Chapter 22 : Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap22-1.gif /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap22-2.gif


Interactions between oral streptococci have developed because of ecological pressures within the oral environment. The high abundance of oral streptococci makes it very likely that they have evolved close relationships manifested in diverse interspecies interactions. Interspecies interactions in the oral biofilm can be defined by the purpose and nature of the interactions. Although there are many potential interactions between oral streptococci and other members of the oral biofilm community as well as the host, this chapter specifically focuses on streptococcus-streptococcus interactions. By promoting genetic exchange, the interspecies interaction, although not beneficial for the lysed bacterial species, is important in the context of evolution. A counteroffensive strategy was recently identified for , another oral streptococcal species and competitor of . Surprisingly, is able to utilize the lactic acid produced by cariogenic species, such as , to generate hydrogen peroxide, leading to growth inhibition of the lactic acid producer. Expanding research into multispecies models is desirable and would most likely reveal interesting synergistic behavior of oral streptococci. The close relationship of the oral streptococci enables the reconstruction of biochemical networks from already-existing metabolic functions identified in other streptococci. The spatial-temporal developmental patterns of oral streptococci in the biofilm, including the molecular mechanisms, are characterized. The oral biofilm is easily accessible, and the variety of genetic manipulation options for oral streptococci allows for experimental verification of in silico predictions.

Citation: Kreth J, Merritt J, Qi F, Dong X, Shi W. 2011. Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions, p 331-343. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch22
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Interspecies interactions among , and Shown is the production of lactic acid, mutacin, CSP (involved in stimulation of mutacin gene expression), challisin, and hydrogen peroxide, important in the antagonistic relationship between these oral streptococci. Lactic acid inhibits the growth of acid-sensitive streptococci. uses lactic acid for the production of growth-inhibiting concentrations of HO via the lactate oxidase (Lox). Conversely, HO is also generated by and by the pyruvate oxidase (Pox). HO inhibits growth of and are sensitive to the mutacins produced by utilizes challisin to interfere with the mutacin production by reducing the levels of the stimulating compound CSP. In a synergistic manner, and are able to degrade mucin, a glycoprotein present in saliva. is more efficient in binding to the saliva-coated tooth via the adhesin Hsa than is For further details, see the text. Modified after reference .

Citation: Kreth J, Merritt J, Qi F, Dong X, Shi W. 2011. Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions, p 331-343. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Alignment of the upstream promoter regions of the pyruvate oxidase-encoding genes of (S.g.), (S.s.), and (S.m.). ATG indicates the start of the coding sequence for pyruvate oxidase.

