Skip to main content

Advertisement

Log in

Streptococcus dentisani is a common inhabitant of the oral microbiota worldwide and is found at higher levels in caries-free individuals

  • Original Article
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Streptococcus dentisani has been proposed as a promising probiotic against tooth decay, due to its ability to buffer acidic pH and to inhibit the growth of oral pathogens. However, it is unknown if this bacterial species has a global distribution. The current study aimed to establish the presence of S. dentisani in oral samples from different geographic locations by identifying the sequence of its 16S rRNA gene in available datasets from across the globe. In addition, an analytical and cross-sectional study was carried out to determine if the levels of this probiotic strain are higher in caries-free individuals compared to those with dental caries. Samples from various geographical sources demonstrated that S. dentisani is present in saliva and dental plaque from individuals of different continents. Typical S. dentisani levels in saliva ranged from 104 to 105 cells/ml and a total of 106–107 cells in dental plaque. Using real-time qPCR, S. dentisani was quantified from supragingival dental plaque of 25 caries-free and 29 caries-active individuals from a Mexican children population, where significantly higher proportions of S. dentisani were found in the caries-free group (p = 0.002). Finally, a negative correlation was found between caries levels (as measured by the dmft caries index) and the percentage of S. dentisani (p < 0.001). Thus, the current manuscript indicates that this species has a global distribution, can be found in saliva and dental plaque, and appears to be present in higher numbers in plaque samples from caries-free children.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Original qPCR data are available from the authors upon request.

References

  • Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, Leys EJ, Paster BJ (2008) Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46(4):1407–1417

    Article  CAS  Google Scholar 

  • Allaker RP, Stephen AS (2017) Use of probiotics and oral health. Curr Oral Health Rep 4(4):309–318

    Article  Google Scholar 

  • Angarita-Díaz MP, Díaz JA, Tupaz HA, López-López A, Forero D, Mira A, Dávila F, Cerón XA, Ochoa-Acosta EM, Goméz OL, Gonzalez G (2019) Presence of Streptococcus dentisani in the dental plaque of children from different Colombian cities. Clin Exp Dent Res 5(3):184–190

    Article  Google Scholar 

  • Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, Romero H, Simón-Soro A, Pignatelli M, Mira A (2012) The oral metagenome in health and disease. ISME J 6(1):46–56

    Article  CAS  Google Scholar 

  • Beighton D, Al-Haboubi M, Mantzourani M, Gilbert SC, Clark D, Zoitopoulos L, Gallagher JE (2010) Oral Bifidobacteria: caries-associated bacteria in older adults. J Dent Res 89(9):970–974

    Article  CAS  Google Scholar 

  • Benítez-Páez A, Portune KJ, Sanz Y (2016) Species-level resolution of 16S rRNA gene amplicons sequenced through the MinION portable nanopore sequencer. Gigascience 28(5):4

    Article  Google Scholar 

  • Camelo-Castillo A, Benítez-Páez A, Belda-Ferre P, Cabrera-Rubio R, Mira A (2014) Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 64(Pt 1):60–65

  • Cabrera-Rubio R, Garcia-Núñez M, Setó L, Antó JM, Moya A, Monsó E, Mira A (2012) Microbiome diversity in the bronchial tracts of patients with chronic obstructive pulmonary disease. J Clin Microbiol 50(11):3562–3568

    Article  Google Scholar 

  • Claesson MJ, O’Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O’Toole PW (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4(8):e6669.

  • Conrads G, Bockwoldt JA, Kniebs C, Abdelbary MMH (2018) Commentary: health-associated niche inhabitants as oral probiotics: The case of streptococcusdentisani. Front Microbiol 9:340. https://doi.org/10.3389/fmicb.2018.00340

  • Conrads G, Westenberger J, Lürkens M, Abdelbary MMH (2019) Isolation and bacteriocin-related typing of Streptococcus dentisani. Front Cell Infect Microbiol 16(9):110

    Article  Google Scholar 

  • Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WGJ (2010) The Human Oral Microbiome Bacteriol 192(19):5002–5017

    CAS  Google Scholar 

  • Dzidic M, Collado MC, Abrahamsson T, Artacho A, Stensson M, Jenmalm MC, Mira A (2018) Oral microbiome development during childhood: an ecological succession influenced by postnatal factors and associated with tooth decay. ISME J 12(9):2292–2306

    Article  Google Scholar 

  • Eren AM, Borisy GG, Huse SM, Mark Welch JL (2014) Oligotyping analysis of the human oral microbiome.Proc Natl Acad Sci U S A 111(28):E2875–84.

  • Escapa IF, Chen T, Huang Y, Gajare P, Dewhirst FE, Lemon KP (2018) New insights into human nostril microbiome from the expanded Human Oral Microbiome Database (eHOMD): a resource for the microbiome of the human aerodigestive tract. mSystems. 3(6):e00187–18.

  • Esteban-Fernández A, Ferrer MD, Zorraquín-Peña I, López-López A, Moreno-Arribas MV, Mira A (2019) In vitro beneficial effects of Streptococcus dentisani as potential oral probiotic for periodontal diseases. J Periodontol 90(11):1346–1355

    Article  Google Scholar 

  • Ferrer MD, López-López A, Nicolescu T, Perez-Vilaplana S, Boix-Amorós A, Dzidic M, Garcia S, Artacho A, Llena C, Mira A (2020a) Topic application of the probiotic Streptococcus dentisani improves clinical and microbiological parameters associated with oral health. Front Cell Infect Microbiol 31(10):465

  • Ferrer MD, López-López A, Nicolescu T, Salavert A, Méndez I, Cuñé J, Llena C, Mira A (2020b) A pilot study to assess oral colonization and pH buffering by the probiotic Streptococcus dentisani under different dosing regimes. Odontology 108(2):180–187. https://doi.org/10.1007/s10266-019-00458-y

  • He J, Li Y, Cao Y, Xue J, Zhou X (2015) The oral microbiome diversity and its relation to human diseases. Folia Microbiol 60(1):69–80

    Article  CAS  Google Scholar 

  • Huang X, Palmer SR, Ahn SJ, Richards VP, Williams ML, Nascimento MM, Burne RA (2016) A highly arginolytic Streptococcus species that potently antagonizes Streptococcus mutans. Appl Environ Microbiol 82(7):2187–2201

    Article  CAS  Google Scholar 

  • Imfeld TN, Lutz F (1980) Intraplaque acid formation assessed in vivo in children and young adults. Pediatr Dent 2(2):87–93

    Google Scholar 

  • Jensen A, Scholz CFP, Kilian M (2016) Re-evaluation of the taxonomy of the Mitis group of the genus Streptococcus based on whole genome phylogenetic analyses, and proposed reclassification of Streptococcus dentisani as Streptococcus oralis subsp. dentisani comb. nov., Streptococcus tigurinus as Streptococcus oralis subsp. tigurinus comb. nov., and Streptococcus oligofermentans as a later synonym of Streptococcus cristatus. Int J Syst Evol Microbiol 66(11):4803–4820.

  • Kressirer CA, Smith DJ, King WF, Dobeck JM, Starr JR, Tanner ACR (2017) Scardovia wiggsiae and its potential role as a caries pathogen. J Oral Biosci 59(3):135–141

    Article  Google Scholar 

  • Krishnan K, Chen T, Paster BJ (2017) A practical guide to the oral microbiome and its relation to health and disease. Oral Dis 23(3):276–286

    Article  CAS  Google Scholar 

  • Lalloo R, Tadakamadla SK, Kroon J, Tut O, Kularatna S, Boase R, Kapellas K, Gilchrist D, Cobbledick E, Rogers J, Johnson NW (2019) Salivary characteristics and dental caries experience in remote Indigenous children in Australia: a cross-sectional study. B.M.C. oral health 19(1):21

  • Li J, Quinque D, Horz HP, Li M, Rzhetskaya M, Raff JA, Hayes MG, Stoneking M (2014) Comparative analysis of the human saliva microbiome from different climate zones: Alaska, Germany, and Africa. BMC Microbiol 14(1):316

    Article  CAS  Google Scholar 

  • Llena C, Almarche A, Mira A, López MA (2019) Antimicrobial efficacy of the supernatant of Streptococcus dentisani against microorganisms implicated in root canal infections. J Oral Sci 61(1):184–194

    Article  Google Scholar 

  • López-López A, Camelo-Castillo A, Ferrer MD, Simon-Soro Á, Mira A (2017) Health-associated niche inhabitants as oral probiotics: the case of Streptococcus dentisani. Front Microbiol 8:379

    Article  Google Scholar 

  • Mason MR, Nagaraja H.N., Camerlengo T, Joshi V, Kumar PS (2013) Deep sequencing identifies ethnicity-specific bacterial signatures in the oral microbiome. PloS one 8(10): e77287

  • Mira A (2018) Oral microbiome studies: potential diagnostic and therapeutic implications. Adv Dent Res 29(1):71–77

    Article  CAS  Google Scholar 

  • Morou-Bermudez E, Rodriguez S, Bello AS, Dominguez-Bello MG (2015) Urease and dental plaque microbial profiles in children. PloS one 10(9):e0139315

  • Nakas E, Zukanović A (2007) The prevalence of cariogenic salivary microorganisms in children of various ages. Bosn J Basic Med Sci 7(2):166–170

    Article  Google Scholar 

  • Nascimento MM, Zaura E, Mira A, Takahashi N, Ten Cate JM (2017) Second era of OMICS in caries research: moving past the phase of disillusionment. J Dent Res 96(7):733–740

    Article  CAS  Google Scholar 

  • Nasidze I, Li J, Schroeder R, Creasey JL, Li M, Stoneking M (2011) High diversity of the saliva microbiome in Batwa Pygmies. PloS one 6(8):e23352

  • Navazesh M (1993) Methods for collecting saliva. Ann N Y Acad Sci 694:72–77

    Article  CAS  Google Scholar 

  • Rosier BT, Buetas E, Moya-Gonzalvez EM, Artacho A, Mira A (2020a) Nitrate as a potential prebiotic for the oral microbiome. Sci Rep 10(1):12895

    Article  CAS  Google Scholar 

  • Rosier BT, Moya-Gonzalvez EM, Corell-Escuin P, Mira A (2020) Isolation and characterization of nitrate-reducing bacteria as potential probiotics for oral and systemic health. Front Microbiol 15(11):555465.

  • Schaumann S, Staufenbiel I, Scherer R, Schilhabel M, Winkel A, Stumpp SN, Eberhard J, Stiesch M (2014) Pyrosequencing of supra- and subgingival biofilms from inflamed peri-implant and periodontal sites. BMC Oral Health 14:157

    Article  Google Scholar 

  • Simón-Soro A, Tomás I, Cabrera-Rubio R, Catalan MD, Nyvad B, Mira A (2013) Microbial geography of the oral cavity. J Dent Res 92(7):616–621

    Article  Google Scholar 

  • Velsko IM, Chakraborty B, Nascimento MM, Burne RA, Richards VP (2018) Species designations belie phenotypic and genotypic heterogeneity in oral streptococci. mSystems 3(6):e00158–18.

  • Verma D, Garg PK, Dubey AK (2018) Insights into the human oral microbiome. Arch Microbiology 200(4):525–540

    Article  CAS  Google Scholar 

  • Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP (2008) STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE)statement: guidelines for reporting observational studies. J Clin Epidemiol 61(4):344–349.

  • Walker GV, Heng NCK, Carne A, Tagg JR, Wescombe PA (2016) Salivaricin E and abundant dextranase activity may contribute to the anti-cariogenic potential of the probiotic candidate Streptococcus salivarius JH. Microbiology (reading) 162(3):476–486

    Article  CAS  Google Scholar 

  • Wang, Y., and Qian, P-Y (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4: e7401.

  • World Health Organization (2013) Oral health surveys: basic methods - 5th edition

  • Xu H, Hao W, Zhou Q, Wang W, Xia Z, Liu C, Chen X, Qin M, Chen F (2014) Plaque bacterial microbiome diversity in children younger than 30 months with or without caries prior to eruption of second primary molars. PloS one 9(2):e89269

  • Yamanaka W, Takeshita T, Shibata Y, Matsuo K, Eshima N, Yokoyama T, Yamashita Y (2012) Compositional stability of a salivary bacterial population against supragingival microbiota shift following periodontal therapy. PloS one 7(8):e42806

  • Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glöckner FO, Rosselló-Móra R (2008) The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31(4):241–250

    Article  CAS  Google Scholar 

  • Zaura E, Brandt BW, Prodan A, Teixeira de Mattos MJ, Imangaliyev S, Kool J, Buijs MJ, Jagers FL, Hennequin-Hoenderdos NL, Slot DE, Nicu EA, Lagerweij MD, Janus MM, Fernandez-Gutierrez MM, Levin E, Krom BP, Brand HS, Veerman EC, Kleerebezem M, Loos BG, van der Weijden GA, Crielaard W, Keijser, (2017) On the ecosystemic network of saliva in healthy young adults. BJ ISME J 11(5):1218–1231

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Sandra García Esteban for assistance with laboratory work.

Funding

This project was funded by grant FAI-2017 C17-FAI-06–53.53 (Universidad Autónoma de San Luis Potosí UASLP) from Fondo de Apoyo a la Investigación, Mexico, and by project PREVECAM reference INNVAL20/19/006 from Agencia Valenciana de Innovación (AVI), Spain.

Author information

Authors and Affiliations

Authors

Contributions

AM and ALL conceived and designed research. HLS, VEV, and SAR recruited patients and collected samples. HLS, SAR, and ACC analyzed data. ACC and ARG reviewed literature and collected data. ALL conducted experiments. HLS and ARG made figures. AM, ARG, HLS, and SAR wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Alex Mira.

Ethics declarations

Ethics approval and consent to participate

The study was approved by the Institutional Research Ethics Committee (Code: CEIFE-021–017), San Luis Potosí, Mexico. All parents of the children who qualified for the study received information about the purpose and the procedures, signed the informed consent, and agreed to participate voluntarily in this project.

Conflict of interest

AM is the inventor of a patent protecting the use of S. dentisani as a probiotic. The other authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López-Santacruz, H.D., López-López, A., Revilla-Guarinos, A. et al. Streptococcus dentisani is a common inhabitant of the oral microbiota worldwide and is found at higher levels in caries-free individuals. Int Microbiol 24, 619–629 (2021). https://doi.org/10.1007/s10123-021-00222-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-021-00222-9

Keywords

Navigation