1887

Microbiology Society logo

Volume 159, Issue Pt_2

Arginine deiminase inhibits surface attachment Free

Abstract

The oral cavity is host to a complex microbial community whose maintenance depends on an array of cell-to-cell interactions and communication networks, with little known regarding the nature of the signals or mechanisms by which they are sensed and transmitted. Determining the signals that control attachment, biofilm development and outgrowth of oral pathogens is fundamental to understanding pathogenic biofilm development. We have previously identified a secreted arginine deiminase (ADI) produced by that inhibited biofilm development of the commensal pathogen through downregulation of genes encoding the major () and minor () fimbriae, both of which are required for proper biofilm development. Here we report that this inhibitory effect is dependent on enzymic activity. We have successfully cloned, expressed and defined the conditions to ensure that ADI from is enzymically active. Along with the cloning of the wild-type allele, we have created a catalytic mutant (ADIC399S), in which the resulting protein is not able to catalyse the hydrolysis of -arginine to -citrulline. is insensitive to the ADIC399S catalytic mutant, demonstrating that enzymic activity is required for the effects of ADI on biofilm formation. Biofilm formation is absent under -arginine-deplete conditions, and can be recovered by the addition of the amino acid. Taken together, the results indicate that arginine is an important signal that directs biofilm formation by this anaerobe. Based on our findings, we postulate that ADI functions to reduce arginine levels and, by a yet to be identified mechanism, signals to alter biofilm development. ADI release from the streptococcal cell and its cross-genera effects are important findings in understanding the nature of inter-bacterial signalling and biofilm-mediated diseases of the oral cavity.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.062695-0
2013-02-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/2/275.html?itemId=/content/journal/micro/10.1099/mic.0.062695-0&mimeType=html&fmt=ahah

