1887

Abstract

Ambient pH regulates the expression of virulence genes of , but it was unknown if can regulate ambient pH. Mutants of altered in production of oxalic acid were evaluated for the interrelationship of ambient pH, buffering capacity added to media, growth, and generation of extracellular proteases and ammonia. Wild-type and acid-overproducing mutants [Acid(+)] grew almost as well at pH 8 as at pH 6, but acid-non-producing [Acid(−)] mutants showed limited growth at pH 8, indicating that acid production is linked to the ability to grow at higher pH. Production of ammonia by was strongly stimulated by low levels of amino acids in the medium when cells were derepressed for nitrogen and carbon. Likewise, although and produced some ammonia in minimal media, addition of low levels of amino acids enhanced production. Ammonia production by , and increased the pH of the medium and allowed production of subtilisin proteases, whose activities are observed only at basic pH. In contrast, protease production by the Acid(+) mutants of was greatly reduced because of the acidification of the medium. This suggests that alkalinization by ammonia production is adaptive by facilitating the utilization of proteinaceous nutrients. Collectively, the data imply that ammonia may have functions related to regulation of the microenvironment and that it represents a previously unconsidered virulence factor in diverse fungi with the potential to harm tissues and disturb the host’s immune system.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-145-10-2691
1999-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/145/10/1452691a.html?itemId=/content/journal/micro/10.1099/00221287-145-10-2691&mimeType=html&fmt=ahah

