Abstract
The properties of a teichoic acid degrading enzyme (teichoicase) isolated from Bacillus subtilis Marburg are described. The purified enzyme showed phosphodiesterase activity but not phosphomonoesterase activity, and it had an absolute substrate specificity for alpha-glucosylated glycerol teichoic acid, the endogenous cell wall teichoic acid of the enzyme-producing cell. The substrate was degraded by an exo-mechanism yielding the monomer alpha-D-glucose 1 leads to 2 (sn)glycero-3-phosphate. When B. subtilis Marburg was grown in a rich medium, enzyme activity was detected in extracts from sporulating cells. Teichoicase activity was present in a mutant blocked in stage II of the sporulation process but was absent in a mutant blocked in stage O. It was concluded that teichoicase is active on enzyme-producing cells since the reaction product could be detected in their culture supernatant. Attempts to demonstrate analogous enzyme activity in other Bacillus strains failed. The enzyme could be used for the rapid detection of alpha-glucosylated glycerol teichoic acid and for the controlled alteration of native bacterial cell surfaces exhibiting the appropriate structure.
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- AMES B. N., DUBIN D. T. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J Biol Chem. 1960 Mar;235:769–775. [PubMed] [Google Scholar]
- ARMSTRONG J. J., BADDILEY J., BUCHANAN J. G. Further studies on the teichoic acid from Bacillus subtilis walls. Biochem J. 1961 Aug;80:254–261. doi: 10.1042/bj0800254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anderson A. J., Green R. S., Sturman A. J., Archibald A. R. Cell wall assembly in Bacillus subtilis: location of wall material incorporated during pulsed release of phosphate limitation, its accessibility to bacteriophages and concanavalin A, and its susceptibility to turnover. J Bacteriol. 1978 Dec;136(3):886–899. doi: 10.1128/jb.136.3.886-899.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BURGER M. M., GLASER L. THE SYNTHESIS OF TEICHOIC ACIDS. I. POLYGLYCEROPHOSPHATE. J Biol Chem. 1964 Oct;239:3168–3177. [PubMed] [Google Scholar]
- Beachey E. H., Chiang T. M., Ofek I., Kang A. H. Interaction of lipoteichoic acid of group A streptococci with human platelets. Infect Immun. 1977 May;16(2):649–654. doi: 10.1128/iai.16.2.649-654.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beveridge T. J., Murray R. G. Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol. 1980 Feb;141(2):876–887. doi: 10.1128/jb.141.2.876-887.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birdsell D. C., Doyle R. J., Morgenstern M. Organization of teichoic acid in the cell wall of Bacillus subtilis. J Bacteriol. 1975 Feb;121(2):726–734. doi: 10.1128/jb.121.2.726-734.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burger M. M., Glaser L. The synthesis of teichoic acids. V. Polyglucosylglycerol phosphate and polygalactosylglycerol phosphate. J Biol Chem. 1966 Jan 25;241(2):494–506. [PubMed] [Google Scholar]
- Burger M. M. Teichoic acids: antigenic determinants, chain separation, and their location in the cell wall. Proc Natl Acad Sci U S A. 1966 Sep;56(3):910–917. doi: 10.1073/pnas.56.3.910. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chatterjee A. N., Mirelman D., Singer H. J., Park J. T. Properties of a novel pleiotropic bacteriophage-resistant mutant of Staphylococcus aureus H. J Bacteriol. 1969 Nov;100(2):846–853. doi: 10.1128/jb.100.2.846-853.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dancer B. N. Requirement for peptidoglycan synthesis during sporulation of Bacillus subtilis. J Bacteriol. 1979 Dec;140(3):786–797. doi: 10.1128/jb.140.3.786-797.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Boer W. R., Kruyssen F. J., Wouters J. T. The structure of teichoic acid from Bacillus subtilis var, niger WM as determined by C nuclear-magnetic-resonance spectroscopy. Eur J Biochem. 1976 Feb 2;62(1):1–6. doi: 10.1111/j.1432-1033.1976.tb10090.x. [DOI] [PubMed] [Google Scholar]
