Archives of Microbiology

, Volume 161, Issue 4, pp 286–292 | Cite as

The adaptive acid tolerance response in root nodule bacteria and Escherichia coli

  • Graham W. O'Hara
  • Andrew R. Glenn
Original Papers


Root nodule bacteria and Escherichia coli show an adaptive acid tolerance response when grown under mildly acidic conditions. This is defined in terms of the rate of cell death upon exposure to acid shock at pH 3.0 and expressed in terms of a decimal reduction time, D. The D values varied with the strain and the pH of the culture medium. Early exponential phase cells of three strains of Rhizobium leguminosarum (WU95, 3001 and WSM710) had D values of 1, 6 and 5 min respectively when grown at pH 7.0; and D values of 5, 20 and 12 min respectively when grown at pH 5.0. Exponential phase cells of Rhizobium tropici UMR1899, Bradyrhizobium japonicum USDA110 and peanut Bradyrhizobium sp. NC92 were more tolerant with D values of 31, 35 and 42 min when grown at pH 7.0; and 56, 86 and 68 min when grown at pH 5.0. Cells of E. coli UB1301 in early exponential phase at pH 7.0 had a D value of 16 min, whereas at pH 5.0 it was 76 min. Stationary phase cells of R. leguminosarum and E. coli were more tolerant (D values usually 2 to 5-fold higher) than those in exponential phase. Cells of R. leguminosarum bv. trifolii 3001 or E. coli UB1301 transferred from cultures at pH. 7.0 to medium at pH 5.0 grew immediately and induced the acid tolerance response within one generation. This was prevented by the addition of chloramphenicol. Acidadapted cells of Rhizobium leguminosarum bv. trifolii WU95 and 3001; or E. coli UB1301, M3503 and M3504 were as sensitive to UV light as those grown at neutral pH.

