1887

Abstract

Haemin/haem is one of the essential nutrients required by periodontopathogens such as Porphyromonas gingivalis to grow in vitro. In the oral cavity, this nutrient is believed to be provided by the crevicular fluid, a serum-like exudate produced during gum inflammation. However, P. gingivalis is also present in the healthy dental biofilm where inflammation is absent. This study was designed to answer the question: what organism(s) in the healthy dental biofilm provides haemin/haem to those periodontal pathogens? We report here that veillonellae, a group of bridging species in dental biofilm development, harbour a complete gene cluster for haem biosynthesis. Haemin production was detected from cell lysate, suggesting that the haem biosynthesis pathway is functional in veillonellae. Using the only transformable strain Veillonella atypica OK5, we inactivated specific key genes in the haem biosynthesis pathway. Inactivation of hemE, encoding the enzyme uroporphyrinogen decarboxylase, not only abolished haemin production but also significantly decreased OK5-supported growth of P. gingivalis. A luciferase gene reporter to the hemEHG operon demonstrated up-regulation of operon expression by P. gingivalis. Analysis of all sequenced genomes of oral bacteria in the HOMD database identified three genera (Veillonella, Propionibacterium and Aggregatibacter) that have a complete haem biosynthesis gene cluster, suggesting that they all could be potential haemin/haem providers in the dental biofilm.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000366
2016-10-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/10/1735.html?itemId=/content/journal/micro/10.1099/mic.0.000366&mimeType=html&fmt=ahah

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 Microbiol43:5721–5732. [CrossRef][PubMed]
    [Google Scholar]
  2. Anzaldi L. L., Skaar E. P..( 2010;). Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. . Infect Immun78:4977–4989. [CrossRef][PubMed]
    [Google Scholar]
  3. 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 Microbiol40:1001–1009. [CrossRef][PubMed]
    [Google Scholar]
  4. Daep C. A., Novak E. A., Lamont R. J., Demuth D. R..( 2011;). Structural dissection and in vivo effectiveness of a peptide inhibitor of Porphyromonas gingivalis adherence to Streptococcus gordonii. . Infect Immun79:67–74. [CrossRef][PubMed]
    [Google Scholar]
  5. Hajishengallis G..( 2011;). Immune evasion strategies of Porphyromonas gingivalis. . J Oral Biosci53:233–240. [CrossRef][PubMed]
    [Google Scholar]
  6. Hajishengallis G., Lamont R. J..( 2012;). Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. . Mol Oral Microbiol27:409–419. [CrossRef][PubMed]
    [Google Scholar]
  7. He X., Wu C., Yarbrough D., Sim L., Niu G., Merritt J., Shi W., Qi F..( 2008;). The cia operon of Streptococcus mutans encodes a unique component required for calcium-mediated autoregulation. . Mol Microbiol70: 112–126. [CrossRef][PubMed]
    [Google Scholar]
  8. Huang R., Li M., Gregory R. L..( 2011;). Bacterial interactions in dental biofilm. . Virulence2:435–444. [CrossRef][PubMed]
    [Google Scholar]
  9. Jakubovics N. S., Gill S. R., Vickerman M. M., Kolenbrander P. E..( 2008;). Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. . FEMS Microbiol Ecol66:637–644. [CrossRef][PubMed]
    [Google Scholar]
  10. Kolenbrander P. E., Palmer R. J., Rickard A. H., Jakubovics N. S., Chalmers N. I., Diaz P. I..( 2006;). Bacterial interactions and successions during plaque development. . Periodontol 200042:47–79. [CrossRef][PubMed]
    [Google Scholar]
  11. Kolenbrander P. E., Palmer R. J., Periasamy S., Jakubovics N. S..( 2010;). Oral multispecies biofilm development and the key role of cell-cell distance. . Nat Rev Microbiol8:471–480. [CrossRef][PubMed]
    [Google Scholar]
  12. Lamont R. J., Jenkinson H. F..( 1998;). Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. . Microbiol Mol Biol Rev62:1244–1263.
    [Google Scholar]
  13. Lamont R. J., Yilmaz O..( 2002;). In or out: the invasiveness of oral bacteria. . Periodontol 200030:61–69. [CrossRef][PubMed]
    [Google Scholar]
  14. Liu J., Xie Z., Merritt J., Qi F..( 2012;). Establishment of a tractable genetic transformation system in Veillonella spp. . Appl Environ Microbiol78:3488–3491. [CrossRef][PubMed]
    [Google Scholar]
  15. Periasamy S., Kolenbrander P. E..( 2009;). Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. . J Bacteriol191:6804–6811. [CrossRef][PubMed]
    [Google Scholar]
  16. Periasamy S., Kolenbrander P. E..( 2010;). Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. . J Bacteriol192:2965–2972. [CrossRef][PubMed]
    [Google Scholar]
  17. Rogosa M..( 1964;). The genus Veillonella. I. General cultural, ecological, and biochemical considerations. . J Bacteriol87:162–170.
    [Google Scholar]
  18. Sharma A..( 2010;). Virulence mechanisms of Tannerella forsythia. . Periodontol 200054:106–116. [CrossRef][PubMed]
    [Google Scholar]
  19. Stinson M. W., Safulko K., Levine M. J..( 1991;). Adherence of Porphyromonas (Bacteroides) gingivalis to Streptococcus sanguis in vitro. . Infect Immun59:102–108.[PubMed]
    [Google Scholar]
  20. Stinson M. W., Haraszthy G. G., Zhang X. L., Levine M. J..( 1992;). Inhibition of Porphyromonas gingivalis adhesion to Streptococcus gordonii by human submandibular-sublingual saliva. . Infect Immun60:2598–2604.[PubMed]
    [Google Scholar]
  21. Tribble G. D., Lamont R. J..( 2010;). Bacterial invasion of epithelial cells and spreading in periodontal tissue. . Periodontol 200052:68–83. [CrossRef][PubMed]
    [Google Scholar]
  22. Zhou P., Li X., Qi F..( 2015a;). Establishment of a counter-selectable markerless mutagenesis system in Veillonella atypica. . J Microbiol Meth112:70–72. [CrossRef][PubMed]
    [Google Scholar]
  23. Zhou P., Liu J., Li X., Takahashi Y., Qi F..( 2015b;). The sialic acid binding protein, Hsa, in Streptococcus gordonii DL1 also mediates intergeneric coaggregation with Veillonella species. . Plos One10:,e0143898. [CrossRef]
    [Google Scholar]
  24. Zhou P., Liu J., Merritt J., Qi F..( 2015c;). A YadA-like autotransporter, Hag1 in Veillonella atypica is a multivalent hemagglutinin involved in adherence to oral streptococci, Porphyromonas gingivalis, and human oral buccal cells. . Mol Oral Microbiol30:269–279. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000366
Loading
/content/journal/micro/10.1099/mic.0.000366
Loading

Data & Media loading...

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