Over the last hundred years, groundbreaking research in oral microbiology has provided a broad and deep understanding about the oral microbiome, its interactions with our body, and how the community can affect our health, be protective, or lead to the development of dental diseases. During this exciting journey, hypotheses were proposed, and concepts were established, discarded, and later revisited from updated perspectives. Dental plaque, previously considered a polymicrobial community of unspecific pathogenicity, is recognized as microbial biofilms with healthy, cariogenic, or periodontopathogenic profiles, resulting from specific ecologic determinants and host factors. The “one pathogen, one disease” paradigm of oral infections has been replaced by a holistic concept of a microbial community as the entity of pathogenicity. Cutting-edge technology can now explore large microbial communities related to different clinical conditions, which has led to finding several novel disease-associated species and potential pathobionts and pathobiomes. This vast amount of data generated over time has widened our view of the etiology of caries and periodontal and peri-implant diseases and has promoted updated strategies to treat and prevent the oral diseases.
AasJAGriffenALDardisSRLeeAMOlsenIDewhirstFELeysEJPasterBJ. 2008. Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol. 46(4):1407–1417.
2.
AbuslemeLDupuyAKDutzanNSilvaNBurlesonJAStrausbaughLDGamonalJDiazPI. 2013. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 7(5):1016–1025.
3.
ApatzidouDLappinDFHamiltonGPapadopoulosCAKonstantinidisARiggioMP. 2017. Microbiome associated with peri-implantitis versus periodontal health in individuals with a history of periodontal disease. J Oral Microbiol. 9 Supp1:1325218.
4.
AxelssonPLindheJ.1978. Effect of controlled oral hygiene procedures on caries and periodontal disease in adults. J Clin Periodontol. 5(2):133–151.
5.
Belda-FerrePAlcarazLDCabrera-RubioRRomeroHSimon-SoroAPignatelliMMiraA.2012. The oral metagenome in health and disease. ISME J. 6(1):46–56.
6.
BoutinSHagenfeldDZimmermannHEl SayedNHöpkerTGreiserHKBecherHKimT-SDalpkeAH. 2017. Clustering of subgingival microbiota reveals microbial disease ecotypes associated with clinical stages of periodontitis in a cross-sectional study. Front Microbio. 8:340.
7.
BowenWH.1969. The induction of rampant dental caries in monkeys (Macacairus). Caries Res. 3(3):227–237.
8.
BrailsfordSRShahBSimonsDGilbertSClarkDInesIAdamsSEAllisonCBeightonD.2001. The predominant aciduric microflora of root-caries lesions. J Dent Res. 80(9):1828–1833.
9.
BurneRAMarquisRE. 2000. Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol Lett. 193(1):1–6.
10.
CaufieldPWLiYDasanayakeASaxenaD.2007. Diversity of lactobacilli in the oral cavities of young women with dental caries. Caries Res. 41(1):2–8.
11.
CharalampakisGBelibasakisGN. 2015. Microbiome of peri-implant infections: lessons from conventional, molecular and metagenomic analyses. Virulence. 6(3):183–187.
12.
ChoIBlaserMJ. 2012. The human microbiome: at the interface of health and disease. Nat Rev Genet. 13(4):260–270.
13.
ClarkeJK.1924. On the bacterial factor in the aetiology of dental caries. Br J Exp Pathol. 5(3):141–147.
14.
ColomboAPBennetSCottonSLGoodsonJMKentRHaffajeeADSocranskySSHasturkHVan DykeTEDewhirstFEet al. 2009. Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis and periodontal health using the Human Oral Microbe Identification Microarray (HOMIM). J Periodontol. 80(9):1421–1432.
15.
ColomboAPHaffajeeADDewhirstFEPasterBJSmithCMCuginiMASocranskySS. 1998. Clinical and microbiological features of refractory periodontitis subjects. J Clin Periodontol. 25(2):169–180.
16.
CostertonJWChengKJGeeseyGGLaddTINickelNCDasguptaMMarieTJ. 1987. Bacterial biofilms in nature and disease. Ann Rev Microbiol. 41:435–464.
17.
DabdoubSMTsigaridaAAKumarPS. 2013. Patient-specific analysis of periodontal and peri-implant microbiomes. J Dent Res. 92(12):168S–175S.
18.
DewhirstFEChenTIzardJPasterBJTannerACYuWHLakshmananAWadeWG. 2010. The human oral microbiome. J Bacteriol. 192(19):5002–5017.
19.
EdwardssonS.1968. Characteristics of caries-inducing human streptococci resembling Streptococcus mutans. Arch Oral Biol. 13(6):637–646.
20.
ErikssonLLif HolgersonPEsbergAJohanssonI.2018. Microbial complexes and caries in 17-year-olds with and without streptococcus mutans. J Dent Res. 97(3):275–282.
