Saliva as the sole nutritional source in the development of multispecies communities in dental plaque

Microbiology Spectrum

Volumn 3, Issue 3, 2015, Pages

  Jakubovics, Nicholas S ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BIOFILM; CHEMISTRY; DENTAL CARIES; ENAMEL; GINGIVA; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; PERIODONTITIS; SALIVA; TOOTH PLAQUE;

BACTERIA; BIOFILMS; DENTAL CARIES; DENTAL ENAMEL; DENTAL PLAQUE; GINGIVA; HUMANS; PERIODONTITIS; SALIVA;

EID: 84959064347     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MBP-0013-2014     Document Type: Article

References (94)

1. Dye BA, Li X, Beltran-Aguilar ED. 2012. Selected oral health indicators in the United States, 2005-2008. NCHS Data Brief 96:1-8.
2. Pitts NB, Chestnutt IG, Evans D, White D, Chadwick B, Steele JG. 2006. The dentinal caries experience of children in the United Kingdom, 2003. Br Dent J 200:313-320.
3. Thornton-Evans G, Eke P, Wei L, Palmer A, Moeti R, Hutchins S, Borrell LN, Centers for Disease Control and Prevention. 2013. Periodontitis among adults aged =30 years-United States, 2009-2010. MMWR Surveill Summ 62(Suppl 3):129-135.
4. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG. 2010. The human oral microbiome. J Bacteriol 192:5002-5017.
5. Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, Nelson KE, Gill SR, Fraser-Liggett CM, Relman DA. 2010. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J 4:962-974.
6. Li K, Bihan M, Methè BA. 2013. Analyses of the stability and core taxonomic memberships of the human microbiome. PLoS One 8:e63139. doi:10.1371/journal.pone.0063139
7. Xu X, He J, Xue J, Wang Y, Li K, Zhang K, Guo Q, Liu X, Zhou Y, Cheng L, Li M, Li Y, Li Y, Shi W, Zhou X. 2014. Oral cavity contains distinct niches with dynamic microbial communities. Environ Microbiol: In press. doi:10.1111/1462-2920.12502.
8. Ge X, Rodriguez R, Trinh M, Gunsolley J, Xu P. 2013. Oral microbiome of deep and shallow dental pockets in chronic periodontitis. PLoS One 8:e65520. doi:10.1371/journal.pone.0065520
9. Li Y, He J, He Z, Zhou Y, Yuan M, Xu X, Sun F, Liu C, Li J, Xie W, Deng Y, Qin Y, VanNostrand JD, Xiao L, Wu L, Zhou J, Shi W, Zhou X. 2014. Phylogenetic and functional gene structure shifts of the oral microbiomes in periodontitis patients. ISME J 8:1879-1891.
10. Teles RP, Haffajee AD, Socransky SS. 2006. Microbiological goals of periodontal therapy. Periodontol 2000 42:180-218.
11. Marsh PD. 2003. Are dental diseases examples of ecological catastrophes? Microbiology 149:279-294.
12. Bowden GH, Li YH. 1997. Nutritional influences on biofilm development. Adv Dent Res 11:81-99.
13. de Almeida Pdel V, Grégio AM, Machado MA, de Lima AA, Azevedo LR. 2008. Saliva composition and functions: a comprehensive review. J Contemp Dent Pract 9:72-80.
14. Goodson JM. 2003. Gingival crevice fluid flow. Periodontol 2000 31:43-54.
15. Mori M, Kaseda M, Yamamoto T, Yamada S, Itabashi H. 2012. Capillary ion electrophoresis-capacitively coupled contactless conductivity detection of inorganic cations in human saliva on a polyvinyl alcoholcoated capillary. Anal Bioanal Chem 402:2425-2430.
16. Chen Z, Feng S, Pow EH, Lam OL, Mai S, Wang H. 2014. Organic anion composition of human whole saliva as determined by ion chromatography. Clin Chim Acta 438:231-235.
