Comparative analysis of oral treponemes associated with periodontal health and disease

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  You, Meng ^a,b   Mo, Sisu ^a   Leung, W Keung ^a   Watt, Rory M ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Bacterial etiology; Bacterial phylogeny; Clinical study; Dentistry; Operational Taxonomic Unit; Oral microbiota; Oral treponeme; Periodontitis; Phylogroup; Treponema

Indexed keywords

RNA 16S;

ADOLESCENT; ADULT; AGED; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM DETECTION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DENTAL HEALTH; DISEASE ASSOCIATION; FEMALE; GENE SEQUENCE; HEALTH STATUS; HUMAN; MALE; MICROBIAL DIVERSITY; MOLECULAR LIBRARY; MOLECULAR PHYLOGENY; MOUTH FLORA; MOUTH PLAQUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIODONTITIS; PLASMID; POPULATION ABUNDANCE; SPECIES COMPOSITION; SPECIES RICHNESS; TAXONOMY; TREPONEMA DENTICOLA;

ADULT; CASE-CONTROL STUDIES; CLONE CELLS; DENTAL PLAQUE; FEMALE; GENE LIBRARY; GINGIVA; HUMANS; MALE; MIDDLE AGED; PERIODONTITIS; PHYLOGENY; RNA, RIBOSOMAL, 16S; TREPONEMA; TREPONEMAL INFECTIONS;

EID: 84875958883     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-174     Document Type: Article

References (68)

1. Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev 2001, 14(4):727-752. 10.1128/CMR.14.4.727-752.2001, 89001, 11585783.
2. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 2010, 8(7):481-490. 10.1038/nrmicro2337, 20514045.
3. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005, 366(9499):1809-1820. 10.1016/S0140-6736(05)67728-8, 16298220.
4. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2005, 38:135-187.
5. Rylev M, Kilian M. Prevalence and distribution of principal periodontal pathogens worldwide. J Clin Periodontol 2008, 35(8 Suppl):346-361.
6. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol 1998, 25(2):134-144. 10.1111/j.1600-051X.1998.tb02419.x, 9495612.
7. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE. Bacterial diversity in human subgingival plaque. J Bacteriol 2001, 183(12):3770-3783. 10.1128/JB.183.12.3770-3783.2001, 95255, 11371542.
8. Simonson LG, Goodman CH, Bial JJ, Morton HE. Quantitative relationship of Treponema denticola to severity of periodontal disease. Infect Immun 1988, 56(4):726-728. 259361, 3346072.
9. Loesche WJ, Syed SA, Schmidt E, Morrison EC. Bacterial profiles of subgingival plaques in periodontitis. J Periodontol 1985, 56(8):447-456. 10.1902/jop.1985.56.8.447, 3869648.
10. Loesche WJ. The role of spirochetes in periodontal disease. Adv Dent Res 1988, 2(2):275-283.
11. Ellen RP, Galimanas VB. Spirochetes at the forefront of periodontal infections. Periodontol 2005, 38:13-32.
12. Armitage GC, Dickinson WR, Jenderseck RS, Levine SM, Chambers DW. Relationship between the percentage of subgingival spirochetes and the severity of periodontal disease. J Periodontol 1982, 53(9):550-556. 10.1902/jop.1982.53.9.550, 6957592.
13. Dewhirst FE, Tamer MA, Ericson RE, Lau CN, Levanos VA, Boches SK, Galvin JL, Paster BJ. The diversity of periodontal spirochetes by 16S rRNA analysis. Oral Microbiol Immun 2000, 15(3):196-202.
14. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG. The human oral microbiome. J Bacteriol 2010, 192(19):5002-5017. 10.1128/JB.00542-10, 2944498, 20656903.
15. Radolf JD, Lukehart SA. Pathogenic Treponema: molecular and cellular biology 2006, 9-18. Wymondham: Caister Academic, Ch. 1.
16. Moter A, Hoenig C, Choi BK, Riep B, Gobel UB. Molecular epidemiology of oral treponemes associated with periodontal disease. J Clin Microbiol 1998, 36(5):1399-1403. 104836, 9574713.
17. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK, Podar M, Leys EJ. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 2012, 6(6):1176-1185. 10.1038/ismej.2011.191, 22170420.
18. Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the " red complex" , a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2005, 38:72-122.
19. Sela MN. Role of Treponema denticola in periodontal diseases. Crit Rev Oral Biol Med 2001, 12(5):399-413. 10.1177/10454411010120050301, 12002822.
20. Dashper SG, Seers CA, Tan KH, Reynolds EC. Virulence factors of the oral spirochete Treponema denticola. J Dent Res 2011, 90(6):691-703. 10.1177/0022034510385242, 3144123, 20940357.
21. Ishihara K. Virulence factors of Treponema denticola. Periodontol 2010, 54(1):117-135.
22. Takeuchi Y, Umeda M, Sakamoto M, Benno Y, Huang Y, Ishikawa I. Treponema socranskii, Treponema denticola, and Porphyromonas gingivalis are associated with severity of periodontal tissue destruction. J Periodontol 2001, 72(10):1354-1363. 10.1902/jop.2001.72.10.1354, 11699477.
23. Choi BK, Paster BJ, Dewhirst FE, Gobel UB. Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infect Immun 1994, 62(5):1889-1895. 186432, 8168954.
24. Hampp EG, Scott DB, Wyckoff RW. Morphologic characteristics of certain cultured strains of oral spirochetes and Treponema pallidum as revealed by the electron microscope. J Bacteriol 1948, 56(6):755-769. 518649, 16561628.
25. Klein HS. What role do Treponema vincenti play in certain diseases of the gingiva?. Acta Odontol Scand 1946, 7:92-96. 10.3109/00016354609040426, 20989512.
26. Umemoto T, Nakazawa F, Hoshino E, Okada K, Fukunaga M, Namikawa I. Treponema medium sp. nov., isolated from human subgingival dental plaque. Int J Syst Bacteriol 1997, 47(1):67-72. 10.1099/00207713-47-1-67, 8995804.
27. Chan EC, Siboo R, Keng T, Psarra N, Hurley R, Cheng SL, Iugovaz I. Treponema denticola (ex Brumpt 1925) sp. nov., nom. rev., and identification of new spirochete isolates from periodontal pockets. Int J Syst Bacteriol 1993, 43(2):196-203. 10.1099/00207713-43-2-196, 8494734.
28. Wyss C, Moter A, Choi BK, Dewhirst FE, Xue Y, Schupbach P, Gobel UB, Paster BJ, Guggenheim B. Treponema putidum sp. nov., a medium-sized proteolytic spirochaete isolated from lesions of human periodontitis and acute necrotizing ulcerative gingivitis. Int J Syst Evol Microbiol 2004, 54(Pt 4):1117-1122.
29. Wyss C, Choi BK, Schupbach P, Guggenheim B, Gobel UB. Treponema maltophilum sp. nov., a small oral spirochete isolated from human periodontal lesions. Int J Syst Bacteriol 1996, 46(3):745-752. 10.1099/00207713-46-3-745, 8782684.
30. Wyss C, Choi BK, Schupbach P, Moter A, Guggenheim B, Gobel UB. Treponema lecithinolyticum sp. nov., a small saccharolytic spirochaete with phospholipase A and C activities associated with periodontal diseases. Int J Syst Bacteriol 1999, 49(Pt 4):1329-1339.
31. Wyss C, Choi BK, Schupbach P, Guggenheim B, Gobel UB. Treponema amylovorum sp. nov., a saccharolytic spirochete of medium size isolated from an advanced human periodontal lesion. Int J Syst Bacteriol 1997, 47(3):842-845. 10.1099/00207713-47-3-842, 9226916.
32. Smibert RM, Johnson JL, Ranney RR. Treponema socranskii sp. nov., Treponema socranskii subsp. socranskii subsp. nov., Treponema socranskii subsp. buccale subsp. nov., and Treponema socranskii subsp. paredis subsp. nov. Isolated from the Human Periodontia. Int J Syst Bacteriol 1984, 34(4):457-462.
33. Paster BJ, Dewhirst FE, Coleman BC, Lau CN, Ericson RL. Phylogenetic analysis of cultivable oral treponemes from the Smibert collection. Int J Syst Bacteriol 1998, 48(Pt 3):713-722.
34. Wyss C, Dewhirst FE, Gmur R, Thurnheer T, Xue Y, Schupbach P, Guggenheim B, Paster BJ. Treponema parvum sp nov., a small, glucuronic or galacturonic acid-dependent oral spirochaete from lesions of human periodontitis and acute necrotizing ulcerative gingivitis. Int J Syst Evol Microbiol 2001, 51:955-962. 10.1099/00207713-51-3-955, 11411720.
35. Smibert RM, Burmeister JA. Treponema pectinovorum sp. nov. Isolated from Humans with Periodontitis. Int J Syst Bacteriol 1983, 33(4):852-856.
36. Seshadri R, Myers GS, Tettelin H, Eisen JA, Heidelberg JF, Dodson RJ, Davidsen TM, DeBoy RT, Fouts DE, Haft DH. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 2004, 101(15):5646-5651. 10.1073/pnas.0307639101, 397461, 15064399.
37. Evans NJ, Brown JM, Demirkan I, Murray RD, Birtles RJ, Hart CA, Carter SD. Treponema pedis sp. nov., a spirochaete isolated from bovine digital dermatitis lesions. Int J Syst Evol Microbiol 2009, 59(Pt 5):987-991.
38. Ficarra G, Carlos R. Syphilis: the renaissance of an old disease with oral implications. Head Neck Pathol 2009, 3(3):195-206. 10.1007/s12105-009-0127-0, 2811633, 20596972.
39. You M, Mo S, Watt RM, Leung WK. Prevalence and diversity of Synergistetes taxa in periodontal health and disease. J Periodontal Res 2013, 48(2):159-168. 10.1111/j.1600-0765.2012.01516.x, 22881378.
40. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, 75(23):7537-7541. 10.1128/AEM.01541-09, 2786419, 19801464.
41. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35(21):7188-7196. 10.1093/nar/gkm864, 2175337, 17947321.
42. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267. 10.1128/AEM.00062-07, 1950982, 17586664.
43. Schloss PD, Westcott SL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 2011, 77(10):3219-3226. 10.1128/AEM.02810-10, 3126452, 21421784.
44. Chen T, Yu WH, 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 (Oxford) 2010, 2010. Article ID baq013.
45. Posada D. JModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25(7):1253-1256. 10.1093/molbev/msn083, 18397919.
46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
47. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574. 10.1093/bioinformatics/btg180, 12912839.
48. Wickham H. ggplot2: elegant graphics for data analysis 2009, New York: Springer-Verlag, 978-0-387-98140-6.
49. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005, 71(12):8228-8235. 10.1128/AEM.71.12.8228-8235.2005, 1317376, 16332807.
50. Schloss PD, Larget BR, Handelsman J. Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 2004, 70(9):5485-5492. 10.1128/AEM.70.9.5485-5492.2004, 520927, 15345436.
51. Singleton DR, Furlong MA, Rathbun SL, Whitman WB. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 2001, 67(9):4374-4376. 10.1128/AEM.67.9.4374-4376.2001, 93175, 11526051.
52. Lozupone C, Hamady M, Knight R. UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinforma 2006, 7:371.
53. Schloss PD, Handelsman J. Introducing TreeClimber, a test to compare microbial community structures. Appl Environ Microbiol 2006, 72(4):2379-2384. 10.1128/AEM.72.4.2379-2384.2006, 1449046, 16597933.
54. Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, ten Cate JM, Crielaard W. Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 2008, 87(11):1016-1020. 10.1177/154405910808701104, 18946007.
55. Segata N, Haake SK, Mannon P, Lemon KP, 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(6):R42. 10.1186/gb-2012-13-6-r42, 3446314, 22698087.
56. Willis SG, Smith KS, Dunn VL, Gapter LA, Riviere KH, Riviere GR. Identification of seven Treponema species in health- and disease-associated dental plaque by nested PCR. J Clin Microbiol 1999, 37(3):867-869. 84590, 9986879.
57. Asai Y, Jinno T, Igarashi H, Ohyama Y, Ogawa T. Detection and quantification of oral treponemes in subgingival plaque by real-time PCR. J Clin Microbiol 2002, 40(9):3334-3340. 10.1128/JCM.40.9.3334-3340.2002, 130738, 12202575.
58. Moter A, Riep B, Haban V, Heuner K, Siebert G, Berning M, Wyss C, Ehmke B, Flemmig TF, Gobel UB. Molecular epidemiology of oral treponemes in patients with periodontitis and in periodontitis-resistant subjects. J Clin Microbiol 2006, 44(9):3078-3085. 10.1128/JCM.00322-06, 1594669, 16954230.
59. Sakamoto M, Umeda M, Benno Y. Molecular analysis of human oral microbiota. J Periodontal Res 2005, 40(3):277-285. 10.1111/j.1600-0765.2005.00793.x, 15853975.
60. Haffajee AD, Teles RP, Socransky SS. Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. Oral Microbiol Immun 2006, 21(5):269-282.
61. Mineoka T, Awano S, Rikimaru T, Kurata H, Yoshida A, Ansai T, Takehara T. Site-specific development of periodontal disease is associated with increased levels of Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia in subgingival plaque. J Periodontol 2008, 79(4):670-676. 10.1902/jop.2008.070398, 18380560.
62. Colombo APV, Boches SK, Cotton SL, Goodson JM, Kent R, Haffajee AD, Socransky SS, Hasturk H, Van Dyke TE, Dewhirst F. Comparisons of Subgingival Microbial Profiles of Refractory Periodontitis, Severe Periodontitis, and Periodontal Health Using the Human Oral Microbe Identification Microarray. J Periodontol 2009, 80(9):1421-1432. 10.1902/jop.2009.090185, 3627366, 19722792.
63. Hutter G, Schlagenhauf U, Valenza G, Horn M, Burgemeister S, Claus H, Vogel U. Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiology 2003, 149(Pt 1):67-75.
64. Lai Y, Chu L. Novel mechanism for conditional aerobic growth of the anaerobic bacterium Treponema denticola. Appl Environ Microbiol 2008, 74(1):73-79. 10.1128/AEM.01972-07, 2223203, 17981934.
65. Fenno JC. Treponema denticola interactions with host proteins. J Oral Microbiol 2012, 4:9929.
66. Marsh PD, Devine DA. How is the development of dental biofilms influenced by the host?. J Clin Periodontol 2011, 38(Suppl 11):28-35.
67. Cogoni V, Morgan-Smith A, Fenno JC, Jenkinson HF, Dymock D. Treponema denticola chymotrypsin-like proteinase (CTLP) integrates spirochaetes within oral microbial communities. Microbiology 2012, 158(Pt 3):759-770.
68. Rosen G, Genzler T, Sela MN. Coaggregation of Treponema denticola with Porphyromonas gingivalis and Fusobacterium nucleatum is mediated by the major outer sheath protein of Treponema denticola. FEMS Microbiol Lett 2008, 289(1):59-66. 10.1111/j.1574-6968.2008.01373.x, 19054094.