References

  1. Abdelal A. T.( 1979). Arginine catabolism by microorganisms. Annu Rev Microbiol 33:139–168 [View Article][PubMed]
     [Google Scholar]
  2. Amano A., Nakagawa I., Okahashi N., Hamada N.( 2004). Variations of Porphyromonas gingivalis fimbriae in relation to microbial pathogenesis. J Periodontal Res 39:136–142 [View Article][PubMed]
     [Google Scholar]
  3. Beenken K. E., Dunman P. M., McAleese F., Macapagal D., Murphy E., Projan S. J., Blevins J. S., Smeltzer M. S.( 2004). Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186:4665–4684 [View Article][PubMed]
     [Google Scholar]
  4. Bernier S. P., Ha D. G., Khan W., Merritt J. H., O’Toole G. A.( 2011). Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Res Microbiol 162:680–688 [View Article][PubMed]
     [Google Scholar]
  5. Brand H. S., Jörning G. G., Chamuleau R. A., Abraham-Inpijn L.( 1997). Effect of a protein-rich meal on urinary and salivary free amino acid concentrations in human subjects. Clin Chim Acta 264:37–47 [View Article][PubMed]
     [Google Scholar]
  6. Burne R. A., Marquis R. E.( 2000). Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol Lett 193:1–6 [View Article][PubMed]
     [Google Scholar]
  7. Burne R. A., Parsons D. T., Marquis R. E.( 1989). Cloning and expression in Escherichia coli of the genes of the arginine deiminase system of Streptococcus sanguis NCTC 10904. Infect Immun 57:3540–3548[PubMed]
     [Google Scholar]
  8. Caiazza N. C., O’Toole G. A.( 2004). SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186:4476–4485 [View Article][PubMed]
     [Google Scholar]
  9. Casiano-Colón A., Marquis R. E.( 1988). Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microbiol 54:1318–1324[PubMed]
     [Google Scholar]
  10. Chen Z., Potempa J., Polanowski A., Wikstrom M., Travis J.( 1992). Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J Biol Chem 267:18896–18901[PubMed]
     [Google Scholar]
  11. Choil J. I., Nakagawa T., Yamada S., Takazoe I., Okuda K.( 1990). Clinical, microbiological and immunological studies on recurrent periodontal disease. J Clin Periodontol 17:426–434 [View Article][PubMed]
     [Google Scholar]
  12. Christopher A. B., Arndt A., Cugini C., Davey M. E.( 2010). A streptococcal effector protein that inhibits Porphyromonas gingivalis biofilm development. Microbiology 156:3469–3477 [View Article][PubMed]
     [Google Scholar]
  13. Cole J. N., Ramirez R. D., Currie B. J., Cordwell S. J., Djordjevic S. P., Walker M. J.( 2005). Surface analyses and immune reactivities of major cell wall-associated proteins of group A streptococcus. Infect Immun 73:3137–3146 [View Article][PubMed]
     [Google Scholar]
  14. Cunin R., Glansdorff N., Piérard A., Stalon V.( 1986). Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev 50:314–352[PubMed]
     [Google Scholar]
  15. Das K., Butler G. H., Kwiatkowski V., Clark A. D. Jr, Yadav P., Arnold E.( 2004). Crystal structures of arginine deiminase with covalent reaction intermediates; implications for catalytic mechanism. Structure 12:657–667 [View Article][PubMed]
     [Google Scholar]
  16. Dzink J. L., Socransky S. S., Haffajee A. D.( 1988). The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol 15:316–323 [View Article][PubMed]
     [Google Scholar]
  17. Endo J., Otsuka M., Ohara E., Sato M., Nakamura R.( 1989). Cleavage action of a trypsin-like protease from Bacteroides gingivalis 381 on reduced egg-white lysozyme. Arch Oral Biol 34:911–916 [View Article][PubMed]
     [Google Scholar]
  18. Galkin A., Lu X., Dunaway-Mariano D., Herzberg O.( 2005). Crystal structures representing the Michaelis complex and the thiouronium reaction intermediate of Pseudomonas aeruginosa arginine deiminase. J Biol Chem 280:34080–34087 [View Article][PubMed]
     [Google Scholar]
  19. Grossi S. G., Zambon J. J., Ho A. W., Koch G., Dunford R. G., Machtei E. E., Norderyd O. M., Genco R. J.( 1994). Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 65:260–267 [View Article][PubMed]
     [Google Scholar]
  20. Hamada S., Amano A., Kimura S., Nakagawa I., Kawabata S., Morisaki I.( 1998). The importance of fimbriae in the virulence and ecology of some oral bacteria. Oral Microbiol Immunol 13:129–138 [View Article][PubMed]
     [Google Scholar]
  21. Higham S. M., Edgar W. M.( 1989). Human dental plaque pH, and the organic acid and free amino acid profiles in plaque fluid, after sucrose rinsing. Arch Oral Biol 34:329–334 [View Article][PubMed]
     [Google Scholar]
  22. Lamont R. J., Jenkinson H. F.( 1998). Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62:1244–1263[PubMed]
     [Google Scholar]
  23. Lamont R. J., Jenkinson H. F.( 2000). Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 15:341–349 [View Article][PubMed]
     [Google Scholar]
  24. Lewis J. P., Iyer D., Anaya-Bergman C.( 2009). Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155:3758–3774 [View Article][PubMed]
     [Google Scholar]
  25. Lu X., Galkin A., Herzberg O., Dunaway-Mariano D.( 2004). Arginine deiminase uses an active-site cysteine in nucleophilic catalysis of l-arginine hydrolysis. J Am Chem Soc 126:5374–5375 [View Article][PubMed]
     [Google Scholar]
  26. Lu X., Li L., Wu R., Feng X., Li Z., Yang H., Wang C., Guo H., Galkin A.& other authors ( 2006). Kinetic analysis of Pseudomonas aeruginosa arginine deiminase mutants and alternate substrates provides insight into structural determinants of function. Biochemistry 45:1162–1172 [View Article][PubMed]
     [Google Scholar]
  27. Masuda K., Tomita K., Hayashi H., Yoshioka M., Hinode D., Nakamura R.( 2001). Consumption of peptide-derived arginine by a periodontopathogenic bacterium, Porphyromonas gingivalis. Anaerobe 7:209–217 [View Article]
     [Google Scholar]
  28. Masuda K., Yoshioka M., Hinode D., Nakamura R.( 2002). Purification and characterization of arginine carboxypeptidase produced by Porphyromonas gingivalis. Infect Immun 70:1807–1815 [View Article][PubMed]
     [Google Scholar]