Key words

Acid shock Rhizobium Bradyrhizobium Escherichia coli pH Tolerance 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aliabadi Z, Park YK, Slonczewski JL, Foster JW (1988) Novel regulatory loci controlling oxygen- and pH-regulated gene expression in Salmonella typhimurium. J Bacteriol 170: 842–851Google Scholar
  2. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84: 188–198Google Scholar
  3. Bromfield ESP, Jones DG (1980) Studies on acid tolerance of Rhizobium trifolii in culture and soil. J Appl Bacteriol 48: 253–264Google Scholar
  4. Farber JM, Pagatto F (1992) The effect of acid shock on the heat resistance of Listeria monocytogenes. Lett Appl Microbiol 15: 197–201Google Scholar
  5. Flis S, Glenn AR, Dilworth MJ (1993) The interaction between aluminium and root nodule bacteria. Soil Biol Biochem 25: 403–417Google Scholar
  6. Foster JW (1991) Salmonella acid shock proteins are required for the acid tolerance response. J Bacteriol 173: 6896–6902Google Scholar
  7. Foster JW, Hall HK (1990) Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol 172: 771–778Google Scholar
  8. Foster JW, Hall HK (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173: 5129–5135Google Scholar
  9. Goodson M, Rowbury RJ (1989a) Habituation to normally lethal acidity by prior growth of Escherichia coli at a sub-lethal acid pH value. Lett Appl Microbiol 8: 77–79Google Scholar
  10. Goodson M, Rowbury RJ (1989b) Resistance of acid-habituated Escherichia coli to organic acids and its medical and applied significance. Lett Appl Microbiol 8: 211–214Google Scholar
  11. Goodson M, Rowbury RJ (1991) RecA-independent resistance to irradiation with u.v. light in acid-habituated Escherichia coli. J Appl Bacteriol 70: 177–180Google Scholar
  12. Hassani M, Pincus DH, Bennett GN, Hirshfield IN (1992) Temperature-dependant induction of an acid-inducible stimulon of Escherichia coli in broth. Appl Environ Microbiol 58: 2704–2707Google Scholar
  13. Hickey EW, Hirshfield IN (1990) Low-pH-induced effects on patterns of protein synthesis and on internal pH in Escherichia coli and Salmonella typhimurium. Appl Environ Microbiol 56: 1038–1045Google Scholar
  14. Howieson JG, Ewing MA, D'Antuono MF (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105: 179–188Google Scholar
  15. Lowendorf HS, Alexander M (1983a) Identification of Rhizobium phaseoli strains that are tolerant or sensitive to soil acidity. Appl Environ Microbiol 45: 737–742Google Scholar
  16. Lowendorf HS, Alexander M (1983b) Selecting Rhizobium meliloti for inoculation of alfalfa planted in acid soils. Soil Sci Soc Am J 47: 935–938Google Scholar
  17. Munns DN, Keyser HH, Fogle VW, Hohenberg JS, Righetti TL, Lauter DL, Zaroug MG, Clarkin KL, Whitacre KW (1979) Tolerance of soil acidity in mung bean with rhizobia. Agron J 71: 256–260Google Scholar
  18. Munns DN (1986) Acid soil tolerance in legumes and rhizobia. In: Tinker B, Lauchli A (eds) Advances in plant nutrition. Praeger Scientific, New York, pp 63–90Google Scholar
  19. O'Hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid-tolerance in Rhizobium meliloti. Appl Environ Microbiol 55: 1870–1876Google Scholar
  20. Raja N, Goodson M, Chui WCM, Smith DG, Rowbury RJ (1991) Habituation to acid in Escherichia coli: conditions for habituation and its effects on plasmid transfer. J Appl Bacteriol 70: 59–65Google Scholar
  21. Rice WA (1982) Performance of Rhizobium meliloti strains selected for low-pH tolerance. Can J Plant Sci 62: 941–948Google Scholar
  22. Richardson AE, Simpson RJ (1988) Enumeration and distribution of Rhizobium trifolii under a subterranean clover-based pasture growing in an acid soil. Soil Biol Biochem 20: 431–438Google Scholar
  23. Robson AD, Bottomley PJ (1991) Limitations in the use of legumes in agriculture and forestry. In: Dilworth MJ, Glenn AR (eds) The biology and biochemistry of nitrogen fixation. Elsevier, Amsterdam, pp 320–349Google Scholar
  24. Robson AD, Loneragan JF (1970a) Nodulation and growth of Medicago truncatula on acid soils. I. Effect of calcium carbonate and inoculation level on the nodulation of Medicago truncatula on a moderately acid soil. Aust J Agric Res 21: 427–434Google Scholar
  25. Robson AD, Loneragan JF (1970b) Nodulation and growth of Medicago truncatula on acid soils. II. Colonization of acid soils by Rhizobium meliloti. Aust J Agric Res 21: 435–445Google Scholar
  26. Rowbury RJ, Goodson M, Whiting GC (1989) Habituation of Escherichia coli to acid and alkaline pH and its relevance for bacterial survival in chemically-polluted natural waters. Chem Ind 685–686Google Scholar
  27. Thornton FC, Davey CB (1983) Response of the clover-rhizobium symbiosis to soil acidity and rhizobium strain. Agron J 75: 557–560Google Scholar
  28. Thornton FC, Davey CB (1984) Saprophytic competence of acid tolerant strains of Rhizobium trifolii in acid soil. Plant Soil 80: 337–344Google Scholar
  29. Watson N, Dunyak DS, Rosey EL, Slonczewski JL, Olson ER (1992) Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH. J Bacteriol 174: 530–540Google Scholar

Copyright information

© Springer Verlag 1994

Authors and Affiliations

  • Graham W. O'Hara
    • 1
  • Andrew R. Glenn
    • 1
  1. 1.Nitrogen Fixation Research Group, School of Biological and Environmental SciencesMurdoch UniversityMurdochAustralia

Personalised recommendations