21.
FitzgeraldRJKeyesPH. 1960. Demonstration of the etiologic role of streptococci in experimental caries in the hamster. J Am Dent Assoc. 61:9–19.
22.
Frias-LopezJDuran-PinedoA.2012. Effect of periodontal pathogens on the metatranscriptome of a healthy multispecies biofilm model. J Bacteriol. 194(8):2082–2095.
23.
FritschiBZAlbert-KiszelyAPerssonGR. 2008. Staphylococcus aureus and other bacteria in untreated periodontitis. J Dent Res. 87(6):589–593.
24.
GeXRodriguezRTrinhMGunsolleyJXuP.2013. Oral microbiome of deep and shallow dental pockets in chronic periodontitis. PLoS One. 8(6):e65520.
25.
GibbonsRJHayDIChildsWCDavisG.1990. Role of cryptic receptors (cryptitopes) in bacterial adhesion to oral surfaces. Arch Oral Biol. 35:107S–114S.
26.
GibbonsRJVan HouteJ.1971. Selective bacterial adherence to oral epithelial surfaces and its role as an ecological determinant. Infect Immun. 3(4):567–573.
27.
GriffenALBeallCJCampbellJHFirestoneNDKumarPSYangZKPodarMLeysEJ. 2012. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 6(6):1176–1185.
28.
GrossELBeallCJKutschSRFirestoneNDLeysEJGriffenAL. 2012. Beyond Streptococcus mutans: dental caries onset linked to multiple species by 16S rRNA community analysis. PLoS One. 7(10):e47722.
29.
HaffajeeADTelesRPSocranskySS. 2006. The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontol 2000. 42:219–258.
30.
HajishengallisGDarveauRPCurtisMA. 2012. The keystone-pathogen hypothesis. Nat Rev Microbiol. 10(10):717–725.
31.
Hall-StoodleyLCostertonJWStoodleyP.2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2(2):95–108.
32.
HardieJMThomsonPLSouthRJMarshPDBowdenGHMcKeeASFilleryEDSlackGL. 1977. A longitudinal epidemiological study on dental plaque and the development of dental caries—interim results after two years. J Dent Res. 56:C90–C98.
33.
HaubekDEnnibiOKPoulsenKVaethMPoulsenSKilianM.2008. Risk of aggressive periodontitis in adolescent carriers of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitansin Morocco: a prospective longitudinal cohort study. Lancet. 371(9608):237–242.
34.
HongBYFurtado AraujoMVStrausbaughLDTerziEIoannidouEDiazPI. 2015. Microbiome profiles in periodontitis in relation to host and disease characteristics. PLoS One. 10(5):e0127077.
35.
HowePRHatchRE. 1917. A study of the microorganisms of dental caries. J Med Res. 36(3):481–492.
36.
HuangSYangFZengXChenJLiRWenTLiCWeiWLiuJChenLet al. 2011. Preliminary characterization of the oral microbiota of Chinese adults with and without gingivitis. BMC Oral Health. 11:33.
37.
JordanHVKeysPH. 1964. Aerobic, gram-positive filamentous bacteria as etiologic agents of experimental periodontal disease in hamsters. Arch Oral Biol. 9:401–414.
38.
KeyesPH.1960. The infectious and transmissible nature of experimental dental caries. Arch Oral Biol. 1:304–320.
39.
KianoushNNguyenKABrowneGVSimonianMHunterN.2014. pH gradient and distribution of streptococci, lactobacilli, prevotellae, and fusobacteria in carious dentine. Clin Oral Investig. 18(2):659–669.
40.
KirstMELiECAlfantBChiYYWalkerCMagnussonIWangGP. 2015. Dysbiosis and alterations in predicted functions of the subgingival microbiome in chronic periodontitis. Appl Environ Microbiol. 81(2):783–793.
41.
KistlerJOBoothVBradshawDJWadeWG. 2013. Bacterial community development in experimental gingivitis. PLoS One. 8(8):e71227.
42.
KolenbranderPEGaneshkumarNCasselsFJHughesCV. 1993. Coaggregation: specific adherence among human oral plaque bacteria. FASEB J. 7(5):406–413.
43.
KrasseBJordanHVEdwardssonSSvenssonITrellL.1968. The occurrence of certain “caries-inducing” streptococci in human dental plaque material with special reference to frequency and activity of caries. Arch Oral Biol. 13(8):911–918.
44.
KumarPSGriffenALMoeschbergerMLLeysEJ. 2005. Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol. 43(8):3944–3955.
45.
LamontRJHajishengallisG.2015. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med. 21(3):172–183.
46.
LiYIsmailAIGeYTellezMSohnW.2007. Similarity of bacterial populations in saliva from African-American mother-child dyads. J Clin Microbiol. 45(9):3082–3085.