- Doyle R. J., Birdsell D. C., Young F. E. Isolation of the teichoic acid of Bacillus subtilis 168 by affinity chromatography. Prep Biochem. 1973;3(1):13–18. doi: 10.1080/00327487308061485. [DOI] [PubMed] [Google Scholar]
- Doyle R. J., McDannel M. L., Helman J. R., Streips U. N. Distribution of teichoic acid in the cell wall of Bacillus subtilis. J Bacteriol. 1975 Apr;122(1):152–158. doi: 10.1128/jb.122.1.152-158.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischer W., Koch H. U., Rösel P., Fiedler F., Schmuck L. Structural requirements of lipoteichoic acid carrier for recognition by the poly(ribitol phosphate) polymerase from Staphylococcus aureus H. A study of various lipoteichoic acids, derivatives, and related compounds. J Biol Chem. 1980 May 25;255(10):4550–4556. [PubMed] [Google Scholar]
- Forsberg C. W., Wyrick P. B., Ward J. B., Rogers H. J. Effect of phosphate limitation on the morphology and wall composition of Bacillus licheniformis and its phosphoglucomutase-deficient mutants. J Bacteriol. 1973 Feb;113(2):969–984. doi: 10.1128/jb.113.2.969-984.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ganfield M. C., Pieringer R. A. The biosynthesis of nascent membrane lipoteichoic acid of Streptococcus faecium (S. faecalis ATCC 9790) from phosphatidylkojibiosyl diacylglycerol and phosphatidylglycerol. J Biol Chem. 1980 Jun 10;255(11):5164–5169. [PubMed] [Google Scholar]
- Ghosh A., Ghosh B. K. Immunoelectron microscopic localization of penicillinase in Bacillus licheniformis. J Bacteriol. 1979 Mar;137(3):1374–1385. doi: 10.1128/jb.137.3.1374-1385.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glenn A. R., Mandelstam J. Sporulation in Bacillus subtilis 168. Comparison of alkaline phosphatase from sporulating and vegetative cells. Biochem J. 1971 Jun;123(2):129–138. doi: 10.1042/bj1230129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grant W. D. Cell wall teichoic acid as a reserve phosphate source in Bacillus subtilis. J Bacteriol. 1979 Jan;137(1):35–43. doi: 10.1128/jb.137.1.35-43.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartmann R., Bock-Hennig S. B., Schwarz U. Murein hydrolases in the envelope of Escherichia coli. Properties in situ and solubilization from the envelope. Eur J Biochem. 1974 Jan 3;41(1):203–208. doi: 10.1111/j.1432-1033.1974.tb03261.x. [DOI] [PubMed] [Google Scholar]
- Heptinstall S., Archibald A. R., Baddiley J. Teichoic acids and membrane function in bacteria. Nature. 1970 Feb 7;225(5232):519–521. doi: 10.1038/225519a0. [DOI] [PubMed] [Google Scholar]
- Hughes R. C., Tanner P. J., Stokes E. Cell-wall thickening in Bacillus subtilis. Comparison of thickened and normal walls. Biochem J. 1970 Nov;120(1):159–170. doi: 10.1042/bj1200159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes R. C., Tanner P. J. The action of dilute alkali on some bacterial cell walls. Biochem Biophys Res Commun. 1968 Oct 10;33(1):22–28. doi: 10.1016/0006-291x(68)90248-9. [DOI] [PubMed] [Google Scholar]
- Hughes R. C., Thurman P. F., Stokes E. Estimates of the porosity of Bacillus licheniformis and Bacillus subtilis cell walls. Z Immunitatsforsch Exp Klin Immunol. 1975 Jul;149(2-4):126–135. [PubMed] [Google Scholar]
- Iwata S., Tochikubo K., Kato K., Hirata T., Kotani S., Yagi K. Microorganism capable of decomposing N-acetylglucosaminyl ribitol teichoic acid of Staphylococcus aureus. Jpn J Microbiol. 1976 Apr;20(2):123–129. doi: 10.1111/j.1348-0421.1976.tb00918.x. [DOI] [PubMed] [Google Scholar]
- Johnstone K., Simion F. A., Ellar D. J. Teichoic acid and lipid metabolism during sporulation of Bacillus megaterium KM. Biochem J. 1982 Feb 15;202(2):459–467. doi: 10.1042/bj2020459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koch H. U., Fischer W. Acyldiglucosyldiacylglycerol-containing lipoteichoic acid with a poly(3-O-galabiosyl-2-O-galactosyl-sn-glycero-1-phosphate) chain from Streptococcus lactis Kiel 42172. Biochemistry. 1978 Nov 28;17(24):5275–5281. doi: 10.1021/bi00617a030. [DOI] [PubMed] [Google Scholar]
