Variation on a theme; an overview of the Tn916/Tn1545 family of mobile genetic elements in the oral and nasopharyngeal streptococci

Frontiers in Microbiology

Volumn 5, Issue OCT, 2014, Pages

  Santoro, Francesco ^a   Vianna, Morgana E ^b   Roberts, Adam P ^b  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Antibiotic resistance; Conjugation; Conjugative transposon; Horizontal gene transfer; Nasopharyngeal; Oral cavity; Streptococcus; Transformation

Indexed keywords

AMOXICILLIN; AMPICILLIN; AZITHROMYCIN; CEFALEXIN; CEFAZOLIN; CHLORAMPHENICOL; CLINDAMYCIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTEREMIA; DENTAL CARIES; GENE; GENE TRANSFER; GENETIC VARIABILITY; HUMAN; MOBILE GENETIC ELEMENT; NASOPHARYNX; NONHUMAN; STREPTOCOCCUS; STREPTOCOCCUS MITIS; STREPTOCOCCUS MUTANS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS SANGUINIS; TN916; TOOTH PERIAPICAL DISEASE; TRANSPOSON;

STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84927165326     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00535     Document Type: Article

References (104)

1. Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I., and Dewhirst, F. E. (2005). Defining the normal bacterial flora of the oral cavity. J. Clin.Microbiol. 43, 5721-5732. doi: 10.1128/JCM.43.11.5721-5732.2005
2. Bender, I. B., Naidorf, I. J., and Garvey, G. J. (1984). Bacterial endocarditis: a consideration for physician and dentist. J. Am. Dent. Assoc. 109, 415-420.
3. Bentorcha, F., Clermont, D., de Cespédès, G., and Horaud, T. (1992). Natural occurrence of structures in oral streptococci and enterococci with DNA homol- ogytoTn916. Antimicrob. Agents Chemother. 36, 59-63. doi: 10.1128/AAC. 36.1.59
4. Bergstrom, J. (2009). It is unclear if toothbrushing is a risk factor for infec- tive endocarditis in children. J. Evid. Based Dent. Pract. 9, 219-220. doi: 10.1016/j.jebdp.2009.06.005
5. Bertram, J., Strätz,M., andDürre, P. (1991). Natural transfer of conjugative transpo- son Tn916 between gram-positive and gram-negative bacteria. J. Bacteriol. 173, 443-448.
6. Brenciani, A., Tiberi, E., Morici, E., Oryasin, E., Giovanetti, E., and Varaldo, P. E. (2012). ICESp1116, the genetic element responsible for erm(B)-mediated, inducible resistance to erythromycin in Streptococcus pyogenes. Antimicrob. Agents Chemother. 56, 6425-6429. doi: 10.1128/AAC.01494-12
7. Brenciani, A., Tiberi, E., Tili, E., Mingoia, M., Palmieri, C., Varaldo, P. E., et al. (2014). Genetic determinants and elements associated with antibiotic resistance in viridans group streptococci. J. Antimicrob. Chemother. 69, 1197-1204. doi: 10.1093/jac/dkt495
8. Brouwer, M. S., Mullany, P., and Roberts, A. P. (2010). Characterization of the conjugative transposonTn6000 fromEnterococcus casseliflavus 664.1H1 (formerly Enterococcus faecium 664.1H1). FEMS Microbiol. Lett. 309, 71-76.
9. Calatayud, L., Ardanuy, C., Cercenado, E., Fenoll, A., Bouza, E., Pallares, R., et al. (2007). Serotypes, clones, and mechanisms of resistance of erythromycin- resistant Streptococcus pneumoniae isolates collected in spain. Antimicrob. Agents Chemother. 51, 3240-3246. doi: 10.1128/AAC.00157-07
10. Calatayud, L., Ardanuy, C., Tubau, F., Rolo, D., Grau, I., Pallarés, R., et al. (2010). Serotype and genotype replacement among macrolide-resistant invasive pneu- mococci in adults: mechanisms of resistance and association with different transposons. J. Clin. Microbiol. 48, 1310-1316. doi: 10.1128/JCM.01868-09
11. Chávez De Paz, L. E., Dahlén, G., Molander, A., Möller, A., and Bergen- holtz, G. (2003). Bacteria recovered from teeth with apical periodontitis after antimicrobial endodontic treatment. Int. Endod. J. 36, 500-508. doi: 10.1046/j.1365-2591.2003.00686.x
12. Chewapreecha, C., Harris, S. R., Croucher, N. J., Turner, C., Marttinen, P., Cheng, L., et al. (2014). Dense genomic sampling identifies highways of pneumococcal recombination. Nat. Genet. 46, 305-309. doi: 10.1038/ng.2895
13. Ciric, L., Ellatif,M., Sharma, P., Patel, R., Song, X.,Mullany, P., et al. (2012). Tn916- like elements from human, oral, commensal streptococci possess a variety of antibiotic and antiseptic resistance genes. Int. J. Antimicrob. Agents 39, 360-361. doi: 10.1016/j.ijantimicag.2011.12.007
