Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Dec;160(3):1047–1054. doi: 10.1128/jb.160.3.1047-1054.1984

Cyclic AMP levels during induction and repression of cellulase biosynthesis in Thermomonospora curvata.

W E Wood, D G Neubauer, F J Stutzenberger
PMCID: PMC215817  PMID: 6094497

Abstract

Specific cellulase production rates (SCPR) were compared with intracellular cyclic AMP (cAMP) levels in the thermophilic actinomycete, Thermomonospora curvata, during growth on several carbon sources in a chemically defined medium. SCPR and cAMP levels were 0.03 U (endoglucanase [EG] units) and 2 pmol per mg of dry cells, respectively, during exponential growth on glucose. These values increased to about 6 and 25, respectively, during growth on cellulose. Detectable EG production ceased when cAMP levels dropped below 10. Cellobiose (usually considered to be a cellulase inducer) caused a sharp decrease in cAMP levels and repressed EG production when added to cellulose-grown cultures. 2-deoxy-D-glucose, although nonmetabolizable in T. curvata, depressed cAMP to levels observed with glucose, but unlike glucose, the 2DG effect persisted until cells were washed and transferred to fresh medium. SCPR values and cAMP levels in cells grown in continuous culture under conditions of cellobiose limitation were markedly influenced by dilution rate (D). The maxima for both occurred at D = 0.085 (culture generation time of 11.8 h). When D was held constant and cellobiose concentration was increased over a 14-fold range to support higher steady state population levels, SCPR values decreased about fivefold, indicating that extracellular catabolite accumulation may be a factor in EG repression. The role of cAMP in the mechanism of this repression appears to be neither simple nor direct, since large changes (up to 200-fold) in SCPR accompany relatively small changes (10-fold) in cellular cAMP levels.

