Strain-specific colonization patterns and serum modulation of multi-species oral biofilm development

Anaerobe

Volumn 18, Issue 4, 2012, Pages 459-470

  Biyikoĝlu, Basak ^a   Ricker, Austin ^a   Diaz, Patricia I ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Biofilms; Fusobacterium nucleatum; Oral multi species communities; Porphyromonas gingivalis; Serum; Strain variability; Subgingival

Indexed keywords

ACTINOMYCES; ACTINOMYCES ORIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; COMMENSAL; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FUSOBACTERIUM NUCLEATUM; GINGIVA; HOST; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; SALIVA; SERUM; VEILLONELLA PARVULA;

ACTINOMYCES; BACTERIAL ADHESION; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; BIOTA; CULTURE MEDIA; FUSOBACTERIUM NUCLEATUM; HUMANS; MICROBIAL INTERACTIONS; MICROBIAL VIABILITY; PORPHYROMONAS GINGIVALIS; SALIVA; SERUM; SPECIES SPECIFICITY;

ACTINOMYCES; FUSOBACTERIUM NUCLEATUM; PORPHYROMONAS GINGIVALIS; VEILLONELLA PARVULA;

EID: 84864355923     PISSN: 10759964     EISSN: 10958274     Source Type: Journal    
DOI: 10.1016/j.anaerobe.2012.06.003     Document Type: Article

References (52)