References

  1. Al-Aidroos, K. & Seifert, A. M. (1980). Polysaccharide and protein degradation, germination, and virulence against mosquitoes in the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 36, 29-34.[CrossRef] [Google Scholar]
  2. Arst, H. N. & Cove, D. J. (1969). Methylammonium resistance in Aspergillus nidulans. J Bacteriol 98, 1284-1293. [Google Scholar]
  3. Bidochka, M. J. & Khachatourians, G. G. (1993). Oxalic acid hyperproduction in Beauveria bassiana mutants is related to a utilizable carbon source but not to virulence. J Invertebr Pathol 62, 53-57.[CrossRef] [Google Scholar]
  4. Caddick, M. X., Brownlee, A. G. & Arst, H. N. (1986). Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol Gen Genet 203, 346-353.[CrossRef] [Google Scholar]
  5. Chaney, A. L. & Marbach, E. P. (1962). Modified reagents for the determination of urea and ammonia. Clin Chem 8, 130-132. [Google Scholar]
  6. Chen, G., Fournier, R. L., Varanasi, S. & Mahama-Relue, P. A. (1997).Helicobacter pylori survival in gastric mucosa by generation of a pH gradient. Biophys J 73, 1081-1088.[CrossRef] [Google Scholar]
  7. De Bernardis, F., Muhlschlegel, F. A., Cassone, A. & Fonzi, W. A. (1998). The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect Immun 66, 3317-3325. [Google Scholar]
  8. Doyle, C. & Butler, M. (1990). The effect of pH on the toxicity of ammonia to a murine hybridoma. J Biotechnol 15, 91-100.[CrossRef] [Google Scholar]
  9. Emerson, K., Russo, R. & Lund, R. (1975). Aqueous ammonia equilibrium calculations: effect of pH and temperature. J Fish Res Board Can 32, 2379-2383.[CrossRef] [Google Scholar]
  10. Godoy, G., Steadman, J. R., Dickman, M. B. & Dam, R. (1990). Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotina sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 37, 179-191.[CrossRef] [Google Scholar]
  11. Guerrini, V. H. (1997). Excretion of ammonia by Lucilia cuprina larvae suppresses immunity in sheep. Vet Immunol Immunopathol 56, 311-317.[CrossRef] [Google Scholar]
  12. Hallsworth, J. E. & Magan, N. (1996). Culture age, temperature, and pH affect the polyol and trehalose contents of fungal propagules. Appl Environ Microbiol 62, 2435-2442. [Google Scholar]
  13. Jennings, D. H. (1989). Some perspectives on nitrogen and phosphorus metabolism in fungi. In Nitrogen, Phosphorus and Sulphur Utilization by Fungi, pp. 1-31. Edited by L. Boddy, R. Marchant & D. J. Read. Cambridge, UK: Cambridge University Press.
  14. Larsen, J., Svensmark, B. & Nilsson, J. R. (1988). Variation in the growth medium during the culture cycle of Tetrahymena: with special reference to ammonia (NH3), ammonium ( ), and pH. J Protozool 35, 541-546.[CrossRef] [Google Scholar]
  15. Mekalanos, J. J. (1992). Environmental signals controlling expression of virulence determinants in bacteria. J Bacteriol 174, 1-7. [Google Scholar]
  16. Moore, D., Horner, J. & Liu, M. (1987). Co-ordinate control of ammonium-scavenging enzymes in the fruit body cap of Coprinus cinereus avoids inhibition of sporulation by ammonium. FEMS Microbiol Lett 44, 239-242.[CrossRef] [Google Scholar]
  17. Palkova, Z., Janderova, B., Gabriel, J., Zikanova, B., Pospisek, M. & Forstova, J. (1997). Ammonia mediates communications between yeast colonies. Nature 390, 532-535.[CrossRef] [Google Scholar]
  18. Robert, A. & Al-Aidroos, K. M. (1985). Acid production by Metarhizium anisopliae: effects on virulence against mosquitoes and on detection of in vitro amylase, protease, and lipase activity. J Invertebr Pathol 45, 9-15.[CrossRef] [Google Scholar]
  19. Robinson, I. P., Wimpenny, J. W. T. & Earnshaw, R. G. (1991). pH gradients through colonies of Bacillus cereus and the surrounding agar. J Gen Microbiol 137, 2885-2889.[CrossRef] [Google Scholar]
  20. Schaap, P., Brandt, R. & vanEs, S. (1995). Regulation of Dictyostelium adenylcyclases by morphogen-induced modulation of cytosolic pH or Ca2+ levels. Dev Biol 168, 179-188.[CrossRef] [Google Scholar]
  21. Schindler, J. & Sussman, M. (1977). Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. J Mol Biol 116, 161-169.[CrossRef] [Google Scholar]
  22. ter Schure, E. G., Sillje, H. H., Verkleij, A. J., Boonstra, J. & Verrips, C. T. (1995). The concentration of ammonia regulates nitrogen metabolism in Saccharomycescerevisiae. J Bacteriol 177, 6672-6675. [Google Scholar]
  23. Sikora, L. & Marzluf, G. A. (1982). Regulation of l-amino acid oxidase and d-amino acid oxidase in Neurospora crassa. Mol Gen Genet 186, 33-39.[CrossRef] [Google Scholar]
  24. St Leger, R. J., Charnley, A. K. & Cooper, R. M. (1987). Characterization of cuticle-degrading proteases produced by the entomopathogen Metarhizium anisopliae. Arch Biochem Biophys 253, 221-232.[CrossRef] [Google Scholar]
  25. St Leger, R. J., Bidochka, M. J. & Roberts, D. W. (1994). Isoforms of the cuticle degrading Pr1 protease and production of a metalloproteinase by Metarhizium anisopliae. Arch Biochem Biophys 313, 1-7.[CrossRef] [Google Scholar]
  26. St Leger, R. J., Joshi, L. & Roberts, D. (1998). Ambient pH is a major determinant in the expression of cuticle-degrading enzymes and hydrophobin by Metarhizium anisopliae. Appl Environ Microbiol 64, 709-713. [Google Scholar]
  27. Strasser, H., Burgstaller, W. & Schinner, F. (1994). High-yield production of oxalic acid for metal leaching processes by Aspergillus niger. FEMS Microbiol Lett 119, 365-370.[CrossRef] [Google Scholar]
  28. Takahashi, N., Saito, K., Schchtele, C. F. & Yamada, T. (1997). Acid tolerance and acid-neutralizing activity of Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 12, 323-328.[CrossRef] [Google Scholar]
  29. Tsuboi, R., Matsuda, K., Ko, I. J.& Ogawa, H. (1989). Correlationbetween culture medium pH, extracellular proteinase activity,and cell growth of Candida albicans in insoluble stratumcorneum-supplemented media.Arch Dermatol Res 281, 342-345.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-145-10-2691
Loading
/content/journal/micro/10.1099/00221287-145-10-2691
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error