Citation: Kreth J, Merritt J, Qi F, Dong X, Shi W. 2011. Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions, p 331-343. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Aas, J. A.,, B. J. Paster,, L. N. Stokes,, I. Olsen, and, F. E. Dewhirst. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43: 57215732.
2. Becker, M. R.,, B. J. Paster,, E. J. Leys,, M. L. Moeschberger,, S. G. Kenyon,, J. L. Galvin,, S. K. Boches,, F. E. Dewhirst, and, A. L. Griffen. 2002. Molecular analysis of bacterial species associated with childhood caries. J. Clin. Microbiol. 40: 10011009.
3. Berkowitz, R. J. 2003. Causes, treatment and prevention of early childhood caries: a microbiologic perspective. J. Can. Dent. Assoc. 69: 304307.
4. Caufield, P. W.,, A. P. Dasanayake,, Y. Li,, Y. Pan,, J. Hsu, and, J. M. Hardin. 2000. Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect. Immun. 68: 40184023.
5. Caufield, P. W.,, Y. Li,, A. Dasanayake, and, D. Saxena. 2007. Diversity of lactobacilli in the oral cavities of young women with dental caries. Caries Res. 41: 28.
6. Chang, A.,, M. Scheer,, A. Grote,, I. Schomburg, and, D. Schomburg. 2009. BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res. 37: D588D592.
7. Cvitkovitch, D. G. 2001. Genetic competence and transformation in oral streptococci. Crit. Rev. Oral Biol. Med. 12: 217243.
8. Cvitkovitch, D. G.,, Y. Li, and, R. P. Ellen. 2003. Quorum sensing and biofilm formation in streptococcal infections. J. Clin. Investig. 112: 16261632.
9. Deng, H.,, Y. Ding,, M. D. Fu,, X. R. Xiao,, J. Liu, and, T. Zhou. 2004. Purification and characterization of sanguicin—a bacteriocin produced by Streptococcus sanguis. Sichuan Da Xue Xue Bao Yi Xue Ban 35: 555558.
10. Diaz, P. I.,, N. I. Chalmers,, A. H. Rickard,, C. Kong,, C. L. Milburn,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72: 28372848.
11. Eckert, R.,, J. He,, D. K. Yarbrough,, F. Qi,, M. H. Anderson, and, W. Shi. 2006. Targeted killing of Streptococcus mutans by a pheromone-guided “smart” antimicrobial peptide. Antimicrob. Agents Chemother. 50: 36513657.
12. Egland, P. G.,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2004. Interspecies communication in Streptococcus gordonii- Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. USA 101: 1691716922.
13. Facklam, R. 2002. What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin. Microbiol. Rev. 15: 613630.
14. Fejerskov, O. 2004. Changing paradigms in concepts on dental caries: consequences for oral health care. Caries Res. 38: 182191.
15. Fujimura, S.,, and T. Nakamura. 1979. Sanguicin, a bacteriocin of oral Streptococcus sanguis. Antimicrob. Agents Chemother. 16: 262265.
16. Hamada, S.,, and H. D. Slade. 1980. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev. 44: 331384.
17. He, J.,, M. H. Anderson,, W. Shi, and, R. Eckert. 2009. Design and activity of a ‘dualtargeted’ antimicrobial peptide. Int. J. Antimicrob. Agents 33: 532537.
18. He, J.,, D. K. Yarbrough,, J. Kreth,, M. H. Anderson,, W. Shi, and, R. Eckert. 2010. Systematic approach to optimizing specifically targeted antimicrobial peptides against Streptococcus mutans. Antimicrob. Agents Chemother. 54: 21432151.
19. Heng, N. C.,, J. R. Tagg, and, G. R. Tompkins. 2007. Competence-dependent bacteriocin production by Streptococcus gordonii DL1 (Challis). J. Bacteriol. 189: 14681472.
20. Hense, B. A.,, C. Kuttler,, J. Muller,, M. Rothballer,, A. Hartmann, and, J. U. Kreft. 2007. Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5: 230239.
21. Herzberg, M. C. 1996. Platelet-streptococcal interactions in endocarditis. Crit. Rev. Oral Biol. Med. 7: 222236.
22. Herzberg, M. C.,, M. W. Meyer,, A. Kilic, and, L. Tao. 1997. Host-pathogen interactions in bacterial endocarditis: streptococcal virulence in the host. Adv. Dent. Res. 11: 6974.
23. Jenkinson, H. F.,, and R. J. Lamont. 1997. Streptococcal adhesion and colonization. Crit. Rev. Oral Biol. Med. 8: 175200.
24. Kolenbrander, P. E.,, R. J. Palmer, Jr.,, A. H. Rickard,, N. S. Jakubovics,, N. I. Chalmers, and, P. I. Diaz. 2006. Bacterial interactions and successions during plaque development. Periodontol. 2000 42: 4779.
25. Kornfeld, R.,, and S. Kornfeld. 1976. Comparative aspects of glycoprotein structure. Annu. Rev. Biochem. 45: 217237.
26. Kreth, J.,, J. Merritt,, W. Shi, and, F. Qi. 2005. Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol. Microbiol. 57: 392404.
27. Kreth, J.,, J. Merritt,, W. Shi, and, F. Qi. 2005. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 187: 71937203.
28. Kreth, J.,, J. Merritt,, L. Zhu,, W. Shi, and, F. Qi. 2006. Cell density- and ComE-dependent expression of a group of mutacin and mutacinlike genes in Streptococcus mutans. FEMS Microbiol. Lett. 265: 1117.
29. Kreth, J.,, Y. Zhang, and, M. C. Herzberg. 2008. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J. Bacteriol. 190: 46324640.
30. Kuramitsu, H. K.,, X. He,, R. Lux,, M. H. Anderson, and, W. Shi. 2007. Interspecies interactions within oral microbial communities. Microbiol. Mol. Biol. Rev. 71: 653670.
31. Lemos, J. A.,, and R. A. Burne. 2008. A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology 154: 32473255.
32. Li, Y.,, Y. Ge,, D. Saxena, and, P. W. Caufield. 2007. Genetic profiling of the oral microbiota associated with severe earlychildhood caries. J. Clin. Microbiol. 45: 8187.
33. Li, Y. H.,, P. C. Lau,, J. H. Lee,, R. P. Ellen, and, D. G. Cvitkovitch. 2001. Natural genetic transformation of Streptococcus mutans growing in biofilms. J. Bacteriol. 183: 897908.