17. Kim YJ, Kim YK, Kho HS. 2010. Effects of smoking on trace metal levels in saliva. Oral Dis 16:823-830.
18. Jehmlich N, Golatowski C, Murr A, Salazar G, Dhople VM, Hammer E, Volker U. 2014. Comparative evaluation of peptide desalting methods for salivary proteome analysis. Clin Chim Acta 434:16-20.
19. Helmerhorst EJ, Oppenheim FG. 2007. Saliva: a dynamic proteome. J Dent Res 86:680-693.
20. Jurysta C, Bulur N, Oguzhan B, Satman I, Yilmaz TM, Malaisse WJ, Sener A. 2009. Salivary glucose concentration and excretion in normal and diabetic subjects. J Biomed Biotechnol 2009:430426.
21. Hannig C, Hannig M, Attin T. 2005. Enzymes in the acquired enamel pellicle. Eur J Oral Sci 113:2-13.
22. Lee YH, Zimmerman JN, Custodio W, Xiao Y, Basiri T, Hatibovic-Kofman S, Siqueira WL. 2013. Proteomic evaluation of acquired enamel pellicle during in vivo formation. PLoS One 8:e67919. doi:10.1371/journal.pone.0067919
23. Lawson JW. 1971. Growth of cariogenic streptococci in chemically defined medium. Arch Oral Biol 16:339-342.
24. Socransky SS, Dzink JL, Smith CM. 1985. Chemically defined medium for oral microorganisms. J Clin Microbiol 22:303-305.
25. Terleckyj B, Willett NP, Shockman GD. 1975. Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun 11:649-655.
26. Wyss C. 1992. Growth of Porphyromonas gingivalis, Treponema denticola, T. pectinovorum, T. socranskii, and T. vincentii in a chemically defined medium. J Clin Microbiol 30:2225-2229.
27. Schulze-Schweifing K, Banerjee A, Wade WG. 2014. Comparison of bacterial culture and 16S rRNA community profiling by clonal analysis and pyrosequencing for the characterization of the dentine cariesassociated microbiome. Front Cell Infect Microbiol 4:164.
28. Koo H, Falsetta ML, Klein MI. 2013. The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm. J Dent Res 92:1065-1073.
29. Takahashi N, Nyvad B. 2011. The role of bacteria in the caries process: ecological perspectives. J Dent Res 90:294-303.
30. de Soet JJ, Nyvad B, Kilian M. 2000. Strain-related acid production by oral streptococci. Caries Res 34:486-490.
31. Johnson JL, Moore LV, Kaneko B, Moore WE. 1990. Actinomyces georgiae sp. nov., Actinomyces gerencseriae sp. nov., designation of two genospecies of Actinomyces naeslundii, and inclusion of A. naeslundii serotypes II and III and Actinomyces viscosus serotype II in A. naeslundii genospecies 2. Int J Syst Bacteriol 40:273-286.
32. Bradshaw DJ, Homer KA, Marsh PD, Beighton D. 1994. Metabolic cooperation in oral microbial communities during growth on mucin. Microbiology 140:3407-3412.
33. Homer KA, Roberts G, Byers HL, Tarelli E, Whiley RA, Philpott-Howard J, Beighton D. 2001. Mannosidase production by viridans group streptococci. J Clin Microbiol 39:995-1001.
34. Yeung MK. 1993. Complete nucleotide sequence of the Actinomyces viscosus T14V sialidase gene: presence of a conserved repeating sequence among strains of Actinomyces spp. Infect Immun 61:109-116.
35. Kilian M, Mikkelsen L, Henrichsen J. 1989. Taxonomic study of viridans streptococci-description of Streptococcus gordonii sp. nov and emended descriptions of Streptococcus sanguis (White and Niven 1946), Streptococcus oralis (Bridge and Sneath 1982), and Streptococcus mitis (Andrewes and Horder 1906). Int J Syst Evol Microbiol 39:471-484.
36. Rangarajan M, Aduse-Opoku J, Hashim A, Paramonov N, CurtisMA. 2013. Characterization of the α-and β-mannosidases of Porphyromonas gingivalis. J Bacteriol 195:5297-5307.
