Functional signatures of oral dysbiosis during periodontitis progression revealed by microbial metatranscriptome analysis

Genome Medicine

Volumn 7, Issue 1, 2015, Pages

  Yost, Susan ^a   Duran Pinedo, Ana E ^a   Teles, Ricardo ^c   Krishnan, Keerthana ^a   Frias Lopez, Jorge ^a,b  

^a FORSYTH INSTITUTE   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; COBALAMIN; CRISPR ASSOCIATED PROTEIN; HEMOLYSIN; IRON; LIPID A; PEPTIDASE; POTASSIUM; PROTEINASE; RECEPTOR; TRANSCRIPTOME; VIRULENCE FACTOR;

ADULT; AGED; AMINO ACID TRANSPORT; ARTICLE; BIOFILM; BIOSYNTHESIS; CELL MOTILITY; CLINICAL ARTICLE; CLINICAL TRIAL; DATA BASE; DISEASE COURSE; DYSBIOSIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENETIC TRAIT; GENOME ANALYSIS; GINGIVA; HUMAN; IRON TRANSPORT; METAGENOME; MICROBIAL COMMUNITY; MICROBIOME; MOUTH CAVITY; MULTICENTER STUDY; NEXT GENERATION SEQUENCING; ORTHOLOGY; PERIODONTAL DISEASE; PERIODONTITIS; PHYLOGENY; PORPHYROMONAS GINGIVALIS; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PSEUDOMONAS FLUORESCENS; RNA EXTRACTION; STREPTOCOCCUS MITIS; STREPTOCOCCUS MUTANS; STREPTOCOCCUS ORALIS; TANNERELLA FORSYTHIA; UPREGULATION; VEILLONELLA PARVULA; VIRULENCE;

EID: 84928560423     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-015-0153-3     Document Type: Article

References (99)