34. Liljemark, W. F.,, and C. Bloomquist. 1996. Human oral microbial ecology and dental caries and periodontal diseases. Crit. Rev. Oral Biol. Med. 7: 180198.
35. Liljemark, W. F.,, C. G. Bloomquist, and, G. R. Germaine. 1981. Effect of bacterial aggregation on the adherence of oral streptococci to hydroxyapatite. Infect. Immun. 31: 935941.
36. Liljemark, W. F.,, C. G. Bloomquist, and, J. C. Ofstehage. 1979. Aggregation and adherence of Streptococcus sanguis: role of human salivary immunoglobulin A. Infect. Immun. 26: 11041110.
37. Loesche, W. J. 1986. Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50: 353380.
38. Marquis, R. E. 1995. Oxygen metabolism, oxidative stress and acid-base physiology of dental plaque biofilms. J. Ind. Microbiol. 15: 198207.
39. Matta, M.,, M. Gousseff,, F. Monsel,, C. Poyart,, B. Diebold,, I. Podglajen, and, J. L. Mainardi. 2008. First case of Streptococcus oligofermentans endocarditis based on sodA gene sequences determined after amplification directly from valvular samples. J. Clin. Microbiol. 47: 855856.
40. McLean, J. S.,, O. N. Ona, and, P. D. Majors. 2008. Correlated biofilm imaging, transport and metabolism measurements via combined nuclear magnetic resonance and confocal microscopy. ISME J. 2: 121131.
41. Mikx, F. H.,, J. S. van der Hoeven,, K. G. Konig,, A. J. Plasschaert, and, B. Guggenheim. 1972. Establishment of defined microbial ecosystems in germ-free rats. I. The effect of the interactions of Streptococcus mutans or Streptococcus sanguis with Veillonella alcalescens on plaque formation and caries activity. Caries Res. 6: 211223.
42. Nobbs, A. H.,, Y. Zhang,, A. Khammanivong, and, M. C. Herzberg. 2007. Streptococcus gordonii Hsa environmentally constrains competitive binding by Streptococcus sanguinis to salivacoated hydroxyapatite. J. Bacteriol. 189: 31063114.
43. Ogata, H.,, S. Goto,, K. Sato,, W. Fujibuchi,, H. Bono, and, M. Kanehisa. 1999. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27: 2934.
44. Oppegard, C.,, P. Rogne,, L. Emanuelsen,, P. E. Kristiansen,, G. Fimland, and, J. Nissen-Meyer. 2007. The two-peptide class II bacteriocins: structure, production, and mode of action. J. Mol. Microbiol. Biotechnol. 13: 210219.
45. Palmer, R. J., Jr.,, P. I. Diaz, and, P. E. Kolenbrander. 2006. Rapid succession within the Veillonella population of a developing human oral biofilm in situ. J. Bacteriol. 188: 41174124.
46. Petersen, F. C.,, and A. A. Scheie. 2000. Genetic transformation in Streptococcus mutans requires a peptide secretion-like apparatus. Oral Microbiol. Immunol. 15: 329334.
47. Qi, F.,, P. Chen, and, P. W. Caufield. 2001. The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl. Environ. Microbiol. 67: 1521.
48. Qi, F.,, P. Chen, and, P. W. Caufield. 2000. Purification and biochemical characterization of mutacin I from the group I strain of Streptococcus mutans, CH43, and genetic analysis of mutacin I biosynthesis genes. Appl. Environ. Microbiol. 66: 32213229.
49. Qi, F.,, J. Kreth,, C. M. Levesque,, O. Kay,, R. W. Mair,, W. Shi,, D. G. Cvitkovitch, and, S. D. Goodman. 2005. Peptide pheromone induced cell death of Streptococcus mutans. FEMS Microbiol. Lett. 251: 321326.
50. Raes, J.,, and P. Bork. 2008. Molecular ecosystems biology: towards an understanding of community function. Nat. Rev. Microbiol. 6: 693699.
51. Rosan, B.,, and R. J. Lamont. 2000. Dental plaque formation. Microbes Infect. 2: 15991607.
52. Schlegel, R.,, and H. D. Slade. 1972. Bacteriocin production by transformable group H streptococci. J. Bacteriol. 112: 824829.
53. Tong, H.,, W. Chen,, J. Merritt,, F. Qi,, W. Shi, and, X. Dong. 2007. Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H 2O 2: a possible counteroffensive strategy for interspecies competition. Mol. Microbiol. 63: 872880.
54. Tong, H.,, W. Chen,, W. Shi,, F. Qi, and, X. Dong. 2008. SO-LAAO, a novel L-amino acid oxidase that enables Streptococcus oligofermentans to outcompete Streptococcus mutans by generating H 2O 2 from peptone. J. Bacteriol. 190: 47164721.
55. Tong, H.,, X. Gao, and, X. Dong. 2003. Streptococcus oligofermentans sp. nov., a novel oral isolate from caries-free humans. Int. J. Syst. Evol. Microbiol. 53: 11011104.
56. Van der Hoeven, J. S.,, and P. J. Camp. 1991. Synergistic degradation of mucin by Streptococcus oralis and Streptococcus sanguis in mixed chemostat cultures. J. Dent. Res. 70: 10411044.
57. van der Ploeg, J. R. 2005. Regulation of bacteriocin production in Streptococcus mutans by the quorumsensing system required for development of genetic competence. J. Bacteriol. 187: 39803989.
58. Wang, B. Y.,, and H. K. Kuramitsu. 2005. Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii. Appl. Environ. Microbiol. 71: 354362.
59. Yeats, C.,, R. D. Finn, and, A. Bateman. 2002. The PASTA domain: a beta-lactam-binding domain. Trends Biochem. Sci. 27: 438.
60. Zhu, L.,, and J. Kreth. 2010. Role of Streptococcus mutans eukaryotic-type serine/threonine protein kinase in interspecies interactions with Streptococcus sanguinis. Arch. Oral Biol. 55: 385390.


Generic image for table

Distribution of functional groups involved in oral streptococcal interspecies interactions

Citation: Kreth J, Merritt J, Qi F, Dong X, Shi W. 2011. Antagonistic, Synergistic, and Counteroffensive Strategies for Streptococcal Interspecies Interactions, p 331-343. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch22

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error