1887

Abstract

In the oral biofilm, the ‘mitis’ streptococci are among the first group of organisms to colonize the tooth surface. Their proliferation is thought to be an important factor required for antagonizing the growth of cariogenic species such as . In this study, we used a three-species mixed culture to demonstrate that another ubiquitous early colonizing species, can greatly affect the outcome of the competition between a pair of antagonists such as and . Transcriptome analysis further revealed that responds differentially to its friend () and foe (). In the mixed culture with , all but one of the sugar uptake and metabolic genes were downregulated, while genes for alternative energy source utilization and HO tolerance were upregulated, resulting in a slower but persistent growth. In contrast, when cultured with , grew equally well or better than in monoculture and exhibited relatively few changes within its transcriptome. When was introduced into the mixed culture of and , it rescued the growth inhibition of . In this three-species environment, increased the expression of genes required for the uptake and metabolism of minor sugars, while genes required for oxidative stress tolerance were downregulated. We conclude that the major factors that affect the competition between and are carbohydrate utilization and HO resistance. The presence of in the tri-species culture mitigates these two major factors and allows to proliferate, despite the presence of .

Funding
This study was supported by the:
  • NIH (Award R15 DE019940)
  • Centers of Biomedical Research Excellence
  • COBRE (Award P20-RR018741-05)
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2011-09-01
2021-05-06
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References

  1. Aas J. A., Paster B. J., Stokes L. N., Olsen I., Dewhirst F. E. ( 2005). Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732 [CrossRef][PubMed]
    [Google Scholar]
  2. Aas J. A., Griffen A. L., Dardis S. R., Lee A. M., Olsen I., Dewhirst F. E., Leys E. J., Paster B. J. ( 2008). Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407–1417 [CrossRef][PubMed]
    [Google Scholar]
  3. Abranches J., Candella M. M., Wen Z. T., Baker H. V., Burne R. A. ( 2006). Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans . J Bacteriol 188:3748–3756 [CrossRef][PubMed]
    [Google Scholar]
  4. Ajdić D., Pham V. T. ( 2007). Global transcriptional analysis of Streptococcus mutans sugar transporters using microarrays. J Bacteriol 189:5049–5059 [CrossRef][PubMed]
    [Google Scholar]
  5. Ajdić D., McShan W. M., McLaughlin R. E., Savić G., Chang J., Carson M. B., Primeaux C., Tian R., Kenton S. et al. ( 2002). Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 99:14434–14439 [CrossRef][PubMed]
    [Google Scholar]
  6. Antranikian G., Gottschalk G. ( 1989). Phosphorylation of citrate lyase ligase in Clostridium sphenoides and regulation of anaerobic citrate metabolism in other bacteria. Biochimie 71:1029–1037 [CrossRef][PubMed]
    [Google Scholar]
  7. Bakaletz L. O. ( 2004). Developing animal models for polymicrobial diseases. Nat Rev Microbiol 2:552–568 [CrossRef][PubMed]
    [Google Scholar]
  8. Baldeck J. D., Marquis R. E. ( 2008). Targets for hydrogen-peroxide-induced damage to suspension and biofilm cells of Streptococcus mutans . Can J Microbiol 54:868–875 [CrossRef][PubMed]
    [Google Scholar]
  9. Becker M. R., Paster B. J., Leys E. J., Moeschberger M. L., Kenyon S. G., Galvin J. L., Boches S. K., Dewhirst F. E., Griffen A. L. ( 2002). Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009 [CrossRef][PubMed]
    [Google Scholar]
  10. Brogden K. A., Guthmiller J. M., Taylor C. E. ( 2005). Human polymicrobial infections. Lancet 365:253–255[PubMed] [CrossRef]
    [Google Scholar]
  11. Caufield P. W., Cutter G. R., Dasanayake A. P. ( 1993). Initial acquisition of mutans streptococci by infants: evidence for a discrete window of infectivity. J Dent Res 72:37–45 [CrossRef][PubMed]