47.
ListgartenMA.1965. Electron microscopic observations of the bacterial flora of acute necrotizing ulcerative gingivitis. J Periodontol. 36:328–339.
48.
ListgartenMA.1976. Structure of the microbial flora associated with periodontal health and disease in man: a light and electron microscopic study. J Periodontol. 47(1):1–18.
49.
LiuBFallerLLKlitgordNMazumdarVGhodsiMSommerDDGibbonsTRTreangenTJChangYLiSet al. 2012. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoSOne. 7(6):e37919.
50.
LöeHTheiladeEJensenSB. 1965. Experimental gingivitis in man. J Periodontol. 36:177–187.
51.
LoescheWJ.1979. Clinical and microbiological aspects of chemotherapeutic agents used according to the specific plaque hypothesis. J Dent Res. 58(12):2404–2412.
52.
MacdonaldJBSocranskySSGibbonsRJ. 1963. Aspects of the pathogenesis of mixed anaerobic infection of mucous membranes. J Dent Res. 42(1):529–544.
53.
MantzouraniMFenlonMBeightonD.2009. Association between Bifidobacteriaceae and the clinical severity of root caries lesions. Oral Microbiol Immunol. 24(1):32–37.
54.
MarchantSBrailsfordSRTwomeyACRobertsGJBeightonD.2001. The predominant microflora of nursing caries lesions. Caries Res. 35(6):397–406.
55.
Mark WelchJLRossettiBJRiekenCWDewhirstFEBorisyGG. 2016. Biogeography of a human oral microbiome at the micron scale. Proc Natl Acad Sci U S A. 113(3):E791–E800.
56.
MarshPD.1994. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res. 8(2):263–271.
57.
MarshPD.2005. Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol. 32(6):7S–15S.
58.
MaruyamaNMaruyamaFTakeuchiYAikawaCIzumiYNakagawaI.2014. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep. 4:6602.
59.
McLeanJSBorBToTTLiuQKearnsKASoldenLMWrightonKHeXShiW.2018. Evidence of independent acquisition and adaption of ultra-small bacteria to human hosts across the highly diverse yet reduced genomes of the phylum Saccharibacteria. bioRχiv. doi:10.1101/258137.
60.
MeyleJChappleI.2015. Molecular aspects of the pathogenesis of periodontitis. Periodontol 2000. 69(1):7–17.
61.
MillerWD.1890. The micro-organisms of the human mouth: the local and general diseases which are caused by them. Philadelphia (PA): The S.S. White Dental MFG Co.
62.
MombelliAvan OostenMASchurchEJrLandNP. 1987. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol. 2(4):145–151.
63.
MooreWEMooreLV. 1994. The bacteria of periodontal diseases. Periodontol 2000. 5:66–77.
64.
MougeotJLStevensCBCottonSLMortonDSKrishnanKBrennanMTLockhartPBPasterBJBahraniMougeotFK. 2016. Concordance of HOMIM and HOMINGS technologies in the microbiome analysis of clinical samples. J Oral Microbiol. 8:30379.
65.
MunsonMABanerjeeAWatsonTFWadeWG. 2004. Molecular analysis of the microflora associated with dental caries. J Clin Microbiol. 42(7):3023–3029.
66.
OrlandFJBlayneyJRHarrisonRWReyniersJATrexlerPCWagnerMGordonHALuckeyTD. 1954. Use of the germfree animal technic in the study of experimental dental caries: I. Basic observations on rats reared free of all micro-organisms. J Dent Res. 33(2):147–174.
67.
PageRCOffenbacherSSchroederHESeymourGJKornmanKS. 1997. Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000. 14:216–248.
68.
ParkOJYiHJeonJHKangSSKooKTKumKYChunJYunCHHanSH. 2015. Pyrosequencing analysis of subgingival microbiota in distinct periodontal conditions. J Dent Res. 94(7):921–927.
69.
PasterBJBochesSKGalvinJLEricsonRELauCNLevanosVASahasrabudheADewhirstFE. 2001. Bacterial diversity in human subgingival plaque. J Bacteriol. 183(12):3770–3783.
70.
PerssonGRRenvertS.2014. Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res. 16(6):783–793.
71.
PooleS.2016. Rethink: the surprising history of new ideas. New York (NY): Penguin Random House Editors.
72.
PrezaDOlsenIWillumsenTBochesSKCottonSLGrindeBPasterBJ. 2009. Microarray analysis of the microflora of root caries in elderly. Eur J Clin Microbiol Infect Dis. 28(5):509–517.
73.
RomanosGEBiltucciMTKokarasAPasterBJ. 2016. Bacterial composition at the implant-abutment connection under loading in vivo. Clin Implant Dent Relat Res. 8(1):138–145.
74.
RoseburyT.1947. The nature and significance of infection in periodontal disease. Oral Surg Oral Med Oral Pathol. 33(9):658–665.
75.
RoseburyT.1962. Microorganisms indigenous to man. New York (NY): McGraw-Hill Company.
76.
RosierBTMarshPDMiraA.2018. Resilience of the oral microbiota in health: mechanisms that prevent dysbiosis. J Dent Res. 97(4):371–380.
77.
Sanz-MartinIDoolittle-HallJTelesRPPatelMBelibasakisGNHämmerleCHFJungRETelesFRF. 2017. Exploring the microbiome of healthy and diseased peri-implant sites using Illumina sequencing. J Clin Periodontol. 44(12):1274–1284.
78.
SchincagliaGPHongBYRosaniaABaraszJThompsonASobueTPanagakosFBurlesonJADongari-BagtzoglouADiazPI. 2017. Clinical, immune, and microbiome traits of gingivitis and peri-implant mucositis. J Dent Res. 96(1):47–55.
79.
Schulze-SchweifingKBanerjeeAWadeWG. 2014. Comparison of bacterial culture and 16S rRNA community profiling by clonal analysis and pyrosequencing for the characterization of the dentine caries-associated microbiome. Front Cell Infect Microbiol. 4:164.
80.
ShibliJAMeloLFerrariDSFigueiredoLCFaveriMFeresM.2008. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 19(10):975–982.
81.
Simón-SoroABelda-FerrePCabrera-RubioRAlcarazLDMiraA.2013. A tissue-dependent hypothesis of dental caries. Caries Res. 47(6):591–600.
82.
Simón-SoroAGuillen-NavarroMMiraA.2014. Metatranscriptomics reveals overall active bacterial composition in caries lesions. J Oral Microbiol. 6:25443.
SlotsJRamsTEListgartenMA. 1988. Yeasts, enteric rods and pseudomonads in the subgingival flora of severe adult periodontitis. Oral Microbiol Immunol. 3(2):47–52.
85.
SocranskySSGibbonsRJ. 1965. Required role of Bacteroides melaninogenicus in mixed anaerobic infections. J Infect Dis. 115:247–253.
TakahashiN.2015. Oral microbiome metabolism: from “Who are they?” to “What are they doing?”J Dent Res. 94(12):1628–1637.
89.
TakahashiNNyvadB.2016. Ecological hypothesis of dentin and root caries. Caries Res. 50(4):294–303.
90.
TannerACHafferCBratthallGTViscontiRASocranskySS. 1979. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol. 6(5):278–307.
91.
TannerACMathneyJMKentRLChalmersNIHughesCVLooCYPradhanNKanasiEHwangJDahlanMAet al. 2011. Cultivable anaerobic microbiota of severe early childhood caries. J Clin Microbiol. 49(4):1464–1474.
92.
ThomasRZZijngeVCicekAde SoetJJHarmsenHJHuysmansMC. 2012. Shifts in the microbial population in relation to in situ caries progression. Caries Res. 46(5):427–431.
93.
TorlakovicLKlepac-CerajVOgaardBCottonSLPasterBJOlsenI.2012. Microbial community succession on developing lesions on human enamel. J Oral Microbiol. 4(1):e16125.
94.
Van HouteJLopmanJKentR. 1996. The final pH of bacteria comprising the predominant flora on sound and carious human root and enamel surfaces. J Dent Res. 75(4):1008–1014.
95.
Van HouteJSansoneCJoshipuraKKentR. 1991. In vitro acidogenic potential and mutans streptococci of human smooth-surface plaque associated with initial caries lesions and sound enamel. J Dent Res. 70(12):1497–1502.
96.
VartoukianSRAdamowskaALawlorMMoazzezRDewhirstFEWadeWG. 2016. In vitro cultivation of “unculturable” oral bacteria, facilitated by community culture and media supplementation with siderophores. PLoS One. 11(1): e0146926.
97.
Vayssier-TaussatMAlbinaECittiCCossonJFJacquesMALebrunMHLe LoirYOgliastroMPetitMARoumagnacPet al. 2014. Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics. Front Cell Infect Microbiol. 4:29.
98.
XuHTianJHaoWZhangQZhouQShiWQinMHeXChenF.2018. Oral microbiome shifts from caries-free to caries-affected status in 3-year-old Chinese children: a longitudinal study. Front Microbiol. 9:2009.
99.
YostSDuran-PinedoAETelesRKrishnanKFrias-LopezJ.2015. Functional signatures of oral dysbiosis during periodontitis progression revealed by microbial metatranscriptome analysis. Genome Med. 7(1):27. Erratum in: Genome Med. 2015;7(1):111.
100.
ZauraEKeijserBJHuseSMCrielaardW.2009. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 9:259.