1. Duran-Pinedo AE, Chen T, Teles R, Starr JR, Wang X, Krishnan K, et al. Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME J. 2014;8:1659-72.
2. Hajishengallis G. The inflammophilic character of the periodontitis-associated microbiota. Mol Oral Microbiol. 2014;29:248-57.
3. Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJL, Marcenes W. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res. 2014;93:1045-53.
4. Brown LJ, Johns BA, Wall TP. The economics of periodontal diseases. Periodontol 2000. 2002;29:223-34.
5. Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res. 201291:914-20.
6. Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K. Relationship between periodontal infections and systemic disease. Clin Microbiol Infect. 2007;13:3-10.
7. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RLJ. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134-44.
8. Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000. 2005;38:72-122.
9. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000. 2005;38:135-87.
10. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013;7:1016-25.
11. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK, et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 2012;6:1176-85.
12. Goodson JM, Tanner AC, Haffajee AD, Sornberger GC, Socransky SS. Patterns of progression and regression of advanced destructive periodontal disease. J Clin Periodontol. 1982;9:472-81.
13. Heitz-Mayfield LJA. Disease progression: identification of high-risk groups and individuals for periodontitis. J Clin Periodontol. 2005;32:196-209.
14. Ricci M, Garoia F, Tabarroni C, Marchisio O, Barone A, Genovesi A, et al. Association between genetic risk score and periodontitis onset and progression: a pilot study. Arch Oral Biol. 2011;56:1499-505.
15. Eley BM, Cox SW. A 2-year longitudinal study of elastase in human gingival crevicular fluid and periodontal attachment loss. J Clin Periodontol. 1996;23:681-92.
16. Eley BM, Cox SW. The relationship between gingival crevicular fluid cathepsin B activity and periodontal attachment loss in chronic periodontitis patients: a 2-year longitudinal study. J Periodontal Res. 1996;31:381-92.
17. Khalaf H, Lönn J, Bengtsson T. Cytokines and chemokines are differentially expressed in patients with periodontitis: possible role for TGF-β1 as a marker for disease progression. Cytokine. 2014;67:29-35.
18. Persson GR, Matuliené G, Ramseier CA, Persson RE, Tonetti MS, Lang NP. Influence of interleukin-1 gene polymorphism on the outcome of supportive periodontal therapy explored by a multi-factorial periodontal risk assessment model (PRA). Oral Health Prev Dent. 2003;1:17-27.
19. Charalampakis G, Dahlén G, Carlén A, Leonhardt A. Bacterial markers vs. clinical markers to predict progression of chronic periodontitis: a 2-yr prospective observational study. Eur J Oral Sci. 2013;121:394-402.
20. Byrne SJ, Dashper SG, Darby IB, Adams GG, Hoffmann B, Reynolds EC. Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol Immunol. 2009;24:469-77.
21. Haffajee AD, Socransky SS. Attachment level changes in destructive periodontal diseases. J Clin Periodontol. 1986;13:461-75.
22. Haffajee AD, Socransky SS, Smith C, Dibart S. Microbial risk indicators for periodontal attachment loss. J Periodontal Res. 1991;26:293-6.
23. Dzink JL, Socransky SS, Haffajee AD. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol. 1988;15:316-23.
24. Hart SN, Therneau TM, Zhang Y, Poland GA, Kocher J-P. Calculating sample size estimates for RNA sequencing data. J Comput Biol. 2013;20:970-8.
25. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078-9.
26. The Human Oral Microbiome Database. [ http://www.homd.org/ ]
27. PATRIC. Pathosystems Resource Integration Center. [ www.patricbrc.org/portal/portal/patric/Home ]
28. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 2014;42:D581-91.
29. J. Craig Venter Institute. [ www.jcvi.org ]
30. NCBI FTP site for Viral Genomes. [ ftp://ftp.ncbi.nlm.nih.gov/genomes/Viruses/ ]
31. FASTX-Toolkit. FASTQ/A short-reads pre-processing tools. [ hannonlab.cshl.edu/fastx_toolkit/ ]
32. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-2.
33. Lindner MS, Renard BY. Metagenomic abundance estimation and diagnostic testing on species level. Nucleic Acids Res. 2013;41:e10.
34. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
35. Soneson C, Delorenzi M. A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics. 2013;14:91.
36. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011;21:2213-23.
37. The Gene Ontology Consortium. [ http://www.geneontology.org/ ]
38. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008;36:3420-35.
39. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11:R14.
40. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6:e21800.
41. Virulence Factors of Pathogenic Bacteria Database. [ http://www.mgc.ac.cn/VFs/ ]
42. Ho Sui SJ, Fedynak A, Hsiao WWL, Langille MGI, Brinkman FSL. The association of virulence factors with genomic islands. PLoS One. 2009;4:e8094.
43. Chen L, Xiong Z, Sun L, Yang J, Jin Q. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res. 2012;40:D641-5.
44. González I, Cao K-AL, Davis MJ, Déjean S. Visualising associations between paired "omics" data sets. BioData Min. 2012;5:19.
45. Liquet B, Lê Cao K-A, Hocini H, Thiébaut R. A novel approach for biomarker selection and the integration of repeated measures experiments from two assays. BMC Bioinformatics. 2012;13:325.
46. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics. 2011;27:431-2.
47. Slots J. Human viruses in periodontitis. Periodontol 2000. 2010;53:89-110.
48. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, White RA, et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J. 2012;6:915-26.
49. Chen T, Yu W-H, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database J Biol Databases Curation. 2010;2010:baq013.
50. Peterson SN, Meissner T, Su AI, Snesrud E, Ong AC, Schork NJ, et al. Functional expression of dental plaque microbiota. Front Cell Infect Microbiol. 2014;4:108.
51. Benítez-Páez A, Belda-Ferre P, Simón-Soro A, Mira A. Microbiota diversity and gene expression dynamics in human oral biofilms. BMC Genomics. 2014;15:311.
52. Jorth P, Turner KH, Gumus P, Nizam N, Buduneli N, Whiteley M. Metatranscriptomics of the human oral microbiome during health and disease. mBio. 2014;5:e01012-4.
53. Haffajee AD, Socransky SS, Patel MR, Song X. Microbial complexes in supragingival plaque. Oral Microbiol Immunol. 2008;23:196-205.
54. Kumar PS, Mason MR, Brooker MR, O'Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol. 2012;39:425-33.
55. Colombo APV, Boches SK, Cotton SL, Goodson JM, Kent R, Haffajee AD, et al. Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J Periodontol. 2009;80:1421-32.
56. Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA. Methanogenic Archaea and human periodontal disease. Proc Natl Acad Sci U S A. 2004;101:6176-81.
57. Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe. 2011;10:497-506.
58. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012;10:717-25.
59. Aruni W, Chioma O, Fletcher HM. Filifactor alocis: The newly discovered kid on the block with special talents. J Dent Res. 2014;93:725-32.
60. Schlafer S, Riep B, Griffen AL, Petrich A, Hübner J, Berning M, et al. Filifactor alocis - involvement in periodontal biofilms. BMC Microbiol. 2010;10:66.
61. Haffajee AD, Teles RP, Socransky SS. Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. Oral Microbiol Immunol. 2006;21:269-82.
62. Pöllänen MT, Paino A, Ihalin R. Environmental stimuli shape biofilm formation and the virulence of periodontal pathogens. Int J Mol Sci. 2013;14:17221-37.
63. Fives-Taylor PM, Meyer DH, Mintz KP, Brissette C. Virulence factors of Actinobacillus actinomycetemcomitans. Periodontol 2000. 1999;20:136-67.
64. Jain S, Darveau RP. Contribution of Porphyromonas gingivalis lipopolysaccharide to periodontitis. Periodontol 2000. 2010;54:53-70.
65. Murray DA, Wilton JMA. Lipopolysaccharide from the periodontal pathogen Porphyromonas gingivalis prevents apoptosis of HL60-derived neutrophils in vitro. Infect Immun. 2003;71:7232-5.
66. Hiroi M, Shimojima T, Kashimata M, Miyata T, Takano H, Takahama M, et al. Inhibition by Porphyromonas gingivalis LPS of apoptosis induction in human peripheral blood polymorphonuclear leukocytes. Anticancer Res. 1998;18:3475-9.
67. Preshaw PM, Schifferle RE, Walters JD. Porphyromonas gingivalis lipopolysaccharide delays human polymorphonuclear leukocyte apoptosis in vitro. J Periodontal Res. 1999;34:197-202.
68. Tang-Larsen J, Claesson R, Edlund MB, Carlsson J. Competition for peptides and amino acids among periodontal bacteria. J Periodontal Res. 1995;30:390-5.
69. Yoshida A, Yoshimura M, Ohara N, Yoshimura S, Nagashima S, Takehara T, et al. Hydrogen sulfide production from cysteine and homocysteine by periodontal and oral bacteria. J Periodontol. 2009;80:1845-51.
70. Gries CM, Bose JL, Nuxoll AS, Fey PD, Bayles KW. The Ktr potassium transport system in Staphylococcus aureus and its role in cell physiology, antimicrobial resistance and pathogenesis. Mol Microbiol. 2013;89:760-73.
71. Liu Y, Ho KK, Su J, Gong H, Chang AC, Lu S. Potassium transport of Salmonella is important for type III secretion and pathogenesis. Microbiology. 2013;159:1705-19.