  29. McGraw W. T., Potempa J., Farley D., Travis J.( 1999). Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 67:3248–3256[PubMed]
     [Google Scholar]
  30. Milner P., Batten J. E., Curtis M. A.( 1996). Development of a simple chemically defined medium for Porphyromonas gingivalis: requirement for α-ketoglutarate. FEMS Microbiol Lett 140:125–130[PubMed]
     [Google Scholar]
  31. Moore W. E., Moore L. H., Ranney R. R., Smibert R. M., Burmeister J. A., Schenkein H. A.( 1991). The microflora of periodontal sites showing active destructive progression. J Clin Periodontol 18:729–739 [View Article][PubMed]
     [Google Scholar]
  32. Müsken M., Di Fiore S., Dötsch A., Fischer R., Häussler S.( 2010). Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology 156:431–441 [View Article][PubMed]
     [Google Scholar]
  33. Nascimento M. M., Gordan V. V., Garvan C. W., Browngardt C. M., Burne R. A.( 2009). Correlations of oral bacterial arginine and urea catabolism with caries experience. Oral Microbiol Immunol 24:89–95 [View Article][PubMed]
     [Google Scholar]
  34. Navarre W. W., Schneewind O.( 1999). Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229[PubMed]
     [Google Scholar]
  35. Nelson K. E., Fleischmann R. D., DeBoy R. T., Paulsen I. T., Fouts D. E., Eisen J. A., Daugherty S. C., Dodson R. J., Durkin A. S.& other authors ( 2003). Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J Bacteriol 185:5591–5601 [View Article][PubMed]
     [Google Scholar]
  36. Ni Y., Li Z., Sun Z., Zheng P., Liu Y., Zhu L., Schwaneberg U.( 2009). Expression of arginine deiminase from Pseudomonas plecoglossicida CGMCC2039 in Escherichia coli and its anti-tumor activity. Curr Microbiol 58:593–598 [View Article][PubMed]
     [Google Scholar]
  37. Pike R., McGraw W., Potempa J., Travis J.( 1994). Lysine- and arginine-specific proteinases from Porphyromonas gingivalis. Isolation, characterization, and evidence for the existence of complexes with hemagglutinins. J Biol Chem 269:406–411[PubMed]
     [Google Scholar]
  38. Rahman M., Laverack P. D., Clarke P. H.( 1980). The catabolism of arginine by Pseudomonas aeruginosa. J Gen Microbiol 116:371–380[PubMed]
     [Google Scholar]
  39. Rodríguez S. B., Stitt B. L., Ash D. E.( 2009). Expression of peptidylarginine deiminase from Porphyromonas gingivalis in Escherichia coli: enzyme purification and characterization. Arch Biochem Biophys 488:14–22 [View Article][PubMed]
     [Google Scholar]
  40. Seddon S. V., Shah H. N., Hardie J. M., Robinson J. P.( 1988). Chemically defined and minimal media for Bacteroides gingivalis. Curr Microbiol 17:147–149 [View Article]
     [Google Scholar]
  41. Sosroseno W.( 2004). The effect of l-arginine on Porphyromonas gingivalis-induced phagocytosis of a murine macrophage-like RAW264.7 cell line. Immunopharmacol Immunotoxicol 26:309–313 [View Article][PubMed]
     [Google Scholar]
  42. Syrjänen S. M., Alakuijala L., Alakuijala P., Markkanen S. O., Markkanen H.( 1990). Free amino acid levels in oral fluids of normal subjects and patients with periodontal disease. Arch Oral Biol 35:189–193 [View Article][PubMed]
     [Google Scholar]
  43. Takahashi N., Sato T., Yamada T.( 2000). Metabolic pathways for cytotoxic end product formation from glutamate- and aspartate-containing peptides by Porphyromonas gingivalis. J Bacteriol 182:4704–4710 [View Article][PubMed]
     [Google Scholar]
  44. Tang-Larsen J., Claesson R., Edlund M. B., Carlsson J.( 1995). Competition for peptides and amino acids among periodontal bacteria. J Periodontal Res 30:390–395 [View Article][PubMed]
     [Google Scholar]
  45. Téllez N., Aguilera N., Quiñónez B., Silva E., González L. E., Hernández L.( 2008). Arginine and glutamate levels in the gingival crevicular fluid from patients with chronic periodontitis. Braz Dent J 19:318–322 [View Article][PubMed]
     [Google Scholar]
  46. Van Wuyckhuyse B. C., Perinpanayagam H. E., Bevacqua D., Raubertas R. F., Billings R. J., Bowen W. H., Tabak L. A.( 1995). Association of free arginine and lysine concentrations in human parotid saliva with caries experience. J Dent Res 74:686–690 [View Article][PubMed]
     [Google Scholar]
  47. Wang C., Xu D., Zhang L., Xie D., Guo H.( 2007). Molecular dynamics and density functional studies of substrate binding and catalysis of arginine deiminase. J Phys Chem B 111:3267–3273 [View Article][PubMed]
     [Google Scholar]
  48. Wei Y., Zhou H., Sun Y., He Y., Luo Y.( 2007). Insight into the catalytic mechanism of arginine deiminase: functional studies on the crucial sites. Proteins 66:740–750 [View Article][PubMed]
     [Google Scholar]
  49. Wu G., Morris S. M. Jr( 1998). Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17[PubMed]
     [Google Scholar]
  50. Wu J., Xie H.( 2010). Role of arginine deiminase of Streptococcus cristatus in Porphyromonas gingivalis colonization. Antimicrob Agents Chemother 54:4694–4698 [View Article][PubMed]
     [Google Scholar]
  51. Xie H., Lin X., Wang B. Y., Wu J., Lamont R. J.( 2007). Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153:3228–3234 [View Article][PubMed]
     [Google Scholar]
  52. Xu Y., Labedan B., Glansdorff N.( 2007). Surprising arginine biosynthesis: a reappraisal of the enzymology and evolution of the pathway in microorganisms. Microbiol Mol Biol Rev 71:36–47 [View Article][PubMed]
     [Google Scholar]
  53. Zhu Y., Weiss E. C., Otto M., Fey P. D., Smeltzer M. S., Somerville G. A.( 2007). Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis. Infect Immun 75:4219–4226 [View Article][PubMed]
     [Google Scholar]
  54. Zhu T., Lou Q., Wu Y., Hu J., Yu F., Qu D.( 2010). Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile. BMC Microbiol 10:287 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.062695-0
Loading
Arginine deiminase inhibits Porphyromonas gingivalis surface attachment
Microbiology 159, 275 (2013); https://doi.org/10.1099/mic.0.062695-0
/content/journal/micro/10.1099/mic.0.062695-0
/content/journal/micro/10.1099/mic.0.062695-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error