1887

Abstract

JB1 does not normally lyse, but stationary phase lysis can be induced by including 2-deoxyglucose (2DG) in the growth medium. Isolates deficient in glucose/2DG phosphotransferase activity (PTS) also lysed when 2DG was present (Lys) and this result indicated that 2DG phosphorylation via the PTS was not an obligate requirement for 2DG-induced lysis. Cells and cell walls from 2DG-grown cultures lysed faster when proteinase K was added, but glucose-grown cultures and cell walls were not affected. A lipoteichoic acid (LTA) extract (aqueous phase from hot phenol treatment) from glucose-grown cells inhibited the lysis of 2DG-grown cultures, but a similar extract prepared from 2DG-grown cells was without effect. Thin-layer chromatography and differential staining indicated that wild-type and Lys PTS cells incorporated 2DG into LTA, but lysis-resistant cultures (Lys PTS and Lys PTS) did not. LTA from lysis-resistant (Lys PTS and Lys PTS) cells grown with glucose and 2DG also prevented 2DG-dependent lysis of the wild-type. LTA could not inhibit degradation of cell walls isolated from 2DG-grown cultures, but LTA inhibited the lysis of () cells that were exposed to supernatants from 2DG-grown cultures. Group D streptococci (including . ) normally have an α-1,2 linked glucose disaccharide (kojibiose) in their LTA, but kojibiose cannot be synthesized from 2DG. This observation suggested that the kojibiose moiety of LTA was involved in autolysin inactivation. Wild-type had ATP- as well as PEP-dependent mechanisms of 2DG phosphorylation and one lysis-resistant phenotype (Lys PTS) had reduced levels of both activities. However, the Lys PTS phenotype was still able to phosphorylate 2DG via ATP and PEP and this result indicated that some other step of 2DG incorporation into LTA was being inhibited. Based on these results, growth in the presence of 2DG appears to prevent synthesis of normal LTA, which is involved in the regulation of autolytic enzymes.

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1999-10-01
2024-04-19
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References

  1. Bailey, R. W. (1958). The reaction of pentoses with anthrone. Biochem J 68, 669-672. [Google Scholar]
  2. Biely, P., Krátky, Z., Kovarı́k, J. & Bauer, S. (1971). Effect of 2-deoxyglucose on cell wall formation in Saccharomyces cerevisiae and its relation to cell growth inhibition. J Bacteriol 107, 121-129. [Google Scholar]
  3. Blackman, S. A., Smith, T. J. & Foster, S. J. (1988). The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144, 73-82. [Google Scholar]
  4. Buist, G., Venema, G. & Kok, J. (1988). Autolysis of Lactococcuslactis is influenced by proteolysis. J Bacteriol 180, 5947-5953. [Google Scholar]
  5. Cleveland, R. F., Wicken, A. J., Daneo-Moore, L. & Shockman, G. D. (1976a). Inhibition of wall autolysis in Streptococcus faecalis by lipoteichoic acid and lipids. J Bacteriol 126, 192-197. [Google Scholar]
  6. Cleveland, R. F., Wicken, A. J., Daneo-Moore, L. & Shockman, G. D. (1976b). Effect of lipoteichoic acid and lipids on lysis of intact cells of Streptococcus faecalis. J Bacteriol 127, 1582-1584. [Google Scholar]
  7. Cook, G. M. & Russell, J. B. (1994). Alternative strategies of 2-deoxyglucose resistance and low affinity glucose transport in the ruminal bacteria, Streptococcus bovis and Selenomonas ruminantium. FEMS Microbiol Lett 123, 207-212.[CrossRef] [Google Scholar]
  8. Cook, G. M., Ye, J. J., Russell, J. B. & Saier, M. H. (1995). Properties of two sugar phosphate phosphatases from Streptococcus bovis and their involvement in inducer expulsion. J Bacteriol 177, 7007-7009. [Google Scholar]
  9. Diederick Meyer, P. & Wouters, J. T. M. (1987). Lipoteichoic acid from Bacillus subtilis subsp. Niger WM, isolation and effects on cell wall autolysis and turnover. J Bacteriol 169, 973-980. [Google Scholar]
  10. Fischer, W. (1988). Physiology of lipoteichoic acids in bacteria. Adv Microb Physiol 29, 235-247. [Google Scholar]
  11. Fischer, W. (1994). Lipoteichoic acids and lipoglycans. In New Comprehensive Biochemistry, pp. 199-214. Edited by J.-M. Ghuysen & R. Hakenback. Amsterdam: Elsevier.