- Kusser W., Fiedler F. Purification, Mr-value and subunit structure of a teichoic acid hydrolase from Bacillus subtilis. FEBS Lett. 1982 Nov 22;149(1):67–70. doi: 10.1016/0014-5793(82)81073-9. [DOI] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Le Hégarat J. C., Anagnostopoulos C. Purification, subunit structure and properties of two repressible phosphohydrolases of Bacillus subtilis. Eur J Biochem. 1973 Nov 15;39(2):525–539. doi: 10.1111/j.1432-1033.1973.tb03151.x. [DOI] [PubMed] [Google Scholar]
- Nelson D. L., Kornberg A. Biochemical studies of bacterial sporulation and germination. XIX. Phosphate metabolism during sporulation. J Biol Chem. 1970 Mar 10;245(5):1137–1145. [PubMed] [Google Scholar]
- Nielsen J. B., Caulfield M. P., Lampen J. O. Lipoprotein nature of Bacillus licheniformis membrane penicillinase. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3511–3515. doi: 10.1073/pnas.78.6.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Priest F. G. Extracellular enzyme synthesis in the genus Bacillus. Bacteriol Rev. 1977 Sep;41(3):711–753. doi: 10.1128/br.41.3.711-753.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SHOCKMAN G. D., SLADE H. D. THE CELLULAR LOCATION OF THE STREPTOCOCCAL GROUP D ANTIGEN. J Gen Microbiol. 1964 Dec;37:297–305. doi: 10.1099/00221287-37-3-297. [DOI] [PubMed] [Google Scholar]
- STROMINGER J. L., GHUYSEN J. M. ON THE LINKAGE BETWEEN TEICHOIC ACID AND THE GLYCOPEPTIDE IN THE CELL WALL OF STAPHYLOCOCCUS AUREUS. Biochem Biophys Res Commun. 1963 Aug 14;12:418–424. doi: 10.1016/0006-291x(63)90117-7. [DOI] [PubMed] [Google Scholar]
- Scherrer R., Gerhardt P. Molecular sieving by the Bacillus megaterium cell wall and protoplast. J Bacteriol. 1971 Sep;107(3):718–735. doi: 10.1128/jb.107.3.718-735.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schleifer K. H., Kandler O. Zur chemischen Zusammensetzung der Zellwand der Streptokokken. I. Die Aminosäuresequenz des Mureins von Str. thermophilus und Str. faecalis. Arch Mikrobiol. 1967 Jul 6;57(4):335–364. [PubMed] [Google Scholar]
- Schneider J. E., Kennedy E. P. A novel phosphodiesterase from Aspergillus niger and its application to the study of membrane-derived oligosaccharides and other glycerol-containing biopolymers. J Biol Chem. 1978 Nov 10;253(21):7738–7743. [PubMed] [Google Scholar]
- Singh R. P., Setlow P. Regulation of phosphoglycerate phosphomutase in developing forespores and dormant and germinated spores of Bacillus megaterium by the level of free manganous ions. J Bacteriol. 1979 Sep;139(3):889–898. doi: 10.1128/jb.139.3.889-898.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sterlini J. M., Mandelstam J. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance. Biochem J. 1969 Jun;113(1):29–37. doi: 10.1042/bj1130029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vasantha N., Freese E. The role of manganese in growth and sporulation of Bacillus subtilis. J Gen Microbiol. 1979 Jun;112(2):329–336. doi: 10.1099/00221287-112-2-329. [DOI] [PubMed] [Google Scholar]
- Wise E. M., Jr, Glickman R. S., Teimer E. Teichoic acid hydrolase activity in soil bacteria (Bacillus subtilis-sporulation-phosphodiesterase-polyamines-concanavalin A). Proc Natl Acad Sci U S A. 1972 Jan;69(1):233–237. doi: 10.1073/pnas.69.1.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamada M., Hirose A., Matsuhashi M. Association of lack of cell wall teichuronic acid with formation of cell packets of Micrococcus lysodeikticus (luteus) mutants. J Bacteriol. 1975 Aug;123(2):678–686. doi: 10.1128/jb.123.2.678-686.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young F. E. Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Proc Natl Acad Sci U S A. 1967 Dec;58(6):2377–2384. doi: 10.1073/pnas.58.6.2377. [DOI] [PMC free article] [PubMed] [Google Scholar]