37. Roy S, Phansopa C, Stafford P, Honma K, Douglas CW, Sharma A, Stafford GP. 2012. Beta-hexosaminidase activity of the oral pathogen Tannerella forsythia influences biofilm formation on glycoprotein substrates. FEMS Immunol Med Microbiol 65:116-120.
38. Reinholdt J, Tomana M, Mortensen SB, Kilian M. 1990. Molecular aspects of immunoglobulin A1 degradation by oral streptococci. Infect Immun 58:1186-1194.
39. van der Hoeven JS, van den Kieboom CW. 1990. Oxygen-dependent lactate utilization by Actinomyces viscosus and Actinomyces naeslundii. Oral Microbiol Immunol 5:223-225.
40. Brown SA, Whiteley M. 2007. A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol 189:6407-6414.
41. Aujoulat F, Bouvet P, Jumas-Bilak E, Jean-Pierre H, Marchandin H. 2014. Veillonella seminalis sp. nov., a novel anaerobic Gram-stainnegative coccus from human clinical samples, and emended description of the genus Veillonella. Int J Syst Evol Microbiol 64:3526-3531.
42. Traudt M, Kleinberg I. 1996. Stoichiometry of oxygen consumption and sugar, organic acid and amino acid utilization in salivary sediment and pure cultures of oral bacteria. Arch Oral Biol 41:965-978.
43. Curtis MA, Griffiths GS, Price SJ, Coulthurst SK, Johnson NW. 1988. The total protein concentration of gingival crevicular fluid. Variation with sampling time and gingival inflammation. J Clin Periodontol 15:628-632.
44. Andrade JA, Feres M, Figueiredo LC, Salvador SL, Cortelli SC. 2010. The ability of the BANA Test to detect different levels of P. gingivalis, T. denticola and T. forsythia. Braz Oral Res 24:224-230.
45. Rogers AH, Zilm PS, Gully NJ, Pfennig AL, Marsh PD. 1991. Aspects of the growth and metabolism of Fusobacterium nucleatum ATCC 10953 in continuous culture. Oral Microbiol Immunol 6:250-255.
46. Tan KH, Seers CA, Dashper SG, Mitchell HL, Pyke JS, Meuric V, Slakeski N, Cleal SM, Chambers JL, McConville MJ, Reynolds EC. 2014. Porphyromonas gingivalis and Treponema denticola exhibit metabolic symbioses. PLoS Pathog 10:e1003955. doi:10.1371/journal.ppat.1003955
47. Liu YL, Nascimento M, Burne RA. 2012. Progress toward understanding the contribution of alkali generation in dental biofilms to inhibition of dental caries. Int J Oral Sci 4:135-140.
48. Cowman RA, Perrella MM, Adams BO, Fitzgerald RJ. 1975. Amino acid requirements and proteolytic activity of Streptococcus sanguis. Appl Microbiol 30:374-380.
49. Terleckyj B, Shockman GD. 1975. Amino acid requirements of Streptococcus mutans and other oral streptococci. Infect Immun 11:656-664.
50. Jakubovics NS, Gill SR, Iobst SE, Vickerman MM, Kolenbrander PE. 2008. Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J Bacteriol 190:3646-3657.
51. Xu P, Ge X, Chen L, Wang X, Dou Y, Xu JZ, Patel JR, Stone V, Trinh M, Evans K, Kitten T, Bonchev D, Buck GA. 2011. Genome-wide essential gene identification in Streptococcus sanguinis. Sci Rep 1:125.
52. Dell'Anno A, Danovaro R. 2005. Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309:2179.
53. Liao S, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, Burne RA, Koo H, Brady LJ, Wen ZT. 2014. Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bacteriol 196:2355-2366.
54. Vitkov L, Klappacher M, Hannig M, Krautgartner WD. 2009. Extracellular neutrophil traps in periodontitis. J Periodontal Res 44:664-672.
