and Exhibit Metabolic Symbioses

English version České info

Unlike the traditional view that most diseases are caused by infection with a single bacterial species, some chronic diseases including periodontitis result from the perturbation of the natural microbiota and the proliferation of a number of opportunistic pathogens. Both Porphyromonas gingivalis and Treponema denticola have been associated with the progression and severity of chronic periodontitis and have been shown to display synergistic virulence in animal models. However, the underlying mechanisms to these observations are unclear. Here we demonstrate that these two bacteria grow synergistically in continuous co-culture and modify their gene expression. The expression of T. denticola genes encoding known virulence factors and enzymes involved in the uptake and metabolism of the amino acid glycine was up-regulated in co-culture. T. denticola stimulated the proteolytic P. gingivalis to produce free glycine, which T. denticola used as a major carbon source. Our study shows P. gingivalis and T. denticola co-operate metabolically and this helps to explain their synergistic virulence in animal models and their intimate association in vivo.

Vyšlo v časopise: and Exhibit Metabolic Symbioses. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003955
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003955

Souhrn

Zdroje

1. SocranskySS, HaffajeeAD, CuginiMA, SmithC, KentRL (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134–144.

2. DarveauRP (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481–490.

3. HajishengallisG, LiangS, PayneMA, HashimA, JotwaniR, et al. (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10: 497–506.

4. HajishengallisG, LamontRJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27: 409–419.

5. MarshPD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149: 279–294.

6. ByrneSJ, DashperSG, DarbyIB, AdamsGG, HoffmannB, et al. (2009) Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol Immunol 24: 469–477.

7. BrownLF, BeckJD, RozierRG (1994) Incidence of attachment loss in community-dwelling older adults. J Periodontol 65: 316–323.

8. HaffajeeAD, SocranskySS, LindheJ, KentRL, OkamotoH, et al. (1991) Clinical risk indicators for periodontal attachment loss. J Clin Periodontol 18: 117–125.

9. SimonsonLG, McMahonKT, ChildersDW, MortonHE (1992) Bacterial synergy of Treponema denticola and Porphyromonas gingivalis in a multinational population. Oral Microbiol Immunol 7: 111–112.

10. KigureT, SaitoA, SeidaK, YamadaS, IshiharaK, et al. (1995) Distribution of Porphyromonas gingivalis and Treponema denticola in human subgingival plaque at different periodontal pocket depths examined by immunohistochemical methods. J Periodontal Res 30: 332–341.

11. RiviereGR, SmithKS, CarranzaNJr, TzagaroulakiE, KaySL, et al. (1996) Associations between Porphyromonas gingivalis and oral treponemes in subgingival plaque. Oral Microbiol Immunol 11: 150–155.

12. ZijngeV, van LeeuwenMB, DegenerJE, AbbasF, ThurnheerT, et al. (2010) Oral biofilm architecture on natural teeth. PLoS One 5: e9321.

13. WoodSR, KirkhamJ, MarshPD, ShoreRC, NattressB, et al. (2000) Architecture of intact natural human plaque biofilms studied by confocal laser scanning microscopy. J Dent Res 79: 21–27.

14. GrenierD (1992) Nutritional interactions between two suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis. Infect Immun 60: 5298–5301.

15. GrenierD (1992) Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola. Oral Microbiol Immunol 7: 280–284.

16. KesavaluL, HoltSC, EbersoleJL (1998) Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol 13: 373–377.

17. KesavaluL, SathishkumarS, BakthavatchaluV, MatthewsC, DawsonD, et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704–1712.

18. OrthRK, O'Brien-SimpsonNM, DashperSG, ReynoldsEC (2011) Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model. Mol Oral Microbiol 26: 229–240.

19. NiliusAM, SpencerSC, SimonsonLG (1993) Stimulation of in vitro growth of Treponema denticola by extracellular growth factors produced by Porphyromonas gingivalis. J Dent Res 72: 1027–1031.

