Enhanced microbial diversity in the saliva microbiome induced by short-term probiotic intake revealed by 16S rRNA sequencing on the IonTorrent PGM platform

Journal of Biotechnology

Volumn 190, Issue , 2014, Pages 30-39

  Dassi, Erik ^a   Ballarini, Annalisa ^a   Covello, Giuseppina ^a   Abura'ed, Ahmed ^a   Anderle, Marica ^a   Asnicar, Francesco ^a   Betta, Stefano ^a   Branchi P , Paolo ^a   Caumo, Matteo ^a   Chiera, Silvia ^a   Clementi, Elena ^a   Fontana, Jason ^a   Girelli, Gabriele ^a   Holler, Silvia ^a   Lorenzoni, Marco ^a   Lucchini, Valentina ^a   Marchioretti, Caterina ^a   Pederiva, Chiara ^a   Pedot, Gloria ^a   Piol, Diana ^a   Ravanelli, Tommaso ^a   Rizzotto, Dario ^a   Sella, Nadir ^a   Tolio, Thomas ^a   Trenti, Massimiliano ^a   Zanella, Ilaria ^a   Quattrone, Alessandro ^a   Jousson, Olivier ^a   De Sanctis, Veronica ^a   Bertorelli, Roberto ^a   Denti, Michela Alessandra ^a   Segata, Nicola ^a   more..

^a UNIVERSITY OF TRENTO   (Italy)

Author keywords

16S rRNA; IonTorrent; Metagenomics; Probiotics; Saliva microbiome

Indexed keywords

RNA; SURVEYS;

16S RRNA; BACTERIAL DIVERSITY; HIGH-THROUGHPUT SEQUENCING; IONTORRENT; METAGENOMICS; MICROBIAL COMMUNITIES; MICROBIAL DIVERSITY; MICROBIOME;

PROBIOTICS;

PROBIOTIC AGENT; RNA 16S;

ACTINOMYCES; ARTICLE; CONTROLLED STUDY; FEMALE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN EXPERIMENT; MALE; MEDICAL DEVICE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NORMAL HUMAN; ROTHIA; SALIVA; STREPTOCOCCUS;

EID: 84911388443     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.03.024     Document Type: Article

References (47)

1. Abubucker S., Segata N., Goll J., Schubert A.M., Izard J., Cantarel B.L., Rodriguez-Mueller B., Zucker J., Thiagarajan M., Henrissat B., White O., Kelley S.T., Methe B., Schloss P.D., Gevers D., Mitreva M., Huttenhower C. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol. 2012, 8:e1002358.
2. Burne R.A., Zeng L., Ahn S.J., Palmer S.R., Liu Y., Lefebure T., Stanhope M.J., Nascimento M.M. Progress dissecting the oral microbiome in caries and health. Adv. Dent. Res. 2012, 24:77-80.
3. Burton J.P., Wescombe P.A., Macklaim J.M., Chai M.H., Macdonald K., Hale J.D., Tagg J., Reid G., Gloor G.B., Cadieux P.A. Persistence of the oral probiotic Streptococcus salivarius M18 is dose dependent and megaplasmid transfer can augment their bacteriocin production and adhesion characteristics. PLoS One 2013, 8:e65991.
4. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., McDonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
5. Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Huntley J., Fierer N., Owens S.M., Betley J., Fraser L., Bauer M., Gormley N., Gilbert J.A., Smith G., Knight R. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012, 6:1621-1624.
6. Curtis M.A., Zenobia C., Darveau R.P. The relationship of the oral microbiotia to periodontal health and disease. Cell host & microbe 2011, 10:302-306.
7. Dahle U.R., Tronstad L., Olsen I. Spirochaetes in oral infections. Endodont. Dent. Traumatol. 1993, 9:87-94.
8. DeSantis T.Z., Hugenholtz P., Larsen N., Rojas M., Brodie E.L., Keller K., Huber T., Dalevi D., Hu P., Andersen G.L. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 2006, 72:5069-5072.
9. Dewhirst F.E., Chen T., Izard J., Paster B.J., Tanner A.C., Yu W.H., Lakshmanan A., Wade W.G. The human oral microbiome. J. Bacteriol. 2010, 192:5002-5017.
10. Dierksen K.P., Moore C.J., Inglis M., Wescombe P.A., Tagg J.R. The effect of ingestion of milk supplemented with salivaricin A-producing Streptococcus salivarius on the bacteriocin-like inhibitory activity of streptococcal populations on the tongue. FEMS Microbiol. Ecol. 2007, 59:584-591.
11. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 2010, 26:2460-2461.
12. Fujinaka H., Takeshita T., Sato H., Yamamoto T., Nakamura J., Hase T., Yamashita Y. Relationship of periodontal clinical parameters with bacterial composition in human dental plaque. Arch. Microbiol. 2013, 195:371-383.
13. Hamady M., Knight R. Microbial community profiling for human microbiome projects: Tools, techniques, and challenges. Genome Res. 2009, 19:1141-1152.
14. Horz H.P., Meinelt A., Houben B., Conrads G. Distribution and persistence of probiotic Streptococcus salivarius K12 in the human oral cavity as determined by real-time quantitative polymerase chain reaction. Oral Microbiol. Immunol. 2007, 22:126-130.
15. Junemann S., Prior K., Szczepanowski R., Harks I., Ehmke B., Goesmann A., Stoye J., Harmsen D. Bacterial community shift in treated periodontitis patients revealed by ion torrent 16S rRNA gene amplicon sequencing. PLoS One 2012, 7:e41606.
16. Kistler J.O., Booth V., Bradshaw D.J., Wade W.G. Bacterial community development in experimental gingivitis. PLoS One 2013, 8:e71227.
17. Kunin V., Engelbrektson A., Ochman H., Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 2010, 12:118-123.
18. Langille M.G., Zaneveld J., Caporaso J.G., McDonald D., Knights D., Reyes J.A., Clemente J.C., Burkepile D.E., Vega Thurber R.L., Knight R., Beiko R.G., Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31:814-821.
19. Liu B., Faller L.L., Klitgord N., Mazumdar V., Ghodsi M., Sommer D.D., Gibbons T.R., Treangen T.J., Chang Y.C., Li S., Stine O.C., Hasturk H., Kasif S., Segre D., Pop M., Amar S. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 2012, 7:e37919.
20. Loman N.J., Misra R.V., Dallman T.J., Constantinidou C., Gharbia S.E., Wain J., Pallen M.J. Performance comparison of benchtop high-throughput sequencing platforms. Nat. Biotechnol. 2012, 30:434-439.
21. Lozupone C., Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 2005, 71:8228-8235.
22. Martin F.P., Wang Y., Sprenger N., Yap I.K., Lundstedt T., Lek P., Rezzi S., Ramadan Z., van Bladeren P., Fay L.B., Kochhar S., Lindon J.C., Holmes E., Nicholson J.K. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 2008, 4:157.
23. Milani C., Hevia A., Foroni E., Duranti S., Turroni F., Lugli G.A., Sanchez B., Martin R., Gueimonde M., van Sinderen D., Margolles A., Ventura M. Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One 2013, 8:e68739.
24. Morgan X.C., Tickle T.L., Sokol H., Gevers D., Devaney K.L., Ward D.V., Reyes J.A., Shah S.A., LeLeiko N., Snapper S.B., Bousvaros A., Korzenik J., Sands B.E., Xavier R.J., Huttenhower C. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012, 13:R79.
25. Nasidze I., Li J., Quinque D., Tang K., Stoneking M. Global diversity in the human salivary microbiome. Genome Res. 2009, 19:636-643.
26. Petrof E.O., Gloor G.B., Vanner S.J., Weese S.J., Carter D., Daigneault M.C., Brown E.M., Schroeter K., Allen-Vercoe E. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: 'RePOOPulating' the gut. Microbiome 2013, 1:3.
27. Rosenthal M., Aiello A.E., Chenoweth C., Goldberg D., Larson E., Gloor G., Foxman B. Impact of technical sources of variation on the hand microbiome dynamics of healthcare workers. PLoS One 2014, 9:e88999.
28. Rothberg J.M., Hinz W., Rearick T.M., Schultz J., Mileski W., Davey M., Leamon J.H., Johnson K., Milgrew M.J., Edwards M., Hoon J., Simons J.F., Marran D., Myers J.W., Davidson J.F., Branting A., Nobile J.R., Puc B.P., Light D., Clark T.A., Huber M., Branciforte J.T., Stoner I.B., Cawley S.E., Lyons M., Fu Y., Homer N., Sedova M., Miao X., Reed B., Sabina J., Feierstein E., Schorn M., Alanjary M., Dimalanta E., Dressman D., Kasinskas R., Sokolsky T., Fidanza J.A., Namsaraev E., McKernan K.J., Williams A., Roth G.T., Bustillo J. An integrated semiconductor device enabling non-optical genome sequencing. Nature 2011, 475:348-352.
29. Rudney J.D., Xie H., Rhodus N.L., Ondrey F.G., Griffin T.J. A metaproteomic analysis of the human salivary microbiota by three-dimensional peptide fractionation and tandem mass spectrometry. Mol. Oral Microbiol. 2010, 25:38-49.
30. Salipante S.J., Sengupta D.J., Rosenthal C., Costa G., Spangler J., Sims E.H., Jacobs M.A., Miller S.I., Hoogestraat D.R., Cookson B.T., McCoy C., Matsen F.A., Shendure J., Lee C.C., Harkins T.T., Hoffman N.G. Rapid 16S rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS One 2013, 8:e65226.
31. Santagati M., Scillato M., Patane F., Aiello C., Stefani S. Bacteriocin-producing oral streptococci and inhibition of respiratory pathogens. FEMS Immunol. Med. Microbiol. 2012, 65:23-31.
32. Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75:7537-7541.
33. Segata N., Boernigen D., Tickle T.L., Morgan X.C., Garrett W.S., Huttenhower C. Computational meta'omics for microbial community studies. Mol. Syst. Biol. 2013, 9:666.
34. Segata N., Haake S.K., Mannon P., Lemon K.P., Waldron L., Gevers D., Huttenhower C., Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012, 13:R42.
35. Segata N., Izard J., Waldron L., Gevers D., Miropolsky L., Garrett W.S., Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12:R60.
36. Snel J., Marco M.L., Kingma F., Noordman W.M., Rademaker J., Kleerebezem M. Competitive selection of lactic acid bacteria that persist in the human oral cavity. Appl. Environ. Microbiol. 2011, 77:8445-8450.
37. The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
38. Veiga P., Gallini C.A., Beal C., Michaud M., Delaney M.L., DuBois A., Khlebnikov A., van Hylckama Vlieg J.E., Punit S., Glickman J.N., Onderdonk A., Glimcher L.H., Garrett W.S. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18132-18137.
39. Vollaard E.J., Clasener H.A. Colonization resistance. Antimicrob. Agents Chemother. 1994, 38:409-414.
40. Wade W.G. The oral microbiome in health and disease. Pharmacol. Res. 2013, 69:137-143.
41. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73:5261-5267.
42. Wescombe P.A., Heng N.C., Burton J.P., Chilcott C.N., Tagg J.R. Streptococcal bacteriocins and the case for Streptococcus salivarius as model oral probiotics. Fut. Microbiol. 2009, 4:819-835.
43. Whiteley A.S., Jenkins S., Waite I., Kresoje N., Payne H., Mullan B., Allcock R., O'Donnell A. Microbial 16S rRNA Ion Tag and community metagenome sequencing using the Ion Torrent (PGM) Platform. J. Microbiol. Methods 2012, 91:80-88.
44. Whittaker R. Evolution and measurement of species diversity. Taxon 1972, 21:213-251.
45. Yang F., Zeng X., Ning K., Liu K.L., Lo C.C., Wang W., Chen J., Wang D., Huang R., Chang X., Chain P.S., Xie G., Ling J., Xu J. Saliva microbiomes distinguish caries-active from healthy human populations. ISME J. 2012, 6:1-10.
46. Yergeau E., Lawrence J.R., Sanschagrin S., Waiser M.J., Korber D.R., Greer C.W. Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl. Environ. Microbiol. 2012, 78:7626-7637.
47. Yli-Knuuttila H., Snall J., Kari K., Meurman J.H. Colonization of Lactobacillus rhamnosus GG in the oral cavity. Oral Microbiol. Immunol. 2006, 21:129-131.