Definition of a Fundamental Repeating Unit in Streptococcal Glucosyltransferase Glucan-binding Regions and Related Sequences

Abstract

The C-termini of the glucosyltransferases (Gtfs) of oral streptococci are responsible for glucan binding. These glucan-binding domains (GBDs) are composed of a series of repeated sequences that have been classified into four different classes (A-D) by virtue of sequence similarity and which, by inference, have been suggested to be of functional importance. In contrast, we propose that repeat sequences evolve in response to selection for an increase in the number of copies of a particular domain through multiple duplication events occurring at different times. According to this hypothesis, repeats should possess various degrees of similarity, especially if only key residues are of functional importance. Analysis of the GBDs of the Gtfs indicated that a common fundamental repeat, designated the "YG" repeat, could be discerned within the "A", "B", "C", and "D" repeats. Similar elements were also conserved in the ligand-binding repeats of the Clostridium difficile toxins and the lysins and the PspA protein of Streptococcus pneumoniae, suggesting that similar selective pressures had also been imposed on these sequences. Analysis of the "YG" repeats present in the GtfJ and GtfK of Streptococcus salivarius indicated that some of the "YG" repeats in the GBDs of these proteins had arisen as a result of duplication events involving a series of three sequential "YG" repeats.

Keywords

Streptococcus Glucosyltransferase Glucan-binding Evolution.

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References

Abo H. , Matsumura T. , Kodama T. , Ohta H. , Fukui K. , Kato K. , et al. (1991). Peptide sequences for sucrose splitting and glucan binding within Streptococcus sobrinus glucosyltransferase (water-insoluble glucan synthetase). J Bacteriol 173:989-996.

Banas,JA Russell RRB , Ferretti JJ (1990). Sequence analysis of the gene for the glucan-binding protein of Streptococcus mutans Ingbritt. Infect Immun 58:667-673.

Dove CH , Wang S. -Z, Price SB , Phelps CJ , Lyerly DM , Wilkins TD , et al. (1990). Molecular characterization of the Clostridium difficile Toxin A gene. Infect Immun 58:480-488.

Ferretti JJ , Gilpin ML , Russell RRB (1987). Nucleotide sequence of a glucosyltransferase gene from Streptococcus sobrinus MFe28. J Bacteriol 169:4271-4278.

Garcia P. , Garcia JL , Garcia E. , Lopez R. (1986). Nucleotide sequence and expression of the pneumococcal autolysin gene from its own promoter in Escherichia coli. Gene 43:265-272.

Giffard PM , Jacques NA (1992). The glucosyltransferases of oral streptococci . Aust Microbiologist 13:A189.

Giffard PM , Simpson CL , Milward CP , Jacques NA (1991). Molecular characterization of a cluster of at least two glucosyltransferase genes in Streptococcus salivarius ATCC 25975 . J Gen Microbiol 137:2577-2593.

Giffard PM , O'Connor DM , Milward CP , Simpson CL , Jacques NA (1992). Comparison of the GtfK of Streptococcus salivarius with other glucosyltransferases (abstract). J Dent Res 72(Spec Iss):733.

Giffard PM , Allen DM , Milward CP , Simpson CL , Jacques NA (1993). Sequence of the gtfK of Streptococcus salivarius ATCC 25975 and evolution of the gtfS genes of oral streptococci. J Gen Microbiol 139:1511-1522.

10.

Gilmore KS , Russell Rrb , Ferretti JJ (1990). Analysis of the Streptococcus downei gtfS gene, which specifies a glucosyltransferase that synthesizes soluble glucans. Infect Immun 58:2452-2458.

11.

Higgins DG , Bleasby AJ , Fuchs R. (1992). CLUSTALV: improved software for multiple sequence alignment. Computer Appl Biosciences (CABIOS) 8:189-191.

12.

Honda O. , Kato C. , Kuramitsu HK (1990). Nucleotide sequence of the Streptococcus mutans gtfD gene. J Gen Microbiol 136:2099-2105.

13.

Kobayashi S. , Koga K. , Hayashida O. , Nakano Y. , Hasegawa Y. (1989). Glucan-binding domain of a glucosyltransferase from Streptococcus sobrinus: isolation of a 55-kilodalton peptide from a trypsin digest of glucosyltransferase prebound to insoluble glucan. Infect Immun 57:2210-2213.

14.

Mooser G. , Wong C. ( 1988). Isolation of a glucan-binding domain of glucosyltransferase(1,6-α-glucan synthase) from Streptococcus sobrinus. Infect Immun 56:880-884.

15.

Nakano YJ , Kuramitsu HK (1992). Mechanism of Streptococcus mutans glucosyltransferases: Hybrid-enzyme analysis. J Bacteriol 174:5639-5646.

16.

Shiroza T. , Ueda S. , Kuramitsu HK (1987). Sequence analysis of the gtfB gene from Streptococcus mutans GS-5. J Bacteriol 169:4263-4270.

17.

Smith DJ , Taubman MA , Holmberg CF , Eastcott J. , King WF , Ali-Salaam P. (1993). Antigenicity and immunogenicity of a synthetic peptide derived from a glucan-binding domain of mutans streptococcal glucosyltransferase . Infect Immun 61:2899-2905.

18.

Ueda S. , Shiroza T. , Kuramitsu HK (1988). Sequence analysis of the gtfC gene from Streptococcus mutans GS-5. Gene 69:101-109.

19.

von Eichel-Streiber C. , Sauerborn M. , Kuramitsu HK (1992). Evidence for a modular structure of the homologous repetitive C-terminal carbohydrate-binding sites of Clostridium difficile toxins and Streptococcus mutans glucosyltransferases. J Bacteriol 174:6707-6710.

20.

Wong C. , Hefta SA , Paxton RJ , Shively JE , Mooser G. (1990). Size and subdomain architecture of the glucan-binding domain of sucrose:3-α-D-glucosyltransferase from Streptococcus sobrinus . Infect Immun 58:2165-2170.

21.

Wren BW ( 1991). A family of clostridial and streptococcal ligand-binding proteins with conserved C-terminal repeat sequences. Molec Microbiol 5:797-803.

22.

Wren BW , Russell RRB , Tabaqchali S. (1991). Antigenic cross-reactivity and functional inhibition by antibodies to Clostridium difficile Toxin A, Streptococcus mutans glucan-binding protein, and a synthetic peptide. Infect Immun 59:3151-3155.

23.

Yother J. , Briles DE (1992). Structural properties and evolutionary relationships of PspA, a surface protein of Streptococcus pneumoniae, as revealed by sequence analysis. J Bacteriol 174:601-609.