Full text

PDF
1050

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Botsford J. L. Cyclic nucleotides in procaryotes. Microbiol Rev. 1981 Dec;45(4):620–642. doi: 10.1128/mr.45.4.620-642.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Breuil C., Kushner D. J. Cellulase induction and the use of cellulose as a preferred growth substrate by Cellvibrio gilvus. Can J Microbiol. 1976 Dec;22(12):1776–1781. doi: 10.1139/m76-264. [DOI] [PubMed] [Google Scholar]
  3. Buettner M. J., Spitz E., Rickenberg H. V. Cyclic adenosine 3',5'-monophosphate in Escherichia coli. J Bacteriol. 1973 Jun;114(3):1068–1073. doi: 10.1128/jb.114.3.1068-1073.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Epstein W., Rothman-Denes L. B., Hesse J. Adenosine 3':5'-cyclic monophosphate as mediator of catabolite repression in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2300–2304. doi: 10.1073/pnas.72.6.2300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Forrest W. W., Walker D. J. The generation and utilization of energy during growth. Adv Microb Physiol. 1971;5:213–274. doi: 10.1016/s0065-2911(08)60408-7. [DOI] [PubMed] [Google Scholar]
  6. Fraser A. D., Yamazaki H. Effect of carbon sources on the rates of cyclic AMP synthesis, excretion, and degradation, and the ability to produce beta-galactosidase in Escherichia coli. Can J Biochem. 1979 Aug;57(8):1073–1079. doi: 10.1139/o79-136. [DOI] [PubMed] [Google Scholar]
  7. Ghose T. K., Sahai V. Production of cellulases by Trichoderma reesei QM 9414 in fed-batch and continuous-flow culture with cell recycle. Biotechnol Bioeng. 1979 Feb;21(2):283–296. doi: 10.1002/bit.260210213. [DOI] [PubMed] [Google Scholar]
  8. Gilman A. G., Murad F. Assay of cyclic nucleotides by receptor protein binding displacement. Methods Enzymol. 1974;38:49–61. doi: 10.1016/0076-6879(74)38010-x. [DOI] [PubMed] [Google Scholar]
  9. Groleau D., Forsberg C. W. Cellulolytic activity of the rumen bacterium Bacteroides succinogenes. Can J Microbiol. 1981 May;27(5):517–530. doi: 10.1139/m81-077. [DOI] [PubMed] [Google Scholar]
  10. Harman J. G., Botsford J. L. Synthesis of adenosine 3':5'-cyclic monophosphate in Salmonella typhimurium growing in continuous culture. J Gen Microbiol. 1979 Jan;110(1):243–246. doi: 10.1099/00221287-110-1-243. [DOI] [PubMed] [Google Scholar]
  11. Hylemon P. B., Phibbs P. V., Jr Evidence against the presence of cyclic AMP and related enzymes in selected strains of Bacteroides fragilis. Biochem Biophys Res Commun. 1974 Sep 9;60(1):88–95. doi: 10.1016/0006-291x(74)90176-4. [DOI] [PubMed] [Google Scholar]
  12. Joseph E., Danchin A., Ullmann A. Regulation of galactose operon expression: glucose effects and role of cyclic adenosine 3',5'-monophosphate. J Bacteriol. 1981 Apr;146(1):149–154. doi: 10.1128/jb.146.1.149-154.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Landwall P., Holme T. Removal of inhibitors of bacterial growth by dialysis culture. J Gen Microbiol. 1977 Dec;103(2):345–352. doi: 10.1099/00221287-103-2-345. [DOI] [PubMed] [Google Scholar]
  14. Lefebvre G., Raval G., Gay R. Variations du taux D'AMP cyclique et des activités spécifiques de l'adénylate cyclase et de l'AMP cyclique-phosphodiestérase pendant le cycle cellulaire d'un actinomycéte. Biochim Biophys Acta. 1980 Sep 17;632(1):26–34. doi: 10.1016/0304-4165(80)90246-9. [DOI] [PubMed] [Google Scholar]
  15. MAKMAN R. S., SUTHERLAND E. W. ADENOSINE 3',5'-PHOSPHATE IN ESCHERICHIA COLI. J Biol Chem. 1965 Mar;240:1309–1314. [PubMed] [Google Scholar]
  16. MANDELS M., REESE E. T. Induction of cellulase in Trichoderma viride as influenced by carbon sources and metals. J Bacteriol. 1957 Feb;73(2):269–278. doi: 10.1128/jb.73.2.269-278.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matin A., Grootjans A., Hogenhuis H. Influence of dilution rate on enzymes of intermediary metabolism in two freshwater bacteria grown in continuous culture. J Gen Microbiol. 1976 Jun;94(2):323–332. doi: 10.1099/00221287-94-2-323. [DOI] [PubMed] [Google Scholar]
  18. Matin A., Matin M. K. Cellular levels, excretion, and synthesis rates of cyclic AMP in Escherichia coli grown in continuous culture. J Bacteriol. 1982 Mar;149(3):801–807. doi: 10.1128/jb.149.3.801-807.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nisizawa T., Suzuki H., Nisizawa K. Catabolite repression of cellulase formation in Trichoderma viride. J Biochem. 1972 Jun;71(6):999–1007. doi: 10.1093/oxfordjournals.jbchem.a129872. [DOI] [PubMed] [Google Scholar]
  20. Pall M. L. Adenosine 3',5'-phosphate in fungi. Microbiol Rev. 1981 Sep;45(3):462–480. doi: 10.1128/mr.45.3.462-480.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Perlman R. L., Pastan I. Regulation of beta-galactosidase synthesis in Escherichia coli by cyclic adenosine 3',5'-monophosphate. J Biol Chem. 1968 Oct 25;243(20):5420–5427. [PubMed] [Google Scholar]
  22. Peterkofsky A. Cyclic nucleotides in bacteria. Adv Cyclic Nucleotide Res. 1976;7:1–48. [PubMed] [Google Scholar]
  23. Priest F. G. Typist: effect of glucose and cyclic nucleotides on the transcription of alpha-amylase mRHA in Bacillus subtilis. Biochem Biophys Res Commun. 1975 Apr 7;63(3):606–610. doi: 10.1016/s0006-291x(75)80427-x. [DOI] [PubMed] [Google Scholar]
  24. Ragan C. M., Vining L. C. Intracellular cyclic adenosine 3',5'-monophosphate levels and streptomycin production in cultures of Streptomyces griseus. Can J Microbiol. 1978 Aug;24(8):1012–1015. doi: 10.1139/m78-168. [DOI] [PubMed] [Google Scholar]
  25. Setlow B., Setlow P. Levels of cyclic GMP in dormant, germinated, and outgrowing spores and growing and sporulating cells of Bacillus megaterium. J Bacteriol. 1978 Oct;136(1):433–436. doi: 10.1128/jb.136.1.433-436.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stoppok W., Rapp P., Wagner F. Formation, Location, and Regulation of Endo-1,4-beta-Glucanases and beta-Glucosidases from Cellulomonas uda. Appl Environ Microbiol. 1982 Jul;44(1):44–53. doi: 10.1128/aem.44.1.44-53.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stutzenberger F. J. Cellulolytic activity of Thermomonospora curvata: nutritional requirments for cellulase production. Appl Microbiol. 1972 Jul;24(1):77–82. doi: 10.1128/am.24.1.77-82.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stutzenberger F. J. Cellulolytic activity of Thermomonospora curvata: optimal assay conditions, partial purification, and product of the cellulase. Appl Microbiol. 1972 Jul;24(1):83–90. doi: 10.1128/am.24.1.83-90.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thompson W. J., Brooker G., Appleman M. M. Assay of cyclic nucleotide phosphodiesterases with radioactive substrates. Methods Enzymol. 1974;38:205–212. doi: 10.1016/0076-6879(74)38033-0. [DOI] [PubMed] [Google Scholar]
  30. Ullmann A., Monod J. Cyclic AMP as an antagonist of catabolite repression in Escherichia coli. FEBS Lett. 1968 Nov;2(1):57–60. doi: 10.1016/0014-5793(68)80100-0. [DOI] [PubMed] [Google Scholar]
  31. Wanner B. L., Kodaira R., Neidhardt F. C. Regulation of lac operon expression: reappraisal of the theory of catabolite repression. J Bacteriol. 1978 Dec;136(3):947–954. doi: 10.1128/jb.136.3.947-954.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Westwood A. W., Higgins I. J. The effect of cyclic AMP on catabolite repression of Isocitrate lyase in Nocardia salmonicolor (NCIB9701). J Gen Microbiol. 1976 Nov;97(1):133–135. doi: 10.1099/00221287-97-1-133. [DOI] [PubMed] [Google Scholar]
  33. Wright L. F., Milne D. P., Knowles C. J. The regulatory effects of growth rate and cyclic AMP levels on carbon catabolism and respiration in Escherichia coli K-12. Biochim Biophys Acta. 1979 Feb 19;583(1):73–80. doi: 10.1016/0304-4165(79)90311-8. [DOI] [PubMed] [Google Scholar]
  34. Yeung K. H., Larsson G. C., Yamazaki H. Evidence against the involvement of adenosine 3',5'-cyclic monophosphate in glucose inhibition of beta-galactosidase induction in Bacillus megaterium. Can J Biochem. 1976 Oct;54(10):854–865. doi: 10.1139/o76-123. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES