The root canal microbiome diversity and function. A whole-metagenome shotgun analysis.
apical periodontitis
microbiome
toxins
virulence factors
whole-genome sequencing
Journal
International endodontic journal
ISSN: 1365-2591
Titre abrégé: Int Endod J
Pays: England
ID NLM: 8004996
Informations de publication
Date de publication:
02 Mar 2023
02 Mar 2023
Historique:
revised:
23
02
2023
received:
22
12
2022
accepted:
25
02
2023
pubmed:
3
3
2023
medline:
3
3
2023
entrez:
2
3
2023
Statut:
aheadofprint
Résumé
To evaluate the root canal microbiome composition and bacterial functional capability in cases of primary and secondary apical periodontitis utilizing whole-metagenome shotgun sequencing. Twenty-two samples from patients with primary root canal infections, and 18 samples obtained from previously treated teeth currently diagnosed with apical periodontitis were analysed with whole-metagenome shotgun sequencing at a depth of 20 M reads. Taxonomic and functional gene annotations were made using MetaPhlAn3 and HUMAnN3 software. The Shannon and Chao1 indices were utilized to measure alpha diversity. Differences in community composition were evaluated utilizing analysis of similarity (ANOSIM) using Bray-Curtis dissimilarities. The Wilcoxon rank sum test was used to compare differences in taxa and functional genes. Microbial community variations within a community were significantly lower in secondary relative to primary infections (alpha diversity p = .001). Community composition was significantly different in primary versus secondary infection (R = .11, p = .005). The predominant taxa observed among samples (>2.5%) were Pseudopropionibacterium propionicum, Prevotella oris, Eubacterium infirmum, Tannerella forsythia, Atopobium rimae, Peptostreptococcus stomatis, Bacteroidetes bacterium oral taxon 272, Parvimonas micra, Olsenella profusa, Streptococcus anginosus, Lactobacillus rhamnosus, Porphyromonas endodontalis, Pseudoramibacter alactolyticus, Fusobacterium nucleatum, Eubacterium brachy and Solobacterium moorei. The Wilcoxon rank test revealed no significant differences in relative abundances of functional genes in both groups. Genes with greater relative abundances (top 25) were associated with genetic, signalling and cellular processes including the iron and peptide/nickel transport system. Numerous genes encoding toxins were identified: exfoliative toxin, haemolysins, thiol-activated cytolysin, phospholipase C, cAMP factor, sialidase, and hyaluronic glucosaminidase. Despite taxonomic differences between primary and secondary apical periodontitis, the functional capability of the microbiomes was similar.
Types de publication
Journal Article
Langues
eng
Subventions
Organisme : NCATS NIH HHS
ID : UL1-TR002494
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1-TR002494
Pays : United States
Informations de copyright
© 2023 The Authors. International Endodontic Journal published by John Wiley & Sons Ltd on behalf of British Endodontic Society.
Références
Akhtar, A. & Turner, D. (2022) The role of bacterial ATP-binding cassette (ABC) transporters in pathogenesis and virulence: therapeutic and vaccine potential. Microbial Pathogenesis, 171, 105734.
Araki, H., Kuriyama, T., Nakagawa, K. & Karasawa, T. (2004) The microbial synergy of Peptostreptococcus micros and Prevotella intermedia in a murine abscess model. Oral Microbiology and Immunology, 19, 177-181.
Beghini, F., McIver, L., Blanco-Míguez, A., Dubois, L., Asnicar, F., Maharjan, S. et al. (2021) Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. eLife, 10, e65088.
Bukowski, M., Wladyka, B. & Dubin, G. (2010) Exfoliative toxins of Staphylococcus aureus. Toxins, 2, 1148-1165.
Carlsson, J., Larsen, J.T. & Edlund, M.B. (1993) Peptostreptococcus micros has a uniquely high capacity to form hydrogen sulfide from glutathione. Oral Microbiology and Immunology, 8, 42-45.
Casadevall, A. & Pirofski, L.A. (2009) Virulence factors and their mechanisms of action: the view from a damage-response framework. Journal of Water and Health, 7, S2-S18.
Chavez de Paz, L. (2002) Fusobacterium nucleatum in endodontic flare-ups. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology, 93, 179-183.
Clarke, K.R. (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 117-143.
Costalonga, M. & Herzberg, M.C. (2014) The oral microbiome and the immunobiology of periodontal disease and caries. Immunology Letters, 162, 22-38.
Dabdoub, S.M., Ganesan, S.M. & Kumar, P.S. (2016) Comparative metagenomics reveals taxonomically idiosyncratic yet functionally congruent communities in periodontitis. Scientific Reports, 6, 38993.
Dahlen, G., Basic, A. & Bylund, J. (2019) Importance of virulence factors for the persistence of oral bacteria in the inflamed gingival crevice and in the pathogenesis of periodontal disease. Journal of Clinical Medicine, 8, 1339.
Damé-Teixeira, N., Parolo, C., Maltz, M., Rup, A., Devine, D. & Do, T. (2018) Gene expression of bacterial collagenolytic proteases in root caries. Journal of Oral Microbiology, 10, 1424475.
Dixon, D.R. & Darveau, R.P. (2005) Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. Journal of Dental Research, 84, 584-595.
Duran-Pinedo, A., Chen, T., Teles, R., Starr, J., Wang, X., Krishnan, K. et al. (2014) Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME Journal, 8, 1659-1672.
Falace, D.A., Reid, K. & Rayens, M.K. (1996) The influence of deep (odontogenic) pain intensity, quality, and duration on the incidence and characteristics of referred orofacial pain. Journal of Orofacial Pain, 10, 232-239.
Foo, L.H., Balan, P., Pang, L.M., Laine, M. & Seneviratne, J. (2021) Role of the oral microbiome, metabolic pathways, and novel diagnostic tools in intra-oral halitosis: a comprehensive update. Critical Reviews in Microbiology, 47, 359-375.
Fujii, R., Saito, Y., Tokura, Y., Nakagawa, K.I., Okuda, K. & Ishihara, K. (2009) Characterization of bacterial flora in persistent apical periodontitis lesions. Oral Microbiology and Immunology, 24, 502-505.
Georgiades, K. & Raoult, D. (2011) Comparative genomics evidence that only protein toxins are tagging bad bugs. Frontiers in Cellular and Infection Microbiology, 1, 1-9.
Golub, L.M., Siegel, K., Ramamurthy, N.S. & Mandel, I.D. (1976) Some characteristics of collagenase activity in gingival crevicular fluid and its relationship to gingival diseases in humans. Journal of Dental Research, 55, 1049-1057.
Gomes, B.P., Endo, M.S. & Martinho, F.C. (2012) Comparison of endotoxin levels found in primary and secondary endodontic infections. Journal of Endodontics, 38, 1082-1086.
Graves, D.T., Oates, T. & Garlet, G.P. (2011) Review of osteoimmunology and the host response in endodontic and periodontal lesions. Journal of Oral Microbiology, 3, 5304.
Grenier, D. & Dang La, V. (2011) Proteases of Porphyromonas gingivalis as important virulence factors in periodontal disease and potential targets for plant-derived compounds: a review article. Current Drug Targets, 12, 322-331.
Hajishengallis, G. & Lamont, R. (2016) Dancing with the stars: how choreographed bacterial interactions dictate nososymbiocity and give rise to keystone pathogens, accessory pathogens, and pathobionts. Trends in Microbiology, 24, 477-489.
Han, Y.W., Shi, W., Huang, G.T., Kinder Haake, S., Park, N.H., Kuramitsu, H. et al. (2000) Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infection and Immunity, 68, 3140-3146.
Henderson, B., Poole, S. & Wilson, M. (1996) Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis. Microbiological Reviews, 60, 316-341.
Higashi, D.L., McGuire, S., Abdelrahman, Y.M., Zou, Z., Qin, H., Anderson, D. et al. (2022) Development of the first tractable genetic system for Parvimonas micra, a ubiquitous pathobiont in human dysbiotic disease. Microbiology Spectrum, 10, e0046522.
Hillman, B., Al-Ghalith, G., Shields-Cutler, R., Zhu, Q., Gohl, D., Beckman, K. et al. (2018) Evaluating the information content of shallow shotgun metagenomics. mSystems, 3, e00069-00018.
Horiuchi, A., Kokubu, E., Warita, T. & Ishihara, K. (2020) Synergistic biofilm formation by Parvimonas micra and Fusobacterium nucleatum. Anaerobe, 62, 102100.
Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y. & Morishima, K. (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Research, 45, D353-D361.
Kaplan, A., Kaplan, C.W., He, X., McHardy, I., Shi, W. & Lux, R. (2014) Characterization of aid1, a novel gene involved in Fusobacterium nucleatum interspecies interactions. Microbial Ecology, 68, 379-387.
Kaplan, C.W., Lux, R., Haake, S.K. & Shi, W. (2009) The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Molecular Microbiology, 71, 35-47.
Kaplan, C.W., Ma, X., Paranjpe, A., Jewett, A., Lux, R., Kinder-Haake, S. et al. (2010) Fusobacterium nucleatum outer membrane proteins Fap2 and RadD induce cell death in human lymphocytes. Infection and Immunity, 78, 4773-4778.
Kato, T., Takahashi, N. & Kuramitsu, H.K. (1992) Sequence analysis and characterization of the Porphyromonas gingivalis prtC gene, which expresses a novel collagenase activity. Journal of Bacteriology, 174, 3889-3895.
Kawasaki, T. & Kawai, T. (2014) Toll-like receptor signaling pathways. Frontiers in Immunology, 5, 461.
Kelly, B.J., Gross, R., Bittinger, K., Sherrill-Mix, S., Lewis, J.D., Collman, R.G. et al. (2015) Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA. Bioinformatics, 31, 2461-2468.
Knight, R., Vrbanac, A., Taylor, B.C., Aksenov, A., Callewaert, C., Debelius, J. et al. (2018) Best practices for analyzing microbiomes. Nature Reviews Microbiology, 16, 410-422.
Kolenbrander, P.E., Palmer, R., Rickard, A., Jakubovics, N., Chalmers, N. & Diaz, P. (2006) Bacterial interactions and successions during plaque development. Periodontology 2000, 42, 47-79.
Kumar, P.S. (2021) Microbiomics: were we all wrong before? Periodontology 2000, 2021(85), 8-11.
Leung, K.P. & Folk, S.P. (2002) Effects of porphyrins and inorganic iron on the growth of Prevotella intermedia. FEMS Microbiology Letters, 209, 15-21.
Lima, B.P., Shi, W. & Lux, R. (2017) Identification and characterization of a novel Fusobacterium nucleatum adhesin involved in physical interaction and biofilm formation with Streptococcus gordonii. Microbiology, 6, e00444.
Melville, S. & Craig, L. (2013) Type IV pili in Gram-positive bacteria. Microbiology and Molecular Biology Reviews, 77, 323-341.
Neilands, J. (1981) Iron absorption and transport in microorganisms. Annual Review of Nutrition, 1, 27-46.
Neilands, J., Davies, J., Bikker, F. & Svensater, G. (2019) Parvimonas micra stimulates expression of gingipains from Porphyromonas gingivalis in multi-species communities. Anaerobe, 55, 54-60.
Olczak, T., Simpson, W., Liu, X. & Genco, C.A. (2005) Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiology Review, 29, 119-144.
