Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis

ISME Journal

Volumn 8, Issue 8, 2014, Pages 1659-1672

  Duran Pinedo, Ana E ^a   Chen, Tsute ^a,b   Teles, Ricardo ^a,b   Starr, Jacqueline R ^a,b   Wang, Xiaoshan ^a,b   Krishnan, Keerthana ^a   Frias Lopez, Jorge ^a,b  

^a FORSYTH INSTITUTE   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

metagenome; metatranscriptome; oral microbiome; uncultured bacteria; virulence factors

Indexed keywords

TRANSCRIPTOME; VIRULENCE FACTOR;

ADULT; BACTERIUM; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; METAGENOME; MICROBIOLOGY; MICROFLORA; PERIODONTITIS; PHYLOGENY;

ADULT; BACTERIA; HUMANS; METAGENOME; MICROBIOTA; PERIODONTITIS; PHYLOGENY; TRANSCRIPTOME; VIRULENCE FACTORS;

EID: 84904993698     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.23     Document Type: Article

References (91)

1. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, Romero H, Simón-Soro A, Pignatelli M et al. (2012). The oral metagenome in health and disease. ISME J 6: 46-56.
2. Bender MH, Weiser JN. (2006). The atypical amino-terminal LPNTG-containing domain of the pneumococcal human IgA1-specific protease is required for proper enzyme localization and function. Mol Microbiol 61: 526-543.
3. Berezow AB, Darveau RP. (2011). Microbial shift and periodontitis. Periodontol 2000 55: 36-47.
4. Booijink CCGM, Boekhorst J, Zoetendal EG, Smidt H, Kleerebezem M, de Vos WM. (2010). Metatranscrip-tome analysis of the human fecal microbiota reveals subject-specific expression profiles, with genes encoding proteins involved in carbohydrate metabolism being dominantly expressed. Appl Environ Microbiol 76: 5533-5540.
5. Boughton WH. (1982). Rapid detection in spinal fluid of beta-lactamase produced by ampicillin-resistant Hae-mophilus influenzae. J Clin Microbiol 15: 1167-1168.
6. Brinig MM, Lepp PW, Ouverney CC, Armitage GC, Relman DA. (2003). Prevalence of bacteria of division TM7 in human subgingival plaque and their association with disease. Appl Environ Microbiol 69: 1687-1694.
7. Brochu V, Grenier D, Nakayama K, Mayrand D. (2001). Acquisition of iron from human transferrin by Porphy-romonas gingivalis: a role for Arg-and Lys-gingipain activities. Oral Microbiol Immunol 16: 79-87.
8. Brook I. (1986). Presence of beta-lactamase-producing bacteria and beta-lactamase activity in abscesses. Am J Clin Pathol 86: 97-101.
9. Brook I. (2009). The role of beta-lactamase-producing-bacteria in mixed infections. BMC Infect Dis 9: 202.
10. Brown CT, Davis-Richardson AG, Giongo A, Gano KA, Crabb DB, Mukherjee N et al. (2011). Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS One 6: e25792.
11. Bryant RE, Rashad AL, Mazza JA, Hammond D. (1980). Beta-lactamase activity in human pus. J Infect Dis 142: 594-601.
12. Bullon P, Cordero MD, Quiles JL, Ramirez-Tortosa MDC, Gonzalez-Alonso A, Alfonsi S et al. (2012). Autophagy in periodontitis patients and gingival fibroblasts: unraveling the link between chronic diseases and inflammation. BMC Med 10: 122.
13. Casarin RCV, Barbagallo A, Meulman T, Santos VR, Sallum EA, Nociti FH et al. (2013). Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J Periodont Res 48: 30-36.
14. Chaudhuri S, Gantner BN, Ye RD, Cianciotto NP, Freitag NE. (2013). The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity. MBio 4: e00617-12.
15. Chen L, Xiong Z, Sun L, Yang J, Jin Q. (2012). VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40: D641-D645.
16. Chen T, Yu W-H, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. (2010). The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010: baq013.
17. Colombo APV, Boches SK, Cotton SL, Goodson JM, Kent R, Haffajee AD et al. (2009). Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J Periodontol 80: 1421-1432.