    [Google Scholar]
  12. Caufield P. W., Dasanayake A. P., Li Y., Pan Y., Hsu J., Hardin J. M. ( 2000). Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 68:4018–4023 [CrossRef][PubMed]
    [Google Scholar]
  13. Chalmers N. I., Palmer R. J. Jr, Cisar J. O., Kolenbrander P. E. ( 2008). Characterization of a Streptococcus sp.–Veillonella sp. community micromanipulated from dental plaque. J Bacteriol 190:8145–8154 [CrossRef][PubMed]
    [Google Scholar]
  14. Dewhirst F. E., Chen T., Izard J., Paster B. J., Tanner A. C., Yu W. H., Lakshmanan A., Wade W. G. ( 2010). The human oral microbiome. J Bacteriol 192:5002–5017 [CrossRef][PubMed]
    [Google Scholar]
  15. Diaz P. I., Chalmers N. I., Rickard A. H., Kong C., Milburn C. L., Palmer R. J. Jr, Kolenbrander P. E. ( 2006). Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol 72:2837–2848 [CrossRef][PubMed]
    [Google Scholar]
  16. Ganesan B., Stuart M. R., Weimer B. C. ( 2007). Carbohydrate starvation causes a metabolically active but nonculturable state in Lactococcus lactis . Appl Environ Microbiol 73:2498–2512 [CrossRef][PubMed]
    [Google Scholar]
  17. García-Quintáns N., Magni C., de Mendoza D., López P. ( 1998). The citrate transport system of Lactococcus lactis subsp. lactis biovar diacetylactis is induced by acid stress. Appl Environ Microbiol 64:850–857[PubMed]
    [Google Scholar]
  18. Hale J. D., Heng N. C., Jack R. W., Tagg J. R. ( 2005). Identification of nlmTE, the locus encoding the ABC transport system required for export of nonlantibiotic mutacins in Streptococcus mutans . J Bacteriol 187:5036–5039 [CrossRef][PubMed]
    [Google Scholar]
  19. Hughes C. V., Kolenbrander P. E., Andersen R. N., Moore L. V. ( 1988). Coaggregation properties of human oral Veillonella spp.: relationship to colonization site and oral ecology. Appl Environ Microbiol 54:1957–1963[PubMed]
    [Google Scholar]
  20. Hughes C. V., Andersen R. N., Kolenbrander P. E. ( 1992). Characterization of Veillonella atypica PK1910 adhesin-mediated coaggregation with oral Streptococcus spp. Infect Immun 60:1178–1186[PubMed]
    [Google Scholar]
  21. Keijser B. J., Zaura E., Huse S. M., van der Vossen J. M., Schuren F. H., Montijn R. C., ten Cate J. M., Crielaard W. ( 2008). Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87:1016–1020 [CrossRef][PubMed]
    [Google Scholar]
  22. Kolenbrander P. E., Palmer R. J. Jr, Rickard A. H., Jakubovics N. S., Chalmers N. I., Diaz P. I. ( 2006). Bacterial interactions and successions during plaque development. Periodontol 2000 42:47–79 [CrossRef][PubMed]
    [Google Scholar]
  23. Kolenbrander P. E., Palmer R. J. Jr, Periasamy S., Jakubovics N. S. ( 2010). Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8:471–480 [CrossRef][PubMed]
    [Google Scholar]
  24. Korithoski B., Krastel K., Cvitkovitch D. G. ( 2005). Transport and metabolism of citrate by Streptococcus mutans . J Bacteriol 187:4451–4456 [CrossRef][PubMed]
    [Google Scholar]
  25. Krastel K., Senadheera D. B., Mair R., Downey J. S., Goodman S. D., Cvitkovitch D. G. ( 2010). Characterization of a glutamate transporter operon, glnQHMP, in Streptococcus mutans and its role in acid tolerance. J Bacteriol 192:984–993 [CrossRef][PubMed]
    [Google Scholar]
  26. Kreth J., Merritt J., Shi W., Qi F. ( 2005a). Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol Microbiol 57:392–404 [CrossRef][PubMed]
    [Google Scholar]
  27. Kreth J., Merritt J., Shi W., Qi F. ( 2005b). Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187:7193–7203 [CrossRef][PubMed]
    [Google Scholar]
  28. Kreth J., Merritt J., Zhu L., Shi W., Qi F. ( 2006). Cell density- and ComE-dependent expression of a group of mutacin and mutacin-like genes in Streptococcus mutans . FEMS Microbiol Lett 265:11–17 [CrossRef][PubMed]
    [Google Scholar]
  29. Lemme A., Sztajer H., Wagner-Döbler I. ( 2010). Characterization of mleR, a positive regulator of malolactic fermentation and part of the acid tolerance response inStreptococcus mutans . BMC Microbiol 10:58 [CrossRef][PubMed]
