  13. Heise R, Reidlinger J, Müller V, Gottschalk G (1991) A sodium-stimulated ATP synthase in the acetogenic bacteriumAcetobacterium woodii. FEBS Lett 295:119–122PubMedCrossRefGoogle Scholar
  14. 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: 553–557PubMedCrossRefGoogle Scholar
  15. Heise R, Müller V, Gottschalk G (1993) Acetogenesis and ATP synthesis inAcetobacterium woodii are coupled via a transmembrane primary sodium ion gradient. FEMS Microbiol Lett 112:261–268CrossRefGoogle Scholar
  16. Hirota N, Kitada M, Imae Y (1981) Flagellar motors of alkalophilicBacillus are powered by an electrochemical potential gradient of Na+. FEBS Lett 132:278–280CrossRefGoogle Scholar
  17. Hugenholtz J, Ljungdahl LG (1990) Metabolism and energy generation in homoacetogenic clostridia. FEMS Microbiol Rev 87: 383–389CrossRefGoogle Scholar
  18. Hugenholtz JD, Ivey M, Ljungdahl LG (1987) Carbon monoxidedriven electron transport inClostridium thermoautotrophicum membranes. J Bacteriol 169:5845–5847PubMedGoogle Scholar
  19. Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Methods in enzymology, vol 3 B. Academic Press, New York London, pp 117–132Google Scholar
  20. Jones CJ, Aizawa SI (1991) The bacterial flagellum and flagellar motor: structure, function and assembly. Adv Microb Physiol 32:110–172CrossRefGoogle Scholar
  21. Kamlage B (1994) Die Bedeutung der Cytochrome für den Acetyl-CoA-Weg in dem strikt anaeroben homoacetogenen OrganismusSporomusa sphaeroides. Ph D thesis. University of GöttingenGoogle Scholar
  22. Kamlage B, Boelter A, Blaut M (1993) Spectroscopic and potentiometric characterization of cytochromes in twoSporomusa species and their expression during growth on selected substrates. Arch Microbiol 159:189–196CrossRefGoogle Scholar
  23. Kleyman TR, Cragoe E Jr (1988) Amiloride and its analogs as tools for the study of ion transport. J Membr Biol 105:1–21PubMedCrossRefGoogle Scholar
  24. Kluge C, Dimroth P (1993) 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 ion. Biochemistry 32:10378–10386PubMedCrossRefGoogle Scholar
  25. Kluge C, Laubinger W, Dimroth P (1992) The Na+-translocating ATPase ofPropionigenium modestum. Biochem Soc Trans 20: 572–577PubMedGoogle Scholar
  26. Mayer F, Lurz R, Schoberth S (1977) Electron microscopic investigation of the hydrogen-oxidizing acetate-forming anaerobic bacteriumAcetobacterium woodii. Arch Microbiol 115:207–213PubMedCrossRefGoogle Scholar
  27. Macnab R (1987a) Flagella. In: Neidhardt FC, Ingraham HE, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds)Escherichia coli andSalmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 70–83Google Scholar
  28. Macnab R (1987b) Motility and chemotaxis. In: Neidhardt FC, Ingraham HE, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds)Escherichia coli andSalmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 732–759Google Scholar
  29. McCarter L (1994a) MotY, a component of the sodium-type flagellar motor. J Bacteriol 176:4219–4225PubMedGoogle Scholar
  30. McCarter L (1994b) MotX, the channel component of the sodium-type flagellar motor. J Bacteriol 176:5988–5998PubMedGoogle Scholar
  31. Möller B, Oßmer R, Howard H, Gottschalk G, Hippe H (1984)Sporomusa, a new genus of gram-negative anaerobic bacteria includingSporomusa sphaeroides spec. nov. andSporomusa ovata spec. nov. Arch Microbiol 139:85–90CrossRefGoogle Scholar
  32. Müller V, Gottschalk G (1994) The sodium ion cycle in acetogenic and methanogenic bacteria: generation and utilization of a primary electrochemical sodium ion gradient. In: Drake HL (ed) Acetogenesis. Chapman & Hall, New York, pp 127–156Google Scholar
  33. Reidlinger J, Müller V (1994) Purification of ATP synthase fromAcetobacterium woodii and identification as a Na+-translocating F1F0-type enzyme. Eur J Biochem 223:275–283PubMedCrossRefGoogle Scholar
  34. Speelmans G, Poolman B, Abee T, Konings WN (1993a) Energy transduction in the thermophilic anaerobic bacteriumClostridium fervidus is exclusively coupled to sodium ions. Proc Natl Acad Sci USA 90:7975–7979PubMedCrossRefGoogle Scholar
  35. Speelmans G, Poolman B, Konings WN (1993b) Amino acid transport in the thermophilic anaerobeClostridium fervidus is driven by an electrochemical sodium gradient. J Bacteriol 175: 2060–2066PubMedGoogle Scholar
  36. Speelmans G, Poolman B, Abee T, Konings WN (1994) The F- or V-type Na+-ATPase of the thermophilic bacteriumClostridium fervidus. J Bacteriol 176:5160–5162PubMedGoogle Scholar
  37. Spruth M, Reidlinger J, Müller V (1995) Sodium ion dependence of inhibition of the Na+-translocating F1F0-ATPase fromAcetobacterium woodii. Probing the site(s) involved in ion transport. Biochim Biophys Acta 1229:96–102CrossRefGoogle Scholar
  38. Sugiyama S, Cragoe EJ Jr, Imae Y (1988) Amiloride, a specific inhibitor for the Na+-driven flagellar motors of alkalophilicBacillus. J Biol Chem 262:8215–8219Google Scholar
  39. Tschech A, Pfennig N (1984) Growth yield increase linked to caffeate reduction inAcetobacterium woodii. Arch Microbiol 137: 163–167CrossRefGoogle Scholar
  40. Wood HG, Ljungdahl LG (1991) Autotrophic character of the acetogenic bacteria. In: Shively J, Barton LL (eds) Variations in autotrophic life. Academic Press, New York London, pp 201–250Google Scholar
  41. Yang H, Drake HL (1990) Differential effects of sodium on hydrogen-and glucose-dependent growth of the acetogenic bacteriumAcetogenium kivui. Appl Environ Microbiol 56:81–86PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  1. 1.Institut für Mikrobiologie der Georg-August-Universität GöttingenGöttingenGermany

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