Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1996 Jun;64(6):2240–2245. doi: 10.1128/iai.64.6.2240-2245.1996

Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae.

J N Weiser 1, Z Markiewicz 1, E I Tuomanen 1, J H Wani 1
PMCID: PMC174062  PMID: 8675333

Abstract

Streptococcus pneumoniae undergoes phase variation in colony morphology, which has been implicated as a factor in the pathogenesis of pneumococcal disease. Phenotypic differences between opaque and transparent colony forms correlate with differences in rates of autolysis. This study examined whether differences in autolysis are caused by differences in expression of the major amidase, LytA, or the structure of its peptidoglycan substrate. No significant difference was detected by high-pressure liquid chromatography analysis of stem peptides released after treatment of purified peptidoglycan with amidase. Differences in the rate of digestion of purified cell walls, furthermore, did not correlate with susceptibility to autolysis. Lower levels of autolysis in opaque variants, however, was associated with decreased levels of immunodetectable LytA on colony immunoblots and Western blots (immunoblots). Diminished cell-surface-associated LytA in opaque variants was also demonstrated by whole-cell inhibition enzyme-linked immunosorbent assay. Since transparent variants have been shown both to colonize the nasopharynx more efficiently in an animal model and to express more surface-exposed LytA, it was determined whether LytA contributes to colonization in a neonatal rat model of pneumococcal carriage. Defined mutants in the lytA gene were used to show that there was no significant contribution by LytA to nasopharyngeal colonization in this model. Although the expression of LytA was shown to undergo phase variation in association with colony morphology, lytA mutants are still capable of phenotypic variation in colony morphology, which suggests that other factors are responsible for intrastrain differences which affect colonization.

Full Text

The Full Text of this article is available as a PDF (513.6 KB).

Selected References

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

  1. Berry A. M., Lock R. A., Hansman D., Paton J. C. Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun. 1989 Aug;57(8):2324–2330. doi: 10.1128/iai.57.8.2324-2330.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blake M. S., Blake C. M., Apicella M. A., Mandrell R. E. Gonococcal opacity: lectin-like interactions between Opa proteins and lipooligosaccharide. Infect Immun. 1995 Apr;63(4):1434–1439. doi: 10.1128/iai.63.4.1434-1439.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Briese T., Hakenbeck R. Interaction of the pneumococcal amidase with lipoteichoic acid and choline. Eur J Biochem. 1985 Jan 15;146(2):417–427. doi: 10.1111/j.1432-1033.1985.tb08668.x. [DOI] [PubMed] [Google Scholar]
  4. Cundell D. R., Gerard N. P., Gerard C., Idanpaan-Heikkila I., Tuomanen E. I. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature. 1995 Oct 5;377(6548):435–438. doi: 10.1038/377435a0. [DOI] [PubMed] [Google Scholar]
  5. Cundell D. R., Weiser J. N., Shen J., Young A., Tuomanen E. I. Relationship between colonial morphology and adherence of Streptococcus pneumoniae. Infect Immun. 1995 Mar;63(3):757–761. doi: 10.1128/iai.63.3.757-761.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dougherty T. J. Involvement of a change in penicillin target and peptidoglycan structure in low-level resistance to beta-lactam antibiotics in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1985 Jul;28(1):90–95. doi: 10.1128/aac.28.1.90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Díaz E., García E., Ascaso C., Méndez E., López R., García J. L. Subcellular localization of the major pneumococcal autolysin: a peculiar mechanism of secretion in Escherichia coli. J Biol Chem. 1989 Jan 15;264(2):1238–1244. [PubMed] [Google Scholar]
  8. Díaz E., López R., García J. L. Role of the major pneumococcal autolysin in the atypical response of a clinical isolate of Streptococcus pneumoniae. J Bacteriol. 1992 Sep;174(17):5508–5515. doi: 10.1128/jb.174.17.5508-5515.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garcia-Bustos J. F., Chait B. T., Tomasz A. Structure of the peptide network of pneumococcal peptidoglycan. J Biol Chem. 1987 Nov 15;262(32):15400–15405. [PubMed] [Google Scholar]
  10. Garcia-Bustos J. F., Tomasz A. Teichoic acid-containing muropeptides from Streptococcus pneumoniae as substrates for the pneumococcal autolysin. J Bacteriol. 1987 Feb;169(2):447–453. doi: 10.1128/jb.169.2.447-453.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. García J. L., García E., López R. Overproduction and rapid purification of the amidase of Streptococcus pneumoniae. Arch Microbiol. 1987;149(1):52–56. doi: 10.1007/BF00423136. [DOI] [PubMed] [Google Scholar]
  12. Geelen S., Bhattacharyya C., Tuomanen E. The cell wall mediates pneumococcal attachment to and cytopathology in human endothelial cells. Infect Immun. 1993 Apr;61(4):1538–1543. doi: 10.1128/iai.61.4.1538-1543.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. LACKS S., HOTCHKISS R. D. A study of the genetic material determining an enzyme in Pneumococcus. Biochim Biophys Acta. 1960 Apr 22;39:508–518. doi: 10.1016/0006-3002(60)90205-5. [DOI] [PubMed] [Google Scholar]
  14. Markiewicz Z., Tomasz A. Protein-bound choline is released from the pneumococcal autolytic enzyme during adsorption of the enzyme to cell wall particles. J Bacteriol. 1990 May;172(5):2241–2244. doi: 10.1128/jb.172.5.2241-2244.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Saluja S. K., Weiser J. N. The genetic basis of colony opacity in Streptococcus pneumoniae: evidence for the effect of box elements on the frequency of phenotypic variation. Mol Microbiol. 1995 Apr;16(2):215–227. doi: 10.1111/j.1365-2958.1995.tb02294.x. [DOI] [PubMed] [Google Scholar]
  16. Tomasz A., Moreillon P., Pozzi G. Insertional inactivation of the major autolysin gene of Streptococcus pneumoniae. J Bacteriol. 1988 Dec;170(12):5931–5934. doi: 10.1128/jb.170.12.5931-5934.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Weiser J. N., Austrian R., Sreenivasan P. K., Masure H. R. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun. 1994 Jun;62(6):2582–2589. doi: 10.1128/iai.62.6.2582-2589.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES