Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis
Open accessAbstract
Despite increasing knowledge on phylogenetic composition of the human microbiome, our understanding of the in situ activities of the organisms in the community and their interactions with each other and with the environment remains limited. Characterizing gene expression profiles of the human microbiome is essential for linking the role of different members of the bacterial communities in health and disease. The oral microbiome is one of the most complex microbial communities in the human body and under certain circumstances, not completely understood, the healthy microbial community undergoes a transformation toward a pathogenic state that gives rise to periodontitis, a polymicrobial inflammatory disease. We report here the in situ genome-wide transcriptome of the subgingival microbiome in six periodontally healthy individuals and seven individuals with periodontitis. The overall picture of metabolic activities showed that iron acquisition, lipopolysaccharide synthesis and flagellar synthesis were major activities defining disease. Unexpectedly, the vast majority of virulence factors upregulated in subjects with periodontitis came from organisms that are not considered major periodontal pathogens. One of the organisms whose gene expression profile was characterized was the uncultured candidate division TM7, showing an upregulation of putative virulence factors in the diseased community. These data enhance understanding of the core activities that are characteristic of periodontal disease as well as the role that individual organisms in the subgingival community play in periodontitis.
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Application of transcriptomic approaches has proved extremely significant for delineating both microbial and host gene expression in the context of oral health and pathology.
“Application of transcriptomic approaches has proved extremely significant for delineating both microbial and host gene expression in the context of oral health and pathology.14, 68, 94”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [68]
Culture-independent methods have improved our understanding of microbial diversity in the oral cavity.
“Culture‐independent methods have improved our understanding of microbial diversity in the oral cavity.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [68]
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Cited by
Sorted by citations
Microbiota in health and diseases
Hou, K., Wu, Z.-X., Chen, X.-Y., Wang, J.-Q., Zhang, D., Xiao, C., Zhu, D., Koya, J. B., Wei, L., Li, J., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00974-4 · Cited by 3,171 · see citing works
“In periodontal disease, inflammation has been found to be an important driver for the growth of pathogenic microorganisms since inflammation can cause tissue destruction, which provides nutrient to microbiomes.(108) However, inflammation could subsequently trigger bactericidal activity of the immune system.”
BackgroundThe Oral Microbiota: Dynamic Communities and Host Interactions
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217 · see citing works
Species-level functional profiling of metagenomes and metatranscriptomes
Franzosa, E. A., McIver, L. J., Rahnavard, G., Thompson, L. R., Schirmer, M., Weingart, G., Lipson, K. S., Knight, R., Caporaso, J. G., Segata, N., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0176-y · Cited by 1,693 · see citing works
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
The role of the microbiota in periodontal disease
Curtis, M. A., Diaz, P. I., & Van Dyke, T. E. (2020) · Periodontology 2000 · doi:10.1111/prd.12296 · Cited by 698 · see citing works
Sequencing and beyond: integrating molecular 'omics' for microbial community profiling
Franzosa, E. A., Hsu, T. Y., Sirota‐Madi, A., Shafquat, A., Abu-Ali, G., Morgan, X. C., & Huttenhower, C. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3451 · Cited by 725 · see citing works
The role of inflammation and genetics in periodontal disease
Loos, B. G., & Dyke, T. E. V. (2020) · Periodontology 2000 · doi:10.1111/prd.12297 · Cited by 637 · see citing works
Polymicrobial synergy and dysbiosis in inflammatory disease
Lamont, R. J., & Hajishengallis, G. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.11.004 · Cited by 585 · see citing works
Current understanding of periodontal disease pathogenesis and targets for host‐modulation therapy
Hajishengallis, G., Chavakis, T., & Lambris, J. D. (2020) · Periodontology 2000 · doi:10.1111/prd.12331 · Cited by 513 · see citing works
Solving the etiology of dental caries
Simón‐Soro, Á., & Mira, Á. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.10.010 · Cited by 509 · see citing works
Metagenomics, Metatranscriptomics, and Metabolomics Approaches for Microbiome Analysis
Aguiar‐Pulido, V., Huang, W., Suárez-Ulloa, V., Cickovski, T., Mathee, K., & Narasimhan, G. (2016) · Evolutionary Bioinformatics · doi:10.4137/ebo.s36436 · Cited by 503 · see citing works
Lung microbiome: new insights into the pathogenesis of respiratory diseases
Li, R., Li, J., & Zhou, X. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01722-y · Cited by 466 · see citing works
“71,72 73 – 75 Speci fi cally, fungi and bacteria can produce bio fi lm structures that protect fungi and/or bacteria from dehydration, drugs, and immunocyte attack.”
BackgroundThe inflammophilic character of the periodontitis-associated microbiota
Hajishengallis, G. (2014) · Molecular Oral Microbiology · doi:10.1111/omi.12065 · Cited by 407 · see citing works
“Moreover, a plethora of virulence factors upregulated in the microbiome of periodontitis patients is primarily derived from species that are not traditionally considered as ‘periopathogens’ (Duran-Pinedo et al., 2014).”
Valm, A. M. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.016 · Cited by 425 · see citing works
“Supporting this hypothesis, periodontal pathobionts include organisms that require exogenous amino acids for growth in culture and a recent metatranscriptomic analysis of subgingival communities found enhanced expression of genes involved in iron-uptake in periodontitisassociated communities[18,88].”
BackgroundPeriodontal Disease: The Good, The Bad, and The Unknown
Sedghi, L. M., Bacino, M. S., & Kapila, Y. L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.766944 · Cited by 385 · see citing works
Current concepts in the pathogenesis of periodontitis: from symbiosis to dysbiosis
Abdulkareem, A. A., Al-Taweel, F. B. H., Al-Sharqi, A. J. B., Gul, S. S., Sha, A. M., & Chapple, I. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2023.2197779 · Cited by 402 · see citing works
“subgingival biofilms, which could further promote the inflammatory potential of the associated bacteria [136].”
BackgroundThe Oral Microbiome and Cancer
Irfan, M., Delgado, R. Z. R., & Frias-Lopez, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.591088 · Cited by 341 · see citing works
Self-citationA practical guide to the oral microbiome and its relation to health and disease
Krishnan, K., Chen, T., & Paster, B. (2017) · Oral Diseases · doi:10.1111/odi.12509 · Cited by 347 · see citing works
“…sequenced to identify changes in gene expression between disease and normal states to identify key pathways upregulated in disease and expression patterns of potential pathogenic factors and microbial diversity (Yost et al., 2015, Duran-Pinedo et al., 2014, Benitez-Paez et al., 2014) (Wade, 2011).”
BackgroundSelf-citationYost, S. C., Duran-Pinedo, A. E., Teles, R. P., Krishnan, K., & Frias‐Lopez, J. (2015) · Genome Medicine · doi:10.1186/s13073-015-0153-3 · Cited by 342 · see citing works
“Among the most active producers of putative virulence factors was Corynebacterium matruchotii [1], which has also been associated with periodontitis in microbiome studies.”
BackgroundResultInfluentialSelf-citationHajishengallis, G., & Lamont, R. J. (2021) · Periodontology 2000 · doi:10.1111/prd.12371 · Cited by 302 · see citing works
Role of microbial communities in the pathogenesis of periodontal diseases and caries
Mira, Á., Simón‐Soro, Á., & Curtis, M. A. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12671 · Cited by 283 · see citing works
“…that most upregulated virulence factors in periodontitis came from organisms which are generally not considered major periodontal pathogens (Duran-Pinedo et al. 2014b) in agreement with the idea that the whole microbial community could be providing the virulence output (Berezow & Darveau…”
BackgroundInfluentialRole of oral microbiome on oral cancers, a review
Gholizadeh, P., Eslami, H., Yousefi, M., Asgharzadeh, M., Aghazadeh, M. H., & Kafil, H. S. (2016) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2016.09.082 · Cited by 297 · see citing works
The lung mycobiome: an emerging field of the human respiratory microbiome
Nguyen, L. D. N., Viscogliosi, E., & Delhaes, L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00089 · Cited by 260 · see citing works
“Overall, information obtained from oral cavity and gastrointestinal ecosystems indicates that fungi influence bacterial behavior through different interactions (i.e., positive and negative influences between and among microbiome members; Duran-Pinedo et al., 2011, 2014; Iliev et al., 2012).”
BackgroundSharma, N., Bhatia, S., Sodhi, A. S., & Batra, N. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.42 · Cited by 263 · see citing works
A microbial perspective of human developmental biology
Charbonneau, M. R., Blanton, L. V., DiGiulio, D. B., Relman, D. A., Lebrilla, C. B., Mills, D. A., & Gordon, J. I. (2016) · Nature · doi:10.1038/nature18845 · Cited by 246 · see citing works
Microbial Community-Driven Etiopathogenesis of Peri-Implantitis
Belibasakis, G. N., & Manoil, D. (2021) · Journal of Dental Research · doi:10.1177/0022034520949851 · Cited by 244 · see citing works
“To further assess whether differences in virulence profiles could emerge between healthy and diseased conditions, the authors compared their data with reads from healthy periodontal sites retrieved from another RNA-seq experiment deposited at the Human Oral Microbiome Database (Duran-Pinedo et al. 2014).”
ResultHajishengallis, G., & Korostoff, J. M. (2017) · Periodontology 2000 · doi:10.1111/prd.12181 · Cited by 245 · see citing works
“Recent microbiome and mechanistic studies revealed that: (i) the periodontitis-associated microbiota is much more diverse and complex than traditionally thought; and (ii) its role in disease involves polymicrobial synergistic and dysbiotic interactions with the host (4, 49, 52, 90, 143).”
BackgroundDysbiosis in chronic periodontitis: Key microbial players and interactions with the human host
Deng, Z.-L., Szafrański, S. P., Jarek, M., Bhuju, S., & Wagner‐Döbler, I. (2017) · Scientific Reports · doi:10.1038/s41598-017-03804-8 · Cited by 229 · see citing works
Streptococcus Sanguinis Biofilm Formation & Interaction with Oral Pathogens
Zhu, B., Macleod, L. C., Kitten, T. O., & Xu, P. (2018) · Future Microbiology · doi:10.2217/fmb-2018-0043 · Cited by 228 · see citing works
The periodontal war: microbes and immunity
Ebersole, J. L., Dawson, D. R., Emecen‐Huja, P., Nagarajan, R., Howard, K., Grady, M. E., Thompson, K. L., Peyyala, R., Al‐Attar, A., Lethbridge, K., et al. (2017) · Periodontology 2000 · doi:10.1111/prd.12222 · Cited by 212 · see citing works
“sites with progressing periodontitis (140, 141) and by identifying gene expression changes in individual bacterial species that could enhance the dysbiotic disease process triggering destruction of the periodontal structures (248, 250, 251).”
BackgroundOral infections and cardiovascular disease
Kholy, K. E., Genco, R. J., & Dyke, T. E. V. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.03.001 · Cited by 201 · see citing works
The role of oral bacteria in inflammatory bowel disease
Read, E., Curtis, M. A., & Neves, J. F. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00488-4 · Cited by 198 · see citing works
Duran-Pinedo, A. E., & Frias-Lopez, J. (2015) · Microbes and Infection · doi:10.1016/j.micinf.2015.03.014 · Cited by 187 · see citing works
“Moreover, the phylogenetic profiles based on metatranscriptome analysis were more similar than those based on shotgun metagenome analysis [50].”
InfluentialResolvin E1 Reverses Experimental Periodontitis and Dysbiosis
Lee, C.-T., Teles, R. P., Kantarcı, A., Chen, T., McCafferty, J., Starr, J. R., Brito, L. C. N., Paster, B. J., & Dyke, T. E. V. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600859 · Cited by 173 · see citing works
“has been recently demonstrated in bacterial transcriptomic analyses that putative virulence factors are upregulated by bacteria (both putative pathogens and health-associated commensals) in progressing periodontitis sites (66, 67).”
BackgroundSelf-citationPro-resolving mediators in the regulation of periodontal disease
Dyke, T. E. V. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.04.006 · Cited by 169 · see citing works
“The analysis of the microbiome transcriptome revealed that virulence factors are upregulated by both presumed pathogens and also health associated commensals (73, 74).”
BackgroundMicrobial biofilms and the human skin microbiome
Brandwein, M., Steinberg, D., & Meshner, S. (2016) · npj Biofilms and Microbiomes · doi:10.1038/s41522-016-0004-z · Cited by 157 · see citing works
Chemokine Function in Periodontal Disease and Oral Cavity Cancer
Sahingur, S. E., & Yeudall, W. A. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00214 · Cited by 154 · see citing works
Subgingival Microbiome Shifts and Community Dynamics in Periodontal Diseases
Diaz, P. I., Hoare, A., & Hong, B. (2016) · Journal of the California Dental Association · doi:10.1080/19424396.2016.12221035 · Cited by 152 · see citing works
Belstrøm, D., Constancias, F., Liu, Y., Yang, L., Drautz‐Moses, D. I., Schuster, S. C., Kohli, G. S., Jakobsen, T. H., Holmstrup, P., & Givskov, M. (2017) · npj Biofilms and Microbiomes · doi:10.1038/s41522-017-0031-4 · Cited by 150 · see citing works
Linking microbiota to human diseases: a systems biology perspective
Wu, H., Tremaroli, V., & Bäckhed, F. (2015) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2015.09.011 · Cited by 150 · see citing works
“Interestingly, most of the virulence factors overexpressed in periodontitis belonged to bacteria that had not been previously linked to pathogenesis [99].”
BackgroundDe Filippis, F., Vannini, L., La Storia, A., Laghi, L., Piombino, P., Stellato, G., Serrazanetti, D. I., Gozzi, G., Turroni, S., Ferrocino, I., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112373 · Cited by 146 · see citing works
“study carried out on salivary microbiome revealed differences in microbial gene expression in case of oral disbyosis [8].”
BackgroundImmune and regulatory functions of neutrophils in inflammatory bone loss
Hajishengallis, G., Moutsopoulos, N. M., Hajishengallis, E., & Chavakis, T. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.02.002 · Cited by 146 · see citing works
Yost, S., Stashenko, P., Choi, Y., Kukuruzinska, M., Genco, C. A., Salama, A., Weinberg, E. O., Kramer, C. D., & Frias-Lopez, J. (2018) · International Journal of Oral Science · doi:10.1038/s41368-018-0037-7 · Cited by 144 · see citing works
Self-citationOffenbacher, S., Divaris, K., Barros, S. P., MOSS, K. L., Marchesan, J. T., Morelli, T., Zhang, S., Kim, S., Sun, L., Beck, J. D., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw069 · Cited by 143 · see citing works
“First, the six distinct microbial community structures that are associated with disease have microbial patterns that are consistent with previous studies that have performed 16s sequencing methods; including studies that employ multiple intraoral microbial sampling sites in each subject and among subjects with health,…”
ResultMetatranscriptomics for the Human Microbiome and Microbial Community Functional Profiling
Zhang, Y., Thompson, K. N., Branck, T. A., Yan, Y., Nguyen, L. H., Franzosa, E. A., & Huttenhower, C. (2021) · Annual Review of Biomedical Data Science · doi:10.1146/annurev-biodatasci-031121-103035 · Cited by 136 · see citing works
Dabdoub, S. M., Ganesan, S. M., & Kumar, P. (2016) · Scientific Reports · doi:10.1038/srep38993 · Cited by 131 · see citing works
Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
Nowicki, E. M., Shroff, R., Singleton, J. A., Renaud, D. E., Wallace, D. L., Drury, J., Zirnheld, J., Colleti, B., Ellington, A. D., Lamont, R. J., et al. (2018) · mBio · doi:10.1128/mbio.00575-18 · Cited by 124 · see citing works
“14, 18, 20) or metatranscriptome (15, 16, 21, 22) analyses to examine the functional potential of the oral microbiota in health and disease.”
BackgroundScannapieco, F. A., & Dongari‐Bagtzoglou, A. I. (2021) · Journal of Periodontology · doi:10.1002/jper.21-0120 · Cited by 125 · see citing works
Whiteson, K., Bailey, B., Bergkessel, M., Conrad, D., Delhaès, L., Felts, B., Harris, J. K., Hunter, R. C., Lim, Y. W., Maughan, H., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201312-2129pp · Cited by 122 · see citing works
Metatranscriptome of the Oral Microbiome in Health and Disease
Solbiati, J., & Frias‐Lopez, J. (2018) · Journal of Dental Research · doi:10.1177/0022034518761644 · Cited by 119 · see citing works
Self-citationAdverse effects of electronic cigarettes on the disease-naive oral microbiome
Ganesan, S. M., Dabdoub, S. M., Nagaraja, H. N., Scott, M. L., Pamulapati, S., Berman, M. L., Shields, P. G., Wewers, M. E., & Kumar, P. (2020) · Science Advances · doi:10.1126/sciadv.aaz0108 · Cited by 119 · see citing works
“Note that none of the 123 individuals in our study had periodontal disease, yet the functional signatures bore remarkable resemblance to those of individuals with periodontitis (28, 40), attesting to the risk for harm posed by e-cigarettes to the oral ecosystem.”
Szafrański, S. P., Wos‐Oxley, M. L., Vilchez‐Vargas, R., Jáuregui, R., Plumeier, I., Klawonn, F., Tomasch, J., Meisinger, C., Kühnisch, J., Sztajer, H., et al. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.03534-14 · Cited by 118 · see citing works
“As a next step, 556 metatranscriptomics (52,53) or other specialized analyses can then be applied to a smaller 557 number of representative samples.”
BackgroundUriarte, S. M., Edmisson, J. S., & Jimenez‐Flores, E. (2016) · Immunological Reviews · doi:10.1111/imr.12451 · Cited by 112 · see citing works
Macrophages in periodontitis: A dynamic shift between tissue destruction and repair
Yin, L., Li, X., & Hou, J. L. (2022) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2022.10.002 · Cited by 115 · see citing works
“Damage to the periodontal ligament and alveolar bone stems from the immune system, as it attempts to destroy the microbes that disrupt the normal symbiosis between the oral tissues and the oral microbial community [11,12].”
BackgroundAi, D., Huang, R., Wen, J., Li, C., Jiangping, Z., & Xia, L. C. (2017) · BMC Genomics · doi:10.1186/s12864-016-3254-5 · Cited by 110 · see citing works
“Availability of data and materials The two metagenomic datasets are all publicly available in the supplementary of their original publications [20, 21].”
BackgroundMethodAdvancements toward a systems level understanding of the human oral microbiome
McLean, J. S. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00098 · Cited by 108 · see citing works
“…the potential differences in expression between health and disease in caries (Peterson et al., 2013; Benitez-Paez et al., 2014), periodontal disease (Duran-Pinedo et al., 2014; Jorth et al., 2014) and defined mixed communities containing sequenced oral bacteria (Frias-Lopez and DuranPinedo, 2012).”
BackgroundUnderstanding human health through metatranscriptomics
Ojala, T., Kankuri, E. M., & Kankainen, M. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.02.002 · Cited by 107 · see citing works
Aleti, G., Baker, J. L., Tang, X., Alvarez, R., Dinis, M., Tran, N. C., Melnik, A. V., Zhong, C., Ernst, M., Dorrestein, P. C., et al. (2019) · mBio · doi:10.1128/mbio.00321-19 · Cited by 107 · see citing works
Bicalho, M. L. S., Machado, V. S., Higgins, C. H., de Lima, F. S., & Bicalho, R. C. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-12058 · Cited by 105 · see citing works
“…genes involved in resistance to fluoroquinolones, adaptation to d-cysteine (a powerful inhibitor of E. coli growth), and antibiotic resistance (β-lactamase), consistent with the expression of antibiotics as potential mechanisms of homeostasis in the healthy microbiota (Duran-Pinedo et al., 2014).”
BackgroundThe human oral metaproteome reveals potential biomarkers for caries disease
Belda‐Ferre, P., Williamson, J. C., Simón‐Soro, Á., Artacho, A., Jensen, O. N., & Mira, Á. (2015) · PROTEOMICS · doi:10.1002/pmic.201400600 · Cited by 104 · see citing works
“Meta-transcriptomic approaches have begun to be applied in in vitro oral models [12] and dental plaque samples [13, 14], but are limited by the short RNA half-life, the need to amplify and enrich the small mRNA fraction and the fraction of transcripts which are not translated.”
BackgroundIntra‐oral single‐site comparisons of periodontal and peri‐implant microbiota in health and disease
Yu, X., Chan, Y., Zhuang, L., Lai, H., Lang, N. P., Leung, W. K., & Watt, R. M. (2019) · Clinical Oral Implants Research · doi:10.1111/clr.13459 · Cited by 103 · see citing works
Post‐treatment supportive care for the natural dentition and dental implants
Armitage, G. C., & Xenoudi, P. (2016) · Periodontology 2000 · doi:10.1111/prd.12122 · Cited by 104 · see citing works
Determining Microbial Products and Identifying Molecular Targets in the Human Microbiome
Cordy, R. J., Yasuda, K., Shafquat, A., Morgan, X. C., & Huttenhower, C. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.10.003 · Cited by 100 · see citing works
Microbial Interactions in Oral Communities Mediate Emergent Biofilm Properties
Diaz, P. I., & Valm, A. M. (2019) · Journal of Dental Research · doi:10.1177/0022034519880157 · Cited by 100 · see citing works
“…in states of periodontal disease to include genes involved in iron uptake, among others, while longitudinal metatanscriptomic studies offer the possibility of identifying genes within communities that drive the transition from health to disease (Duran-Pinedo et al. 2014; Yost et al. 2015).”
BackgroundThe effect of the stress hormone cortisol on the metatranscriptome of the oral microbiome
Duran-Pinedo, A. E., Solbiati, J., & Frias-Lopez, J. (2018) · npj Biofilms and Microbiomes · doi:10.1038/s41522-018-0068-z · Cited by 96 · see citing works
“3a), which we have previously found associated with the progression of periodontal disease.(22,23) In the case of L.”
BackgroundMethodInfluentialSelf-citationFungal-bacterial interactions and their relevance to oral health: linking the clinic and the bench
Diaz, P. I., Strausbaugh, L. D., & Dongari‐Bagtzoglou, A. I. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00101 · Cited by 96 · see citing works
Galimanas, V. B., Hall, M., Singh, N., Lynch, M. D. J., Goldberg, M. B., Tenenbaum, H. C., Cvitkovitch, D. G., Neufeld, J. D., & Senadheera, D. B. (2014) · Microbiome · doi:10.1186/2049-2618-2-32 · Cited by 96 · see citing works
“Similar to the weak separation found in our findings, a recent metagenomic and metatran-scriptomic study of SubG and SupG plaque failed to find a strong separation between health and CP [33].”
Microbial transitions from health to disease
Joseph, S., & Curtis, M. A. (2021) · Periodontology 2000 · doi:10.1111/prd.12377 · Cited by 94 · see citing works
Koopman, J. E., van der Kaaij, N. C. W., Buijs, M. J., Elyassi, Y., van der Veen, M. H., Crielaard, W., ten Cate, J. M., & Zaura, E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137318 · Cited by 92 · see citing works
The tongue microbiome in healthy subjects and patients with intra-oral halitosis
Seerangaiyan, K., Winkelhoff, A. J. V., Harmsen, H. J. M., Rossen, J. W. A., & Winkel, E. G. (2017) · Journal of Breath Research · doi:10.1088/1752-7163/aa7c24 · Cited by 91 · see citing works
Sakanaka, A., Kuboniwa, M., Hashino, E., Bamba, T., Fukusaki, E., & Amano, A. (2017) · Scientific Reports · doi:10.1038/srep42818 · Cited by 90 · see citing works
Bor, B., McLean, J., Foster, K., Cen, L., To, T. T., Serrato-Guillen, A., Dewhirst, F., Shi, W.-Y., & He, X. (2018) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1810625115 · Cited by 87 · see citing works
Multi-omics tools for studying microbial biofilms: current perspectives and future directions
Seneviratne, C. J., Suriyanarayanan, T., Widyarman, A. S., Lee, L. S., Lau, M., Ching, J., Delaney, C., & Ramage, G. (2020) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2020.1828817 · Cited by 89 · see citing works
“Similarly, a study by Duran-Pinedo et al. (2014) conducted a metagenome and metatranscriptome analysis on the subgingival biofilm samples of patients with and without periodontitis.”
BackgroundImpact of systemic factors in shaping the periodontal microbiome
Teles, F., Wang, Y., Hajishengallis, G., Hastürk, H., & Marchesan, J. T. (2020) · Periodontology 2000 · doi:10.1111/prd.12356 · Cited by 89 · see citing works
Soro, V., Dutton, L. C., Sprague, S. V., Nobbs, A. H., Ireland, A. J., Sandy, J. R., Jepson, M. A., Micaroni, M., Splatt, P., Dymock, D., et al. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.01827-14 · Cited by 88 · see citing works
“However, this is not a prerequisite for TM7 detection, since metagenomic and microbiomic studies have increasingly reported detection of TM7 at a variety of sites, healthy as well as diseased (15, 18, 29).”
BackgroundChen, H., Liu, Y., Zhang, M. H., Wang, G., Qi, Z., Bridgewater, L. C., Zhao, L., Tang, Z., & Pang, X. (2015) · Scientific Reports · doi:10.1038/srep09053 · Cited by 90 · see citing works
Szafrański, S. P., Deng, Z.-L., Tomasch, J., Jarek, M., Bhuju, S., Meisinger, C., Kühnisch, J., Sztajer, H., & Wagner‐Döbler, I. (2015) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2015.17 · Cited by 86 · see citing works
The enduring importance of animal modelsin understanding periodontal disease
Hajishengallis, G., Lamont, R. J., & Graves, D. T. (2015) · Virulence · doi:10.4161/21505594.2014.990806 · Cited by 84 · see citing works
“Moreover, the commensal-turned-pathobiont concept is supported by a recent metatranscriptomic study, which revealed that a plethora of virulence factors upregulated in the microbiome of periodontitis patients is primarily derived from the previously underappreciated species that were not traditionally associated with…”
BackgroundThe impact of fixed orthodontic appliances on oral microbiome dynamics in Japanese patients
Kado, I., Hisatsune, J., Tsuruda, K., Tanimoto, K., & Sugai, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-78971-2 · Cited by 72 · see citing works
Dysbiosis From a Microbial and Host Perspective Relative to Oral Health and Disease
Cugini, C., Ramasubbu, N., Tsiagbe, V. K., & Fine, D. H. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.617485 · Cited by 86 · see citing works
Oral Microorganisms and Biofilms: New Insights to Defeat the Main Etiologic Factor of Oral Diseases
Bertolini, M., Costa, R. L. G. F. D. C., Barão, V. A. R., Villar, C. C., Retamal‐Valdes, B., Feres, M., & Souza, J. G. S. (2022) · Microorganisms · doi:10.3390/microorganisms10122413 · Cited by 91 · see citing works
Shiba, T., Watanabe, T., Kachi, H., Koyanagi, T., Maruyama, N., Murase, K., Takeuchi, Y., Maruyama, F., Izumi, Y., & Nakagawa, I. (2016) · Scientific Reports · doi:10.1038/srep30997 · Cited by 83 · see citing works
“In addition, differences in mRNA abundance between healthy and periodontitis sites have been reported for each microbial taxon and for functional and taxonomic profiles of virulence factors 20 .”
InfluentialThe Oral Mouse Microbiome Promotes Tumorigenesis in Oral Squamous Cell Carcinoma
Stashenko, P., Yost, S. C., Choi, Y., Danciu, T., Chen, T., Yoganathan, S., Kressirer, C. A., Ruiz-Tourrella, M., Das, B., Kokaras, A. S., et al. (2019) · mSystems · doi:10.1128/msystems.00323-19 · Cited by 80 · see citing works
“Other biological processes overrepresented were proteolysis, which has previously been linked to virulence in periodontal disease (24, 25), and anaerobic respiration, which may indicate a highly anaerobic environment in the OSCC site (Fig.”
BackgroundSelf-citationThe role of oral microbiome in periodontitis under diabetes mellitus
Qin, H., Li, G.-Y., Xu, X.-H., Zhang, C., Zhong, W., Xu, S., Yin, Y.-Y., & Song, J.-L. (2022) · Journal of Oral Microbiology · doi:10.1080/20002297.2022.2078031 · Cited by 80 · see citing works
“Consistently, a community-wide transcriptomic study on periodontitis-associated subgingival microbiome has indicated elevated expression of proteolysis-related genes, genes for peptide transport and acquisition of iron, as well as the genes associated with synthesis of lipopolysaccharides that would enhance the proinf…”
BackgroundWang, Q., Ma, J., Wang, B., Zhang, X., Yin, Y., & Bai, H. (2019) · American Journal of Orthodontics and Dentofacial Orthopedics · doi:10.1016/j.ajodo.2018.11.017 · Cited by 80 · see citing works
Profiling of Oral Bacterial Communities
Wade, W. G., & Prosdocimi, E. M. (2020) · Journal of Dental Research · doi:10.1177/0022034520914594 · Cited by 80 · see citing works
“…been developed to investigate microbial function including metagenomics, which describes the functional genetic potential within samples (Alcaraz et al. 2012), and metatranscriptomics, which investigates the genes being actively transcribed at sites at particular times (Duran-Pinedo et al. 2014).”
BackgroundEcological Therapeutic Opportunities for Oral Diseases
Hoare, A., Marsh, P. D., & Diaz, P. I. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.bad-0006-2016 · Cited by 81 · see citing works
“Such metabolic models may allow prediction of the role that each species may have in the health- and/or disease-associated consortia (5, 276, 277, 278).”
BackgroundEnvironmental factors and periodontal microbiome
Buduneli, N. (2020) · Periodontology 2000 · doi:10.1111/prd.12355 · Cited by 80 · see citing works
Huang, S. W., He, T., Yue, F., Xu, X., Wang, L., Zhu, P., Teng, F., Sun, Z., Liu, X., Jing, G., et al. (2021) · mBio · doi:10.1128/mbio.03281-20 · Cited by 76 · see citing works
Defining functional signatures of dysbiosis in periodontitis progression
Wang, G. P. (2015) · Genome Medicine · doi:10.1186/s13073-015-0165-z · Cited by 73 · see citing works
“In another study, Duran-Pinedo and colleagues [8] compared the subgingival in situ genome-wide transcriptome of periodontally healthy and diseased individuals.”
Complement Involvement in Periodontitis: Molecular Mechanisms and Rational Therapeutic Approaches
Hajishengallis, G., Maekawa, T., Abe, T., Hajishengallis, E., & Lambris, J. D. (2015) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-18603-0_4 · Cited by 73 · see citing works
“These recent human microbiome analyses and animal modelbased mechanistic studies collectively suggest that the pathogenesis of periodontitis involves polymicrobial synergy and dysbiosis [ 2 , 34 , 36 , 37 , 40 – 49 ].”
BackgroundPozhitkov, A. E., Leroux, B. G., Randolph, T. W., Beikler, T., Flemmig, T. F., & Noble, P. A. (2015) · BMC Oral Health · doi:10.1186/s12903-015-0109-4 · Cited by 72 · see citing works
“Another study indicated that not only the oral microbial species were drastically different between periodontal health and disease but also their gene expression [48].”