18. Cossart P, Pizarro-Cerdá J, Lecuit M. (2003). Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol 13: 23-31.
19. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu W-H et al. (2010). The human oral microbiome. J Bacteriol 192: 5002-5017.
20. Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ. (2012). Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res 91: 914-920.
21. Enersen M, Nakano K, Amano A. (2013). Porphyromonas gingivalis fimbriae. J Oral Microbiol 5: 20265-20275.
22. Fives-Taylor PM, Meyer DH, Mintz KP, Brissette C. (1999). Virulence factors of Actinobacillus actinomycetemco-mitans. Periodontol 2000 20: 136-167.
23. Frederiksen RF, Paspaliari DK, Larsen T, Storgaard BG, Larsen MH, Ingmer H et al. (2013). Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology (Reading, Engl) 159: 833-847.
24. Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW et al. (2008). Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805-3810.
25. Giannoukos G, Ciulla DM, Huang K, Haas BJ, Izard J, Levin JZ et al. (2012). Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol 13: R23.
26. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ et al. (2008). High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435.
27. Goulhen F, Hafezi A, Uitto VJ, Hinode D, Nakamura R, Grenier D et al. (1998). Subcellular localization and cytotoxic activity of the GroEL-like protein isolated from Actinobacillus actinomycetemcomitans. Infect Immun 66: 5307-5313.
28. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang Z K et al. (2012). Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6: 1176-1185.
29. Gross EL, Leys EJ, Gasparovich SR, Firestone ND, Schwartzbaum JA, Janies DA et al. (2010). Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48: 4121-4128.
30. Haffajee AD, Socransky SS, Patel MR, Song X. (2008). Microbial complexes in supragingival plaque. Oral Microbiol Immunol 23: 196-205.
31. Handal T, Olsen I, Walker CB, Caugant DA. (2004). Beta-lactamase production and antimicrobial susceptibility of subgingival bacteria from refractory periodontitis. Oral Microbiol Immunol 19: 303-308.
32. Herbert MA, Beveridge CJE, Saunders NJ. (2004). Bacterial virulence factors in neonatal sepsis: group B streptococcus. Curr Opin Infect Dis 17: 225-229.
33. Hiroi M, Shimojima T, Kashimata M, Miyata T, Takano H, Takahama M et al. (1998). Inhibition by Porphyromonas gingivalis LPS of apoptosis induction in human peripheral blood polymorphonuclear leukocytes. Anticancer Res 18: 3475-3479.
34. Ho Sui SJ, Fedynak A, Hsiao WWL, Langille MGI, Brinkman FSL. (2009). The association of virulence factors with genomic islands. PLoS One 4: e8094.
35. Hoeijmakers WAM, Bártfai R, Françoijs K-J, Stunnenberg HG. (2011). Linear amplification for deep sequencing. Nat Protoc 6: 1026-1036.
36. Holt SC, Ebersole JL. (2005). Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the 'red complex', a prototype polybacterial pathogenic consortium in periodontitis. Periodontology 2000 38: 72-122.
37. Honma K, Mishima E, Sharma A. (2011). Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun 79: 393-401.
38. Imamura T. (2003). The role of gingipains in the pathogenesis of periodontal disease. J Periodontol 74: 111-118.
39. Inagaki S, Onishi S, Kuramitsu HK, Sharma A. (2006). Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by 'Tannerella forsythia'. Infect. Immun 74: 5023-5028.
40. Jain S, Darveau RP. (2010). Contribution of Porphyromo-nas gingivalis lipopolysaccharide to periodontitis. Periodontol 2000 54: 53-70.
41. Jedrzejas MJ. (2001). Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev 65: 187-207.
42. Kim Y-H, Lee S-Y. (2013). Prevalence of putative period-ontopahogen TM7 and dialister in dental plaque of Koreans. Int J Oral Biol 38: 55-59.
43. Kindt R, Coe R. (2005). Tree Diversity Analysis. A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies. World Agrofor-estry Centre (ICRAF): Nairobi, Kenya. http://www. worldagroforestry.org/ treesandmarkets/tree-diversity-analysis.asp.
44. Kitten T, Kinscherf TG, McEvoy JL, Willis DK. (1998). A newly identified regulator is required for virulence and toxin production in Pseudomonas syringae. Mol Microbiol 28: 917-929.
45. Kolenbrander PE. (2000). Oral microbial communities: biofilms, interactions, and genetic systems. Ann Rev Microbiol 54: 413-437.
46. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJJ. (2002). Communication among oral bacteria. Microbiol Mol Biol Rev 66: 486-505.
47. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ. (2003). New bacterial species associated with chronic periodontitis. J Dental Res 82: 338-344.
48. Larsen MH, Leisner JJ, Ingmer H. (2010). The chitinolytic activity of Listeria monocytogenes EGD is regulated by carbohydrates but also by the virulence regulator PrfA. Appl Environ Microbiol 76: 6470-6476.
49. Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P. (1997). Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65: 5309-5319.
50. Legendre P, Gallagher ED. (2001). Ecologically meaningful transformations for ordination of species data. Oeco-logia 129: 271-280.
51. Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA. (2004). Methanogenic Archaea and human periodontal disease. Proc Natl Acad Sci USA 101: 6176-6181.
52. Liu B, Faller LL, Klitgord N, Mazumdar V, Ghodsi M, Sommer DD et al. (2012). Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 7: e37919.
53. Lux R, Miller JN, Park NH, Shi W. (2001). Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola. Infect Immun 69: 6276-6283.
54. Marcy Y, Ouverney C, Bik EM, Lösekann T, Ivanova N, Martin HG et al. (2007). Dissecting biological 'dark matter' with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci. USA 104: 11889-11894.
55. Marsh PD. (2006). Dental plaque as a biofilm and a microbial community-implications for health and disease. BMC Oral Health 6(Suppl 1): S14.
56. McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR et al. (2010). Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA 107: 16420-16427.
57. Mishima E, Sharma A. (2011). Tannerella forsythia invasion in oral epithelial cells requires phosphoino-sitide 3-kinase activation and clathrin-mediated endo-cytosis. Microbiology (Reading, Engl) 157: 2382-2391.
58. Murray DA, Wilton JMA. (2003). Lipopolysaccharide from the periodontal pathogen Porphyromonas gingivalis prevents apoptosis of HL60-derived neutrophils in vitro. Infect Immun 71: 7232-7235.
59. Nairz M, Schroll A, Sonnweber T, Weiss G. (2010). The struggle for iron-a metal at the host-pathogen interface. Cell Microbiol 12: 1691-1702.
60. Ouverney CC, Armitage GC, Relman DA. (2003). Single-cell enumeration of an uncultivated TM7 subgroup in the human subgingival crevice. Appl Environ Microbiol 69: 6294-6298.
61. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA et al. (2001). Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770-3783.
62. Peterson SN, Snesrud E, Liu J, Ong AC, Kilian M, Schork NJ et al. (2013). The dental plaque microbiome in health and disease. PLoS One 8: e58487.
63. Podar M, Abulencia CB, Walcher M, Hutchison D, Zengler K, Garcia JA et al. (2007). Targeted access to the genomes of low-abundance organisms in complex microbial communities. Appl Environ. Microbiol 73: 3205-3214.
64. Poroyko V, White JR, Wang M, Donovan S, Alverdy J, Liu DC et al. (2010). Gut Microbial Gene Expression in Mother-Fed and Formula-Fed Piglets. PLoS One 5: e12459.
65. Preshaw PM, Schifferle RE, Walters JD. (1999). Porphy-romonas gingivalis lipopolysaccharide delays human polymorphonuclear leukocyte apoptosis in vitro. J Periodont Res 34: 197-202.
66. Quinlan AR, Hall IM. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