  12. Fischer, W. & Koch, H. U. (1981). Alanine ester substitution and its effect on the biological properties of lipoteichoic acids. In Chemistry and Biological Activities of Bacterial Surface Amphiphiles, pp. 181-194. Edited by G. D. Shockman & A. J. Wicken. New York: Academic Press.
  13. Fischer, W., Rösel, P. & Koch, H. U. (1981). Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcusaureus. J Bacteriol 146, 467-475. [Google Scholar]
  14. Foster, S. J. (1992). Analysis of the autolysins of Bacillus subtilis 168 during vegetative growth and differentiation by using renaturing polyacrylaminde gel electrophoresis. J Bacteriol 174, 464-470. [Google Scholar]
  15. Foster, S. J. (1995). Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177, 5723-5725. [Google Scholar]
  16. Hogg, S. D., Whiley, R. A. & De Soet, J. J. (1997). Occurrence of lipoteichoic acid in oral streptococci. Int J Syst Bacteriol 47, 62-66.[CrossRef] [Google Scholar]
  17. Höltje, J.-V. & Tomasz, A. (1975). Lipoteichoic acid: a specific inhibitor of autolysin activity in Pneumococcus. Proc Natl Acad Sci USA 72, 1690-1694.[CrossRef] [Google Scholar]
  18. Hungate, R. E., Dougherty, R. W., Bryant, M. P. & Cello, R. M. (1952). Microbiological and physiological changes associated with acute indigestion in sheep. Cornell Vet 42, 423-449. [Google Scholar]
  19. Jolliffee, L. K., Doyle, R. J. & Streips, U. N. (1980). Extracellular proteases modify cell wall turnover in Bacillus subtilis. J Bacteriol 141, 1199-1208. [Google Scholar]
  20. Kariyama, R. & Shockman, G. D. (1992). Extracellular and cellular distribution of muramindase-2 and muramidase-1 of Enterococcus hirae ATCC 9790. J Bacteriol 174, 3236-3241. [Google Scholar]
  21. Kessler, R. E., Wicken, A. J. & Shockman, G. D. (1983). Increased carbohydrate substitution of lipoteichoic acid during inhibition of protein synthesis. J Bacteriol 155, 138-144. [Google Scholar]
  22. Kessler, R. E., Duke, J. & Goldstein, I. J. (1984). Interaction of anti-kojibiose antibody with the lipoteichoic acids from Streptococcusfaecalis and Streptococcus faecium. Infect Immun 46, 279-281. [Google Scholar]
  23. Krebs, G. L., Leng, R. A. & Nolan, J. V. (1989). Microbial biomass and production rates in the rumen of faunated and fauna-free sheep on low protein fibrous feeds with or without nitrogen supplementation. In The Roles of Protozoa and Fungi in Ruminant Digestion, pp. 295. Edited by J. V. Nolan, R. A. Leng & D. I. Demeyer. Armidale, Australia: Penambul Books.
  24. Kupferwasser, I., Darius, H., Mueller, A. M., Mohr-Kahaly, S., Westermeier, T., Olert, H., Erbel, R. & Meyer, J. (1988). Clinical and morphological characteristics in Streptococcus bovis endocarditis: A comparison with other causative microorganisms in 177 cases. Heart 80, 276-280. [Google Scholar]
  25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef] [Google Scholar]
  26. Martin, S. A. & Russell, J. B. (1986). Phosphoenolpyruvate-dependent phosphorylation of hexoses by rumen bacteria: Evidence for the phosphotransferase system of transport. Appl Environ Microbiol 52, 1348-1352. [Google Scholar]
  27. Nolan, J. V. (1975). Quantitative models of nitrogen metabolism in sheep. In Digestion and Metabolism in the Ruminant, pp. 416-431. Edited by I. W. MacDonald & A. C. I. Warner. Armidale, Australia: University of New England Publishing Unit.