72. Front E, Laster Z, Unis R, Gavish M, Nagler RM. Salivary biomarker analysis complementing regular clinical examination. Biomark Med. 2013;7:701-8.
73. Koregol AC, More SP, Nainegali S, Kalburgi N, Verma S. Analysis of inorganic ions in gingival crevicular fluid as indicators of periodontal disease activity: A clinico-biochemical study. Contemp Clin Dent. 2011;2:278-82.
74. Wyckoff EE, Boulette ML, Payne SM. Genetics and environmental regulation of Shigella iron transport systems. Biometals. 2009;22:43-51.
75. Llamas MA, Imperi F, Visca P, Lamont IL. Cell-surface signaling in Pseudomonas: stress responses, iron transport, and pathogenicity. FEMS Microbiol Rev. 2014;38:569-97.
76. Heuston S, Begley M, Gahan CGM, Hill C. Isoprenoid biosynthesis in bacterial pathogens. Microbiology. 2012;158:1389-401.
77. Ostrovsky D, Diomina G, Lysak E, Matveeva E, Ogrel O, Trutko S. Effect of oxidative stress on the biosynthesis of 2-C-methyl-D-erythritol-2,4-cyclopyrophosphate and isoprenoids by several bacterial strains. Arch Microbiol. 1998;171:69-72.
78. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355-9.
79. Heinzerling HF, Olivares M, Burne RA. Genetic and transcriptional analysis of flgB flagellar operon constituents in the oral spirochete Treponema denticola and their heterologous expression in enteric bacteria. Infect Immun. 1997;65:2041-51.
80. Lux R, Miller JN, Park NH, Shi W. Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola. Infect Immun. 2001;69:6276-83.
81. Van Winkelhoff AJ, Winkel EG, Barendregt D, Dellemijn-Kippuw N, Stijne A, van der Velden U. beta-Lactamase producing bacteria in adult periodontitis. J Clin Periodontol. 1997;24:538-43.
82. Brook I. The role of beta-lactamase-producing-bacteria in mixed infections. BMC Infect Dis. 2009;9:202.
83. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes. Science. 2007;315:1709-12.
84. Louwen R, Staals RHJ, Endtz HP, van Baarlen P, van der Oost J. The role of CRISPR-Cas systems in virulence of pathogenic bacteria. Microbiol Mol Biol Rev. 2014;78:74-88.
85. Endo A, Watanabe T, Ogata N, Nozawa T, Aikawa C, Arakawa S, et al. Comparative genome analysis and identification of competitive and cooperative interactions in a polymicrobial disease. ISME J. 2015;9:629-42.
86. Naito M, Sato K, Shoji M, Yukitake H, Ogura Y, Hayashi T, et al. Characterization of the Porphyromonas gingivalis conjugative transposon CTnPg1: determination of the integration site and the genes essential for conjugal transfer. Microbiology. 2011;157:2022-32.
87. Tribble GD, Garza JJ, Yeung VL, Rigney TW, Dao D-HV, Rodrigues PH, et al. Genetic analysis of mobile tetQ elements in oral Prevotella species. Anaerobe. 2010;16:604-9.
88. Nikolich MP, Hong G, Shoemaker NB, Salyers AA. Evidence for natural horizontal transfer of tetQ between bacteria that normally colonize humans and bacteria that normally colonize livestock. Appl Environ Microbiol. 1994;60:3255-60.
89. Arzese AR, Tomasetig L, Botta GA. Detection of tetQ and ermF antibiotic resistance genes in Prevotella and Porphyromonas isolates from clinical specimens and resident microbiota of humans. J Antimicrob Chemother. 2000;45:577-82.
90. Berezow AB, Darveau RP. Microbial shift and periodontitis. Periodontol 2000. 2011;55:36-47.
91. Relman DA. The human microbiome: ecosystem resilience and health. Nutr Rev. 2012;70:S2-9.
92. López R, Dahlén G, Retamales C, Baelum V. Clustering of subgingival microbial species in adolescents with' periodontitis. Eur J Oral Sci. 2011;119:141-50.
93. Mulcahy LR, Burns JL, Lory S, Lewis K. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol. 2010;192:6191-9.
94. Ciofu O, Hansen CR, Høiby N. Respiratory bacterial infections in cystic fibrosis. Curr Opin Pulm Med. 2013;19:251-8.
95. Armitage GC. Analysis of gingival crevice fluid and risk of progression of periodontitis. Periodontol 2000. 2004;34:109-19.
96. Kadowaki T, Nakayama K, Okamoto K, Abe N, Baba A, Shi Y, et al. Porphyromonas gingivalis proteinases as virulence determinants in progression of periodontal diseases. J Biochem (Tokyo). 2000;128:153-9.
97. Roper JM, Raux E, Brindley AA, Schubert HL, Gharbia SE, Shah HN, et al. The enigma of cobalamin (Vitamin B12) biosynthesis in Porphyromonas gingivalis identification and characterization of a functional corrin pathway. J Biol Chem. 2000;275:40316-23.
98. Datasets used in these analyses was deposited at the Human Oral Microbiome Database (HOMD) under the submission number 20141024. [ ftp://ftp.homd.org/publication_data/20141024/ ]
99. Datasets used in these analyses was deposited at the Human Oral Microbiome Database (HOMD) under the submission number 20130522. [ ftp://ftp.homd.org/publication_data/20130522/ ]