Ordinola-Zapata, R., Costalonga, M., Nixdorf, D., Dietz, M., Schuweiler, D., Lima, B.P. et al. (2023) Taxonomic abundance in primary and secondary root canal infections. International Endodontic Journal, 56, 278-288.
Park, S.R., Kim, D.J., Han, S.H., Kang, M.J., Lee, J.Y., Jeong, Y.J. et al. (2014) Diverse toll-like receptors mediate cytokine production by Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans in macrophages. Infection and Immunity, 82, 1914-1920.
Popoff, M. (2014) Clostridial pore-forming toxins: powerful virulence factors. Anaerobe, 30, 220-238.
Rangarajan, M., Aduse-Opoku, J., Paramonov, N.A., Hashim, A. & Curtis, M.A. (2017) Hemin binding by Porphyromonas gingivalis strains is dependent on the presence of A-LPS. Molecular Oral Microbiology, 32, 365-374.
Rudney, J.D., Chen, R. & Sedgewick, G.J. (2005) Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells. Journal of Dental Research, 84, 59-63.
Schloss, P.D. (2020) Reintroducing mothur: 10 years later. Applied and Environmental Microbiology, 86, e02343-e02319.
Siqueira, J.F. & Roças, I.N. (2007) Bacterial pathogenesis and mediators in apical periodontitis. Brazilian Dental Journal, 18, 267-280.
Siqueira, J.F. & Roças, I.N. (2009) The microbiota of acute apical abscesses. Journal of Dental Research, 88, 61-65.
Siqueira, J.F. & Roças, I.N. (2013) As-yet-uncultivated oral bacteria: breadth and association with oral and extra-oral diseases. Journal of Oral Microbiology, 5, 21077.
Siqueira, J.F., Jr. & Rôças, I.N. (2022) A critical analysis of research methods and experimental models to study the root canal microbiome. International Endodontic Journal, 55, 46-71.
Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. & Kent, R.L. (1988) Microbial complexes in subgingival plaque. Journal of Clinical Periodontology, 25, 134-144.
Steimle, A., Autenrieth, I. & Frick, J.S. (2016) Structure and function: lipid a modifications in commensals and pathogens. International Journal of Medical Microbiology, 306, 290-301.
The Human Microbiome Project Consortium. (2012) Structure, function and diversity of the healthy human microbiome. Nature, 486, 207-214.
Tian, L., Wang, X.W., Wu, A.K., Fan, Y., Friedman, J., Dahlin, A. et al. (2020) Deciphering functional redundancy in the human microbiome. Nature Communications, 11, 6217.
Tibúrcio-Machado, C.S., Michelon, C., Zanatta, F.B., Gomes, M.S., Marin, J.A. & Bier, C.A. (2021) The global prevalence of apical periodontitis: a systematic review and meta-analysis. International Endodontic Journal, 54, 712-735.
Tribble, G. & Lamont, R. (2010) Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontology 2000, 52, 68-83.
van Dalen, P.J., van Deutekom-Mulder, E.C., de Graaff, J. & van Steenbergen, T.J. (1998) Pathogenicity of Peptostreptococcus micros morphotypes and Prevotella species in pure and mixed culture. Journal of Medical Microbiology, 47, 135-140.
Vincents, B., Guentsch, A., Kostolowska, D., von Pawel-Ramingen, U., Eick, S., Potempa, J. et al. (2011) Cleavage of IgG1 and IgG3 by gingipain K from Porphyromonas gingivalis may compromise host defense in progressive periodontitis. The FASEB Journal, 25, 3741-3750.
von Schillde, M.A., Hormannsperger, G., Weiher, M., Alpert, C.A., Hahne, H., Bauerl, C. et al. (2012) Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host & Microbe, 11, 387-396.
Watanabe, T., Hara, Y., Yoshimi, Y., Fujita, Y., Yokoe, M. & Noguchi, Y. (2020) Clinical characteristics of bloodstream infection by Parvimonas micra: retrospective case series and literature review. BMC Infectious Diseases, 20, 578.