55. Rogers AH. 1973. The vitamin requirements of some oral streptococci. Arch Oral Biol 18:227-232.
56. Wyss C. 2007. Fatty acids synthesized by oral treponemes in chemically defined media. FEMS Microbiol Lett 269:70-76.
57. Akcali A, Huck O, Buduneli N, Davideau JL, Köse T, Tenenbaum H. 2014. Exposure of Porphyromonas gingivalis to cortisol increases bacterial growth. Arch Oral Biol 59:30-34.
58. Sreenivasan PK, Meyer DH, Fives-Taylor PM. 1993. Factors influencing the growth and viability of Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 8:361-369.
59. AlJehani YA. 2014. Risk factors of periodontal disease: review of the literature. Int J Dent 2014:182513.
60. Lewis JP. 2010. Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms. Periodontol 2000 52:94-116.
61. Paik S, Brown A, Munro CL, Cornelissen CN, Kitten T. 2003. The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185:5967-5975.
62. Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF. 1998. The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180:290-295.
63. Crump KE, Bainbridge B, Brusko S, Turner LS, Ge X, Stone V, Xu P, Kitten T. 2014. The relationship of the lipoprotein SsaB, manganese and superoxide dismutase in Streptococcus sanguinis virulence for endocarditis. Mol Microbiol 92:1243-1259.
64. Oetjen J, Fives-Taylor P, Froeliger EH. 2002. The divergently transcribed Streptococcus parasanguis virulence-associated fimA operon encoding an Mn(2+)-responsive metal transporter and pepO encoding a zinc metallopeptidase are not coordinately regulated. Infect Immun 70:5706-5714.
65. Haswell JR, Pruitt BW, Cornacchione LP, Coe CL, Smith EG, Spatafora GA. 2013. Characterization of the functional domains of the SloR metalloregulatory protein in Streptococcus mutans. J Bacteriol 195:126-134.
66. Chen YYM, Shieh HR, Chang YC. 2013. The expression of the fim operon is crucial for the survival of Streptococcus parasanguinis FW213 within macrophages but not acid tolerance. PLoS One 8:e66163. doi:10.1371/journal/pone.0066163
67. Jakubovics NS, Smith AW, Jenkinson HF. 2000. Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38:140-153.
68. Jakubovics NS, Smith AW, Jenkinson HF. 2002. Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii. Microbiology 148:3255-3263.
69. Lewis JP, Iyer D, Anaya-Bergman C. 2009. Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155:3758-3774.
70. Barboza-Silva E, Castro AC, Marquis RE. 2005. Mechanisms of inhibition by fluoride of urease activities of cell suspensions and biofilms of Staphylococcus epidermidis, Streptococcus salivarius, Actinomyces naeslundii and of dental plaque. Oral Microbiol Immunol 20:323-332.
71. Chen YY, Burne RA. 2003. Identification and characterization of the nickel uptake system for urease biogenesis in Streptococcus salivarius 57.I. J Bacteriol 185:6773-6779.
72. de Jong MH, van der Hoeven JS, van OS JH, Olijve JH. 1984. Growth of oral Streptococcus species and Actinomyces viscosus in human saliva. Appl Environ Microbiol 47:901-904.
73. Watanabe S, Dawes C. 1988. The effects of different foods and concentrations of citric acid on the flow rate of whole saliva in man. Arch Oral Biol 33:1-5.
74. Kurita-Ochiai T, Fukushima K, Ochiai K. 1995. Volatile fatty acids, metabolic by-products of periodontopathic bacteria, inhibit lymphocyte proliferation and cytokine production. J Dent Res 74:1367-1373.
75. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. 2012. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8:e1002606. doi:10.1371/journal.pcbi.1002606
76. Vartoukian SR, Downes J, Palmer RM, Wade WG. 2013. Fretibacterium fastidiosum gen. nov., sp. nov., isolated from the human oral cavity. Int J Syst Evol Microbiol 63:458-463.