20. OnagawaM, IshiharaK, OkudaK (1994) Coaggregation between Porphyromonas gingivalis and Treponema denticola. Bull Tokyo Dent Coll 35: 171–181.

21. YaoES, LamontRJ, LeuSP, WeinbergA (1996) Interbacterial binding among strains of pathogenic and commensal oral bacterial species. Oral Microbiol Immunol 11: 35–41.

22. KolenbranderPE (2000) Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 54: 413–437.

23. ItoR, IshiharaK, ShojiM, NakayamaK, OkudaK (2010) Hemagglutinin/Adhesin domains of Porphyromonas gingivalis play key roles in coaggregation with Treponema denticola. FEMS Immunol Med Microbiol 60: 251–260.

24. KuramitsuHK, ChenW, IkegamiA (2005) Biofilm formation by the periodontopathic bacteria Treponema denticola and Porphyromonas gingivalis. J Periodontol 76: 2047–2051.

25. YamadaM, IkegamiA, KuramitsuHK (2005) Synergistic biofilm formation by Treponema denticola and Porphyromonas gingivalis. FEMS Microbiol Lett 250: 271–277.

26. Zainal-AbidinZ, VeithPD, DashperSG, ZhuY, CatmullDV, et al. (2012) Differential proteomic analysis of a polymicrobial biofilm. J Proteome Res 11: 4449–4464.

27. VeithPD, DashperSG, O'Brien-SimpsonNM, PaoliniRA, OrthR, et al. (2009) Major proteins and antigens of Treponema denticola. Biochim Biophys Acta 1794: 1421–1432.

28. OrthR, O'Brien-SimpsonN, DashperS, WalshK, ReynoldsE (2010) An efficient method for enumerating oral spirochetes using flow cytometry. J Microbiol Methods 80: 123–128.

29. RouillardJM, ZukerM, GulariE (2003) OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Nucleic Acids Res 31: 3057–3062.

30. MitchellHL, DashperSG, CatmullDV, PaoliniRA, ClealSM, et al. (2010) Treponema denticola biofilm-induced expression of a bacteriophage, toxin-antitoxin systems and transposases. Microbiology 156: 774–788.

31. NelsonKE, FleischmannRD, DeBoyRT, PaulsenIT, FoutsDE, et al. (2003) Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J Bacteriol 185: 5591–5601.

32. YangYH, DudoitS, LuuP, LinDM, PengV, et al. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15.

33. LoAW, SeersCA, BoyceJD, DashperSG, SlakeskiN, et al. (2009) Comparative transcriptomic analysis of Porphyromonas gingivalis biofilm and planktonic cells. BMC Microbiol 9: 18.

34. DashperSG, AngCS, VeithPD, MitchellHL, LoAW, et al. (2009) Response of Porphyromonas gingivalis to heme limitation in continuous culture. J Bacteriol 191: 1044–1055.

35. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57: 289–300.

36. TatusovRL, FedorovaND, JacksonJD, JacobsAR, KiryutinB, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.

37. AlmEJ, HuangKH, PriceMN, KocheRP, KellerK, et al. (2005) The MicrobesOnline Web site for comparative genomics. Genome Res 15: 1015–1022.

38. VandesompeleJ, De PreterK, PattynF, PoppeB, Van RoyN, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034.0031–research0034.0011.

39. RozenS, SkaletskyH (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365–386.

40. SaundersEC, NgWW, ChambersJM, NgM, NadererT, et al. (2011) Isotopomer profiling of Leishmania mexicana promastigotes reveals important roles for succinate fermentation and aspartate uptake in tricarboxylic acid cycle (TCA) anaplerosis, glutamate synthesis, and growth. J Biol Chem 286: 27706–27717.

41. GuestJR (1977) Menaquinone biosynthesis: mutants of Escherichia coli K-12 requiring 2-succinylbenzoate. J Bacteriol 130: 1038–1046.

42. BabaT, AraT, HasegawaM, TakaiY, OkumuraY, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.

43. Sambrook J, Russell DW (2001) Molecular cloning : a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory.

44. WyssC (2007) Fatty acids synthesized by oral treponemes in chemically defined media. FEMS Microbiol Lett 269: 70–76.

45. TatusovRL, KooninEV, LipmanDJ (1997) A genomic perspective on protein families. Science 278: 631–637.

46. MayrandD, McBrideBC (1980) Ecological relationships of bacteria involved in a simple, mixed anaerobic infection. Infect Immun 27: 44–50.

47. SeshadriR, MyersGS, TettelinH, EisenJA, HeidelbergJF, et al. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci U S A 101: 5646–5651.

48. DashperSG, BrownfieldL, SlakeskiN, ZilmPS, RogersAH, et al. (2001) Sodium ion-driven serine/threonine transport in Porphyromonas gingivalis. J Bacteriol 183: 4142–4148.

49. TakahashiN, SatoT, YamadaT (2000) Metabolic pathways for cytotoxic end product formation from glutamate- and aspartate-containing peptides by Porphyromonas gingivalis. J Bacteriol 182: 4704–4710.

50. ConeJE, Del RioRM, DavisJN, StadtmanTC (1976) Chemical characterization of the selenoprotein component of clostridial glycine reductase: identification of selenocysteine as the organoselenium moiety. Proc Natl Acad Sci U S A 73: 2659–2663.

51. Jackson-RosarioS, SelfWT (2009) Inhibition of selenium metabolism in the oral pathogen Treponema denticola. J Bacteriol 191: 4035–4040.

52. AndreesenJR (1994) Glycine metabolism in anaerobes. Antonie Van Leeuwenhoek 66: 223–237.

53. AndreesenJR (2004) Glycine reductase mechanism. Curr Opin Chem Biol 8: 454–461.

54. EbersoleJL, KesavaluL, SchneiderSL, MachenRL, HoltSC (1995) Comparative virulence of periodontopathogens in a mouse abscess model. Oral Dis 1: 115–128.

55. KimizukaR, KatoT, IshiharaK, OkudaK (2003) Mixed infections with Porphyromonas gingivalis and Treponema denticola cause excessive inflammatory responses in a mouse pneumonia model compared with monoinfections. Microbes Infect 5: 1357–1362.

56. KesavaluL, WalkerSG, HoltSC, CrawleyRR, EbersoleJL (1997) Virulence characteristics of oral treponemes in a murine model. Infect Immun 65: 5096–5102.

57. GemmellE, BirdPS, CarterCL, DrysdaleKE, SeymourGJ (2002) Effect of Fusobacterium nucleatum on the T and B cell responses to Porphyromonas gingivalis in a mouse model. Clin Exp Immunol 128: 238–244.

58. WashizuM, IshiharaK, HonmaK, OkudaK (2003) Effects of a mixed infection with Porphyromonas gingivalis and Treponema denticola on abscess formation and immune responses in mice. Bull Tokyo Dent Coll 44: 141–147.

59. CogoniV, Morgan-SmithA, FennoJC, JenkinsonHF, DymockD (2012) Treponema denticola chymotrypsin-like proteinase (CTLP) integrates spirochaetes within oral microbial communities. Microbiology 158: 759–770.

60. HashimotoM, OgawaS, AsaiY, TakaiY, OgawaT (2003) Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin. FEMS Microbiol Lett 226: 267–271.

61. VeseyPM, KuramitsuHK (2004) Genetic analysis of Treponema denticola ATCC 35405 biofilm formation. Microbiology 150: 2401–2407.

62. RosenG, GenzlerT, SelaMN (2008) Coaggregation of Treponema denticola with Porphyromonas gingivalis and Fusobacterium nucleatum is mediated by the major outer sheath protein of Treponema denticola. FEMS Microbiol Lett 289: 59–66.