    [Google Scholar]
  30. Loesche W. J. ( 1986). Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353–380[PubMed]
    [Google Scholar]
  31. Luppens S. B., Kara D., Bandounas L., Jonker M. J., Wittink F. R., Bruning O., Breit T. M., Ten Cate J. M., Crielaard W. ( 2008). Effect of Veillonella parvula on the antimicrobial resistance and gene expression of Streptococcus mutans grown in a dual-species biofilm. Oral Microbiol Immunol 23:183–189 [CrossRef][PubMed]
    [Google Scholar]
  32. Mager D. L., Ximenez-Fyvie L. A., Haffajee A. D., Socransky S. S. ( 2003). Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol 30:644–654 [CrossRef][PubMed]
    [Google Scholar]
  33. Marsh P. D. ( 1994). Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 8:263–271[PubMed]
    [Google Scholar]
  34. Marsh P. D. ( 1999). Microbiologic aspects of dental plaque and dental caries. Dent Clin North Am 43:599–614, v–vi[PubMed]
    [Google Scholar]
  35. Marsh P. D. ( 2006). Dental diseases – are these examples of ecological catastrophes?. Int J Dent Hyg 4:Suppl. 13–10, discussion 50–52 [CrossRef][PubMed]
    [Google Scholar]
  36. Mikx F. H., Van der Hoeven J. S. ( 1975). Symbiosis of Streptococcus mutans and Veillonella alcalescens in mixed continuous cultures. Arch Oral Biol 20:407–410 [CrossRef][PubMed]
    [Google Scholar]
  37. Mikx F. H., van der Hoeven J. S., König K. G., Plasschaert A. J., Guggenheim B. ( 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 6:211–223 [CrossRef][PubMed]
    [Google Scholar]
  38. Mikx F. H., van der Hoeven J. S., Plasschaert A. J., König K. G. ( 1976). Establishment and symbiosis of Actinomyces viscosus, Streptococcus sanguis and Streptococcus mutans in germ-free Osborne-Mendel rats. Caries Res 10:123–132 [CrossRef][PubMed]
    [Google Scholar]
  39. Nyvad B., Kilian M. ( 1990). Microflora associated with experimental root surface caries in humans. Infect Immun 58:1628–1633[PubMed]
    [Google Scholar]
  40. Palmer R. J. Jr, Diaz P. I., Kolenbrander P. E. ( 2006). Rapid succession within the Veillonella population of a developing human oral biofilm in situ. J Bacteriol 188:4117–4124 [CrossRef][PubMed]
    [Google Scholar]
  41. Paster B. J., Boches S. K., Galvin J. L., Ericson R. E., Lau C. N., Levanos V. A., Sahasrabudhe A., Dewhirst F. E. ( 2001). Bacterial diversity in human subgingival plaque. J Bacteriol 183:3770–3783 [CrossRef][PubMed]
    [Google Scholar]
  42. Paster B. J., Olsen I., Aas J. A., Dewhirst F. E. ( 2006). The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 42:80–87 [CrossRef][PubMed]
    [Google Scholar]
  43. Perry J. A., Jones M. B., Peterson S. N., Cvitkovitch D. G., Lévesque C. M. ( 2009). Peptide alarmone signalling triggers an auto-active bacteriocin necessary for genetic competence. Mol Microbiol 72:905–917 [CrossRef][PubMed]
    [Google Scholar]
  44. Qi F., Ferretti J. ( 2011). The StreptococcusVeillonella community: how genome sequencing aids our understanding of interspecies interaction. Oral Microbial Communities: Genomic Inquiry and Interspecies Communication351–370 Kolenbrander P. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  45. Qi F., Chen P., Caufield P. W. ( 2001). The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl Environ Microbiol 67:15–21 [CrossRef][PubMed]
    [Google Scholar]
  46. Ramos A., Poolman B., Santos H., Lolkema J. S., Konings W. N. ( 1994). Uniport of anionic citrate and proton consumption in citrate metabolism generates a proton motive force in Leuconostoc oenos . J Bacteriol 176:4899–4905[PubMed]
    [Google Scholar]
  47. Ramos A., Lolkema J. S., Konings W. N., Santos H. ( 1995). Enzyme basis for pH regulation of citrate and pyruvate metabolism by Leuconostoc oenos . Appl Environ Microbiol 61:1303–1310[PubMed]
    [Google Scholar]
  48. Rogers G. B., Hoffman L. R., Whiteley M., Daniels T. W., Carroll M. P., Bruce K. D. ( 2010). Revealing the dynamics of polymicrobial infections: implications for antibiotic therapy. Trends Microbiol 18:357–364 [CrossRef][PubMed]