BackgroundPapapanou, P., Park, H., Cheng, B., Kokaras, A., Paster, B., Burkett, S., Watson, C., Annavajhala, M., Uhlemann, A., & Noble, J. (2020) · The Journal of Periodontology · doi:10.1002/jper.20-0194 · Cited by 46 · see citing works
Did Omics change periodontal therapy?
Feres, M., Retamal‐Valdes, B., Gonçalves, C., Figueiredo, L. C., & Teles, F. (2020) · Periodontology 2000 · doi:10.1111/prd.12358 · Cited by 67 · see citing works
Natural products as mediators of disease
Garg, N., Luzzatto‐Knaan, T., Melnik, A. V., Caraballo‐Rodríguez, A. M., Floros, D. J., Petras, D., Gregor, R., Dorrestein, P. C., & Phelan, V. V. (2016) · Natural Product Reports · doi:10.1039/c6np00063k · Cited by 68 · see citing works
The Oral Microbiome Bank of China
Xian, P., Zhou, X., Xu, X., Yuqing, L., Li, Y., Li, J., Su, X., Huang, S., Xu, J., & Liao, G. (2018) · International Journal of Oral Science · doi:10.1038/s41368-018-0018-x · Cited by 65 · see citing works
“The new concept of the "oral core microbiome" suggests that this phenomenon should be personalised in accordance with the ecological characteristics of the oral environment in certain populations at different ages or grades of disease.(15,16,39,73) By monitoring the dynamic changes in the structure and function of mic…”
Changes in the oral ecosystem induced by the use of 8% arginine toothpaste
Koopman, J. E., Hoogenkamp, M. A., Buijs, M. J., Brandt, B. W., Keijser, B. J. F., Crielaard, W., ten Cate, J. M., & Zaura, E. (2016) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2016.09.008 · Cited by 64 · see citing works
Ikeda, E., Shiba, T., Ikeda, Y., Suda, W., Nakasato, A., Takeuchi, Y., Azuma, M., Hattori, M., & Izumi, Y. (2019) · Odontology : official journal of The Society of the Nippon Dental University · doi:10.1007/s10266-019-00452-4 · Cited by 55 · see citing works
“Metagenomic/metatranscriptomic analyses of subgingival dental plaque also showed the alteration of functions in diseased microbiota, and genes responsible for functions, such as bacterial motility, energy metabolism, and biosynthesis of lipopolysaccharides and nucleotide, were found to be over-represented in periodont…”
BackgroundMaintaining a protective state for human periodontal tissue
Yamamoto, M., & Aizawa, R. (2021) · Periodontology 2000 · doi:10.1111/prd.12367 · Cited by 65 · see citing works
Komatsu, K., Shiba, T., Takeuchi, Y., Watanabe, T., Koyanagi, T., Nemoto, T., Shimogishi, M., Shibasaki, M., Katagiri, S., Kasugai, S., et al. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596490 · Cited by 62 · see citing works
“Although this comparative analysis has been applied in some periodontitis studies (Duran-Pinedo et al., 2014; Belstrom et al., 2017), metagenomic analysis has not been conducted on the periimplantitis microbial community before.”
Result
- Authors
- Duran-Pinedo, A. E., Chen, T., Teles, R., Starr, J. R., Wang, X., Krishnan, K., & Frias-Lopez, J.
- Affiliations
- The Forsyth Institute (US)
- Harvard University (US)
- Department of Microbiology, Forsyth Institute , Cambridge, MA, USA
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-03-06
- Volume
- 8
- Issue
- 8
- Pages
- 1659-1672
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC4817619
- OpenAlex
- W2080580603
- Cited by
- 327
- References
- 92
- Citations by year
- 2026: 15 · 2025: 19 · 2024: 17 · 2023: 21 · 2022: 36 · 2021: 42 · 2020: 38 · 2019: 26 · 2018: 25 · 2017: 28 · 2016: 21 · 2015: 26 · 2014: 12
- FWCI
- 38.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The ISME Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Dental and Craniofacial Research (DE021127, U01DE021127, DE021553, R01DE021553)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- periodontitis, oral microbiota, subgingival microbiota, microbial gene expression, virulence factors, iron acquisition, lipopolysaccharide biosynthesis, flagellar synthesis, polymicrobial disease, microbial interactions
- MeSH terms
- Adult, Bacteria, Humans, Periodontitis, Phylogeny, Virulence Factors, Metagenome, Transcriptome, Microbiota
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