67. Ramette A. (2007). Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142-160.
68. Rams TE, Degener JE, van Winkelhoff AJ. (2012). Prevalence of b-lactamase-producing bacteria in human periodontitis. J Periodont Res 48: 493-499.
69. Relman DA. (2012). The human microbiome: ecosystem resilience and health. Nutr Rev 70(Suppl 1): S2-S9.
70. Rhodes ER, Menke S, Shoemaker C, Tomaras AP, McGillivary G, Actis LA. (2007). Iron acquisition in the dental pathogen Actinobacillus actinomycetemcomitans: what does it use as a source and how does it get this essential metal? Biometals 20: 365-377.
71. Rodrigues PH, Progulske-Fox A. (2005). Gene expression profile analysis of Porphyromonas gingivalis during invasion of human coronary artery endothelial cells. Infect Immun 73: 6169-6173.
72. Rudney JD, Chen R, Sedgewick GJ. (2005). Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells. J Dent Res 84: 59-63.
73. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D et al. (2012). Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 13: R42.
74. Siqueira JF Jr, Rôças IN, Souto R, de Uzeda M, Colombo AP. (2000). Checkerboard DNA-DNA hybridization analysis of endodontic infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 89: 744-748.
75. Slots J. (2010). Human viruses in periodontitis. Periodontol 2000 53: 89-110.
76. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RLJ. (1998). Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144.
77. Soneson C, Delorenzi M. (2013). A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics 14: 91.
78. Supek F, Bosnjak M, Skunca N, Smuc T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6: e21800.
79. Tang-Larsen J, Claesson R, Edlund MB, Carlsson J. (1995). Competition for peptides and amino acids among periodontal bacteria. J Periodont Res 30: 390-395.
80. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. (2011). Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213-2223.
81. Teles F, Haffajee AD, Socransky SS. (2007). Multiple displacement amplification as an aid in checkerboard DNA-DNA hybridization. Oral Microbiol Immunol 22: 118-125.
82. Thomas RZ, Zijnge V, Ciçek A, de Soet JJ, Harmsen HJM, Huysmans MCDNJM. (2012). Shifts in the microbial population in relation to in situ caries progression. Caries Res 46: 427-431.
83. Van Winkelhoff AJ, Winkel EG, Barendregt D, Dellemijn-Kippuw N, Stijne A, van der Velden U. (1997). beta-Lactamase producing bacteria in adult periodontitis. J Clin Periodontol 24: 538-543.
84. Wang C-H, Lin C-Y, Luo Y-H, Tsai P-J, Lin Y-S, Lin MTet al. (2005). Effects of oligopeptide permease in group a streptococcal infection. Infect Immun 73: 2881-2890.
85. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL et al. (2013). PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42: 581-591.
86. Wright HJ, Chapple ILC, Matthews JB, Cooper PR. (2011). Fusobacterium nucleatum regulation of neutrophil transcription. J Periodont Res 46: 1-12.
87. Xia Q, Wang T, Taub F, Park Y, Capestany CA, Lamont RJ et al. (2007). Quantitative proteomics of intracellular Porphyromonas gingivalis. Proteomics 7: 4323-4337.
88. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. (2000). Comparison of the microbiota of supra-and subgingival plaque in health and periodontitis. J Clin Periodontol 27: 648-657.
89. Xiong X, Frank DN, Robertson CE, Hung SS, Markle J, Canty AJ et al. (2012). Generation and Analysis of a Mouse Intestinal Metatranscriptome through Illumina Based RNA-Sequencing. PLoS One 7: e36009.
90. Young MD, Wakefield MJ, Smyth GK, Oshlack A. (2010). Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11: R14.
91. Yuan L, Rodrigues PH, Bélanger M, Dunn W Jr, Progulske-Fox A. (2007). The Porphyromonas gingi-valis clpB gene is involved in cellular invasion in vitro and virulence in vivo. FEMS Immunol Med Microbiol 51: 388-398.