    [Google Scholar]
  49. Rogosa M., Bishop F. S. ( 1964). The genus Veillonella. II. Nutritional studies. J Bacteriol 87:574–580[PubMed]
    [Google Scholar]
  50. Rosan B., Lamont R. J. ( 2000). Dental plaque formation. Microbes Infect 2:1599–1607 [CrossRef][PubMed]
    [Google Scholar]
  51. Rozkiewicz D., Daniluk T., Zaremba M. L., Cylwik-Rokicka D., Luczaj-Cepowicz E., Milewska R., Marczuk-Kolada G., Stokowska W. ( 2006). Bacterial composition in the supragingival plaques of children with and without dental caries. Adv Med Sci 51:Suppl. 1182–186[PubMed]
    [Google Scholar]
  52. Russell J. I., MacFarlane T. W., Aitchison T. C., Stephen K. W., Burchell C. K. ( 1990). Salivary levels of mutans streptococci, Lactobacillus, Candida, and Veillonella species in a group of Scottish adolescents. Community Dent Oral Epidemiol 18:17–21 [CrossRef][PubMed]
    [Google Scholar]
  53. Salema M., Lolkema J. S., San Romão M. V., Lourero Dias M. C. ( 1996). The proton motive force generated in Leuconostoc oenos by l-malate fermentation. J Bacteriol 178:3127–3132[PubMed]
    [Google Scholar]
  54. Schneider K., Dimroth P., Bott M. ( 2000). Biosynthesis of the prosthetic group of citrate lyase. Biochemistry 39:9438–9450 [CrossRef][PubMed]
    [Google Scholar]
  55. Sheng J., Marquis R. E. ( 2007). Malolactic fermentation by Streptococcus mutans . FEMS Microbiol Lett 272:196–201 [CrossRef][PubMed]
    [Google Scholar]
  56. Sibley C. D., Rabin H., Surette M. G. ( 2006). Cystic fibrosis: a polymicrobial infectious disease. Future Microbiol 1:53–61 [CrossRef][PubMed]
    [Google Scholar]
  57. Sperandio B., Gautier C., Pons N., Ehrlich D. S., Renault P., Guédon E. ( 2010). Three paralogous LysR-type transcriptional regulators control sulfur amino acid supply in Streptococcus mutans . J Bacteriol 192:3464–3473 [CrossRef][PubMed]
    [Google Scholar]
  58. Terleckyj B., Shockman G. D. ( 1975). Amino acid requirements of Streptococcus mutans and other oral streptococci. Infect Immun 11:656–664[PubMed]
    [Google Scholar]
  59. Thomas E. L., Pera K. A., Smith K. W., Chwang A. K. ( 1983). Inhibition of Streptococcus mutans by the lactoperoxidase antimicrobial system. Infect Immun 39:767–778[PubMed]
    [Google Scholar]
  60. Tong H., Chen W., Merritt J., Qi F., Shi W., Dong X. ( 2007). Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2: a possible counteroffensive strategy for interspecies competition. Mol Microbiol 63:872–880 [CrossRef][PubMed]
    [Google Scholar]
  61. van der Ploeg J. R. ( 2005). Regulation of bacteriocin production in Streptococcus mutans by the quorum-sensing system required for development of genetic competence. J Bacteriol 187:3980–3989 [CrossRef][PubMed]
    [Google Scholar]
  62. Wang B. Y., Kuramitsu H. K. ( 2005). Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii . Appl Environ Microbiol 71:354–362 [CrossRef][PubMed]
    [Google Scholar]
  63. Wu C., Ayala E. A., Downey J. S., Merritt J., Goodman S. D., Qi F. ( 2010a). Regulation of ciaXRH operon expression and identification of the CiaR regulon in Streptococcus mutans . J Bacteriol 192:4669–4679 [CrossRef][PubMed]
    [Google Scholar]
  64. Wu C., Cichewicz R., Li Y., Liu J., Roe B., Ferretti J., Merritt J., Qi F. ( 2010b). Genomic island TnSmu2 of Streptococcus mutans harbors a nonribosomal peptide synthetase-polyketide synthase gene cluster responsible for the biosynthesis of pigments involved in oxygen and H2O2 tolerance. Appl Environ Microbiol 76:5815–5826 [CrossRef][PubMed]
    [Google Scholar]
  65. Xie Z., Okinaga T., Niu G., Qi F., Merritt J. ( 2010). Identification of a novel bacteriocin regulatory system in Streptococcus mutans . Mol Microbiol 78:1431–1447 [CrossRef][PubMed]
    [Google Scholar]
  66. Zaura E., Keijser B. J., Huse S. M., Crielaard W. ( 2009). Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 9:259 [CrossRef][PubMed]
    [Google Scholar]
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