1. Zijnge V., van Leeuwen M.B., Degener J.E., Abbas F., Thurnheer T., Gmur R., et al. Oral biofilm architecture on natural teeth. PLoS One 2010, 5:e9321.
2. Kolenbrander P.E. Surface recognition among oral bacteria: multigeneric coaggregations and their mediators. Crit Rev Microbiol 1989, 17:137-159.
3. Bradshaw D.J., Homer K.A., Marsh P.D., Beighton D. Metabolic cooperation in oral microbial communities during growth on mucin. Microbiology 1994, 140(Pt 12):3407-3412.
4. Jakubovics N.S., Gill S.R., Vickerman M.M., Kolenbrander P.E. Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. FEMS Microbiol Ecol 2008, 66:637-644.
5. Jakubovics N.S., Gill S.R., Iobst S.E., Vickerman M.M., Kolenbrander P.E. Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J Bacteriol 2008, 190:3646-3657.
6. Chawla A., Hirano T., Bainbridge B.W., Demuth D.R., Xie H., Lamont R.J. Community signalling between Streptococcus gordonii and Porphyromonas gingivalis is controlled by the transcriptional regulator CdhR. Mol Microbiol 2010, 78:1510-1522.
7. Griffen A.L., Beall C.J., Campbell J.H., Firestone N.D., Kumar P.S., Yang Z.K., et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 2012, 6:1176-1185.
8. Socransky S.S., Haffajee A.D. Periodontal microbial ecology. Periodontol 2000, 2005(38):135-187.
9. Diaz P.I., Zilm P.S., Rogers A.H. Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments. Microbiology 2002, 148:467-472.
10. Loe H., Theilade E., Jensen S.B. Experimental gingivitis in man. J Periodontol 1965, 36:177-187.
11. Kolenbrander P.E., Palmer R.J., Rickard A.H., Jakubovics N.S., Chalmers N.I., Diaz P.I. Bacterial interactions and successions during plaque development. Periodontol 2000, 2006(42):47-79.
12. Socransky S.S., Haffajee A.D., Cugini M.A., Smith C., Kent R.L. Microbial complexes in subgingival plaque. J Clin Periodontol 1998, 25:134-144.
13. Craig R.G., Boylan R., Yip J., Mijares D., Imam M., Socransky S.S., et al. Serum IgG antibody response to periodontal pathogens in minority populations: relationship to periodontal disease status and progression. J Periodontal Res 2002, 37:132-146.
14. Curtis M.A., Slaney J.M., Aduse-Opoku J. Critical pathways in microbial virulence. J Clin Periodontol 2005, 32(Suppl. 6):28-38.
15. Slots J., Gibbons R.J. Attachment of Bacteroides melaninogenicus subsp. asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. Infect Immun 1978, 19:254-264.
16. Periasamy S., Kolenbrander P.E. Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 2009, 191:6804-6811.
17. Maeda K., Tribble G.D., Tucker C.M., Anaya C., Shizukuishi S., Lewis J.P., et al. A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol Microbiol 2008, 69:1153-1164.
18. Kolenbrander P.E., Andersen R.N., Moore L.V. Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun 1989, 57:3194-3203.
19. Frandsen E.V., Poulsen K., Curtis M.A., Kilian M. Evidence of recombination in Porphyromonas gingivalis and random distribution of putative virulence markers. Infect Immun 2001, 69:4479-4485.
20. Igboin C.O., Griffen A.L., Leys E.J. Porphyromonas gingivalis strain diversity. J Clin Microbiol 2009, 47:3073-3081.
21. Neiders M.E., Chen P.B., Suido H., Reynolds H.S., Zambon J.J., Shlossman M., et al. Heterogeneity of virulence among strains of Bacteroides gingivalis. J Periodontal Res 1989, 24:192-198.
22. Genco C.A., Cutler C.W., Kapczynski D., Maloney K., Arnold R.R. A novel mouse model to study the virulence of and host response to Porphyromonas (Bacteroides) gingivalis. Infect Immun 1991, 59:1255-1263.
23. Davey M.E., Duncan M.J. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol 2006, 188:5510-5523.
24. Singh A., Wyant T., Anaya-Bergman C., Aduse-Opoku J., Brunner J., Laine M.L., et al. The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun 2011, 79:4533-4542.
25. Holm-Pedersen P., Agerbaek N., Theilade E. Experimental gingivitis in young and elderly individuals. J Clin Periodontol 1975, 2:14-24.
26. Curtis M.A., Sterne J.A., Price S.J., Griffiths G.S., Coulthurst S.K., Wilton J.M., et al. The protein composition of gingival crevicular fluid sampled from male adolescents with no destructive periodontitis: baseline data of a longitudinal study. J Periodontal Res 1990, 25:6-16.
27. Bostanci N., Heywood W., Mills K., Parkar M., Nibali L., Donos N. Application of label-free absolute quantitative proteomics in human gingival crevicular fluid by LC/MS E (gingival exudatome). J Proteome Res 2010, 9:2191-2199.
28. Ter Steeg P.F., Van der Hoeven J.S., de Jong M.H., van Munster P.J., Jansen M.J. Enrichment of subgingival microflora on human serum leading to accumulation of Bacteroides species, Peptostreptococci and Fusobacteria. Antonie Van Leeuwenhoek 1987, 53:261-272.
29. Jansen H.J., van der Hoeven J.S. Protein degradation by Prevotella intermedia and Actinomyces meyeri supports the growth of non-protein-cleaving oral bacteria in serum. J Clin Periodontol 1997, 24:346-353.
30. Naito Y., Gibbons R.J. Attachment of Bacteroides gingivalis to collagenous substrata. J Dent Res 1988, 67:1075-1080.
31. Diaz P.I., Xie Z., Sobue T., Thompson A., Biyikoglu B., Ricker A., et al. Synergistic interaction between Candida albicans and commensal oral streptococci in a novel in vitro mucosal model. Infect Immun 2012, 80:620-632.
32. Palmer R.J., Kazmerzak K., Hansen M.C., Kolenbrander P.E. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect Immun 2001, 69:5794-5804.
33. Periasamy S., Chalmers N.I., Du-Thumm L., Kolenbrander P.E. Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATCC 43146 for growth on saliva in a three-species community that includes Streptococcus oralis 34. Appl Environ Microbiol 2009, 75:3250-3257.
34. Davey M.E. Techniques for the growth of Porphyromonas gingivalis biofilms. Periodontol 2000, 2006(42):27-35.
35. Foster J.S., Kolenbrander P.E. Development of a multispecies oral bacterial community in a saliva-conditioned flow cell. Appl Environ Microbiol 2004, 70:4340-4348.
36. Chalmers N.I., Palmer R.J., Cisar J.O., Kolenbrander P.E. Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J Bacteriol 2008, 190:8145-8154.
37. Dix K., Watanabe S.M., McArdle S., Lee D.I., Randolph C., Moncla B., et al. Species-specific oligodeoxynucleotide probes for the identification of periodontal bacteria. J Clin Microbiol 1990, 28:319-323.
38. Cisar J.O., Kolenbrander P.E., Mcintire F.C. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces-Viscosus or Actinomyces-Naeslundii. Infect Immun 1979, 24:742-752.
39. Periasamy S., Kolenbrander P.E. Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J Bacteriol 2010, 192:2965-2972.
40. Marsh P.D., Moter A., Devine D.A. Dental plaque biofilms: communities, conflict and control. Periodontol 2000, 2011(55):16-35.
41. Listgarten M.A. Structure of the microbial flora associated with periodontal health and disease in man. A light and electron microscopic study. J Periodontol 1976, 47:1-18.
42. Karpathy S.E., Qin X., Gioia J., Jiang H., Liu Y., Petrosino J.F., et al. Genome sequence of Fusobacterium nucleatum subspecies polymorphum - a genetically tractable fusobacterium. PLoS One 2007, 2:e659.
43. Chen T., Hosogi Y., Nishikawa K., Abbey K., Fleischmann R.D., Walling J., et al. Comparative whole-genome analysis of virulent and avirulent strains of Porphyromonas gingivalis. J Bacteriol 2004, 186:5473-5479.
44. Periasamy S., Kolenbrander P.E. Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva. Infect Immun 2009, 77:3542-3551.
45. Diaz P.I. Microbial diversity and interactions in subgingival communities. Periodontal disease 2012, 17-40. Karger. D. Kinane, A. Mombelli (Eds.).
46. Dige I., Raarup M.K., Nyengaard J.R., Kilian M., Nyvad B. Actinomyces naeslundii in initial dental biofilm formation. Microbiology 2009, 155:2116-2126.
47. Kim H.J., Boedicker J.Q., Choi J.W., Ismagilov R.F. Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc Natl Acad Sci U S A 2008, 105:18188-18193.
48. Hajishengallis G., Liang S., Payne M.A., Hashim A., Jotwani R., Eskan M.A., et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011, 10:497-506.
49. Bradshaw D.J., Marsh P.D., Watson G.K., Allison C. Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect Immun 1998, 66:4729-4732.
50. Kolenbrander P.E., Parrish K.D., Andersen R.N., Greenberg E.P. Intergeneric coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp. Infect Immun 1995, 63:4584-4588.
51. Hammond A., Dertien J., Colmer-Hamood J.A., Griswold J.A., Hamood A.N. Serum inhibits P. aeruginosa biofilm formation on plastic surfaces and intravenous catheters. J Surg Res 2010, 159:735-746.
52. Williams J.C., McInnis K.A., Testerman T.L. Adherence of Helicobacter pylori to abiotic surfaces is influenced by serum. Appl Environ Microbiol 2008, 74:1255-1258.