77. Soro V, Dutton LC, Sprague SV, Nobbs AH, Ireland AJ, Sandy JR, Jepson MA, Micaroni M, Splatt PR, Dymock D, Jenkinson HF. 2014. Axenic culture of a candidate division TM7 bacterium from the human oral cavity and biofilm interactions with other oral bacteria. Appl Environ Microbiol 80:6480-6489.
78. Katharios-Lanwermeyer S, Xi C, Jakubovics NS, Rickard AH. 2014. Mini-review: Microbial coaggregation: ubiquity and implications for biofilm development. Biofouling 30:1235-1251.
79. Palmer RJ Jr, Diaz PI, Kolenbrander PE. 2006. Rapid succession within the Veillonella population of a developing human oral biofilm in situ. J Bacteriol 188:4117-4124.
80. Johnson BP, Jensen BJ, Ransom EM, Heinemann KA, Vannatta KM, Egland KA, Egland PG. 2009. Interspecies signaling between Veillonella atypica and Streptococcus gordonii requires the transcription factor CcpA. J Bacteriol 191:5563-5565.
81. Stacy A, Everett J, Jorth P, Trivedi U, Rumbaugh KP, Whiteley M. 2014. Bacterial fight-and-flight responses enhance virulence in a polymicrobial infection. Proc Natl Acad Sci U S A 111:7819-7824.
82. Mazumdar V, Amar S, Segrè D. 2013. Metabolic proximity in the order of colonization of a microbial community. PLoS One 8:e77617. doi:10.1371/journal.pone.0077617
83. Hendrickson EL, Xia Q, Wang T, Lamont RJ, Hackett M. 2009. Pathway analysis for intracellular Porphyromonas gingivalis using a strain ATCC 33277 specific database. BMC Microbiol 9:185.
84. Hendrickson EL, Wang TS, Dickinson BC, Whitmore SE, Wright CJ, Lamont RJ, Hackett M. 2012. Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiol 12:211.
85. Hendrickson EL, Wang T, Beck DA, Dickinson BC, Wright CJ, Lamont RJ, Hackett M. 2014. Proteomics of Fusobacterium nucleatum within a model developing oral microbial community. Microbiologyopen 3:729-751.
86. Takahashi N, Washio J, Mayanagi G. 2010. Metabolomics of supragingival plaque and oral bacteria. J Dent Res 89:1383-1388.
87. Jorth P, Turner KH, Gumus P, Nizam N, Buduneli N, Whiteley M. 2014. Metatranscriptomics of the human oral microbiome during health and disease. MBio 5:e01012-14. doi:10.1128/mBio.01012-14
88. Edgar WM. 1992. Saliva: its secretion, composition and functions. Br Dent J 172:305-312.
89. Kejriwal S, Bhandary R, Thomas B, Kumari S. 2014. Estimation of levels of salivary mucin, amylase and total protein in gingivitis and chronic periodontitis patients. J Clin Diagn Res 8:ZC56-ZC60.
90. Neyraud E, Bult JH, Dransfield E. 2009. Continuous analysis of parotid saliva during resting and short-duration simulated chewing. Arch Oral Biol 54:449-456.
91. Naumova EA, Sandulescu T, Bochnig C, Al Khatib P, Lee WK, Zimmer S, Arnold WH. 2014. Dynamic changes in saliva after acute mental stress. Sci Rep 4:4884.
92. Watanabe M, Asatsuma M, Ikui A, Ikeda M, Yamada Y, Nomura S, Igarashi A. 2005. Measurements of several metallic elements and matrix metalloproteinases (MMPs) in saliva from patients with taste disorder. Chem Senses 30:121-125.
93. Brand HS, Jörning GG, Chamuleau RA, Abraham-Inpijn L. 1997. Effect of a protein-rich meal on urinary and salivary free amino acid concentrations in human subjects. Clin Chim Acta 264:37-47.
94. Syrjanen SM, Alakuijala L, Alakuijala P, Markkanen SO, Markkanen H. 1990. Free amino acid levels in oral fluids of normal subjects and patients with periodontal disease. Arch Oral Biol 35:189-193.