  28. Pooley, H. M. & Karamate, H. (1984). Genetic analysis of autolysin deficient and flagellaless mutants of Bacillus subtilis. J Bacteriol 160, 1123-1129. [Google Scholar]
  29. Prasad, C. & Freese, E. (1974). Cell lysis of Bacillus subtilis caused by intracellular accumulation of glucose-1-phosphate. J Bacteriol 118, 1111-1122. [Google Scholar]
  30. Rogers, H. J., Taylor, C., Rayter, S. & Ward, J. B. (1984). Purification and properties of autolytic endo-β-N-acetylglucosamidase and the N-acetylmuramyl-l-alanine amidase from Bacillussubtilis strain 168. J Gen Microbiol 130, 2395-2402. [Google Scholar]
  31. Romano, A. H., Trifoneand, J. D. & Brustolon, M. (1979). Distribution of the phosphoenolpyruvate:glucose phophotransferase system in fermentative bacteria. J Bacteriol 139, 93-97. [Google Scholar]
  32. Russell, J. B. (1990). Low affinity, high capacity system of glucose transport in the ruminal bacterium Streptococcus bovis: evidence for a mechanism of facilitated diffusion. Appl Environ Microbiol 56, 3304–3307. [Google Scholar]
  33. Russell, J. B. & Wells, J. E. (1997). The ability of 2-deoxyglucose to promote the lysis of Streptococcus bovis JB1 via a mechanism involving cell wall stability. Curr Microbiol 35, 299-304.[CrossRef] [Google Scholar]
  34. Shockman, G. D. & Barrett, J. F. (1983). Structure, function and assembly of cell walls of gram-positive bacteria. Annu Rev Microbiol 37, 501-527.[CrossRef] [Google Scholar]
  35. Shockman, G. D., Thompson, J. S. & Conover, M. J. (1967). The autolytic enzyme system of Streptococcus faecalis. II. Partial characterization of the autolysin and its substrate. Biochemistry 6, 1054-1064.[CrossRef] [Google Scholar]
  36. Sijtsma, L., Wouters, J. T. M. & Hellingwerf, K. J. (1990). Isolation and characterization of lipoteichoic acid, a cell envelope component involved in preventing phage adsorption, from Lactococcus lactis subsp. cremoris SK110. J Bacteriol 172, 7126-7130. [Google Scholar]
  37. Thompson, J. (1987). Regulation of sugar transport and metabolism in lactic acid bacteria. FEMS Microbiol Rev 46, 221-231.[CrossRef] [Google Scholar]
  38. Wecke, J., Madela, K. & Fischer, W. (1997). The absence of d-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143, 2952-2960. [Google Scholar]
  39. Wells, J. E. & Russell, J. B. (1996a). The effect of growth and starvation on the lysis of the ruminal cellulolytic bacterium Fibrobacter succinogenes. Appl Environ Microbiol 62, 1342-1346. [Google Scholar]
  40. Wells, J. E. & Russell, J. B. (1996b). Why do many ruminal bacteria die and lyse so quickly? J Dairy Sci 79, 1487-1495.[CrossRef] [Google Scholar]
  41. Wicken, A. J. & Baddiley, J. (1963). Structure of intracellular teichoic acids from group D streptococci. Biochem J 87, 54-62. [Google Scholar]
  42. Wicken, A. J. & Knox, K. W. (1975). Lipoteichoic acids: a new class of bacterial antigen. Science 187, 1161-1167.[CrossRef] [Google Scholar]
  43. Zarkin, B. A., Lillemoe, K. D., Cameron, J. L., Effron, P. N., Magnuson, T. H. & Pitt, H. A. (1990). The triad of Streptococcusbovis bacteremia, colonic pathology and liver disease. Ann Surg 211, 786-792.[CrossRef] [Google Scholar]
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