14. Ciric, L., Jasni, A., de Vries, L. E., Agersø, Y.,Mullany, P., and Roberts, A. P. (2011a). "The Tn916/Tn1545 family of conjugative transposons," in Bacterial Integrative Mobile Genetic Elements, eds A. P. Roberts and P. Mullany (Texas, TX: Landes Bioscience).
15. Ciric, L., Mullany, P., and Roberts, A. P. (2011b). Antibiotic and antiseptic resis- tance genes are linked on a novel mobile genetic element: Tn6087. J. Antimicrob. Chemother. 66, 2235-2239. doi: 10.1093/jac/dkr311
16. Clermont, D., and Horaud, T. (1990). Identification of chromosomal antibiotic resistance genes in Streptococcus anginosus ("S. milleri"). Antimicrob. Agents Chemother. 34, 1685-1690. doi: 10.1128/AAC.34.9.1685
17. Cochetti, I., Tili, E., Mingoia, M., Varaldo, P. E., and Montanari, M. P. (2008). erm(B)-carrying elements in tetracycline-resistant pneumococci and cor- respondence between Tn1545 and Tn6003. Antimicrob. Agents Chemother. 52, 1285-1290. doi: 10.1128/AAC.01457-07
18. Cochetti, I., Tili, E.,Vecchi,M.,Manzin, A.,Mingoia,M.,Varaldo, P. E., et al. (2007). New Tn916-related elements causing erm(B)-mediated erythromycin resistance in tetracycline-susceptible pneumococci. J. Antimicrob. Chemother. 60, 127-131. doi: 10.1093/jac/dkm120
19. Cook, L., Chatterjee, A., Barnes, A., Yarwood, J., Hu, W. S., and Dunny, G. (2011). Biofilm growth alters regulation of conjugation by a bacterial pheromone. Mol. Microbiol. 81, 1499-1510. doi: 10.1111/j.1365-2958.2011.07786.x
20. Croucher, N. J., Hanage, W. P., Harris, S. R., McGee, L., van der Linden, M., de Lencastre, H. M., et al. (2014). Variable recombination dynamics during the emergence, transmission and"disarming"of amultidrug-resistant pneumococcal clone. BMC Biol. 1:49. doi: 10.1186/1741-7007-12-49
21. Croucher, N. J.,Harris, S. R., Fraser, C., Quail,M. A., Burton, J., van der Linden,M., et al. (2011). Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430-434. doi: 10.1126/science.1198545
22. Croucher, N. J., Walker, D., Romero, P., Lennard, N., Paterson, G. K., Bason, N. C., et al. (2009). Role of conjugative elements in the evolution of the multidrug- resistant pandemic clone Streptococcus pneumoniae Spain23F ST81. J. Bacteriol. 191, 1480-1489. doi: 10.1128/JB.01343-08
23. Cvitkovitch, D. G. (2001). Genetic competence and transformation in oral Streptococci. Crit. Rev. Oral Biol. Med. 12, 217-243. doi: 10.1177/10454411010120030201
24. Debelian, G. J., Olsen, I., and Tronstad, L. (1995). Bacteremia in conjunction with endodontic therapy. Endod. Dent. Traumatol. 11, 142-149. doi: 10.1111/j.1600- 9657.1995.tb00476.x
25. Del Grosso, M., Camilli, R., Iannelli, F., Pozzi, G., and Pantosti, A. (2006). The mef(E)-carrying genetic element (mega) of Streptococcus pneumoniae: insertion sites and association with other genetic elements. Antimicrob. Agents Chemother. 50, 3361-3366. doi: 10.1128/AAC.00277-06
26. Del Grosso, M., Scotto d'Abusco, A., Iannelli, F., Pozzi, G., and Pantosti, A. (2004). Tn2009, a Tn916-like element containing mef(E) in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 48, 2037-2042. doi: 10.1128/AAC.48.6.2037- 2042.2004
27. Ealla, K. K., Ghanta, S. B., Motupalli, N. K., Bembalgi, M., Madineni, P. K., and Raju, P. K. (2013). Comparative analysis of colony counts of different species of oral streptococci in saliva of dentulous, edentulous and in those wearing partial and complete dentures. J. Contemp. Dent. Pract. 14, 601-604. doi: 10.5005/jp- journals-10024-1371
28. Edwardsson, S., Bing,M., Axtelius, B., Lindberg, B., Söderfeldt, B., and Attström, R. (1999). The microbiota of periodontal pockets with different depths in therapy- resistant periodontitis. J. Clin. Periodontol. 26, 143-152. doi: 10.1034/j.1600- 051X.1999.260303.x
29. Eren, A. M., Borisy, G. G., Huse, S. M., and Mark Welch, J. L. (2014). Oligotyping analysis of the human oral microbiome. Proc. Natl. Acad. Sci. U.S.A. 111, E2875- E2884. doi: 10.1073/pnas.1409644111
30. Franke,A. E., andClewell,D.B. (1981). Evidence for a chromosome-borne resistance transposon (Tn916)in Streptococcus faecalis that is capable of "conjugal" transfer in the absence of a conjugative plasmid. J. Bacteriol. 145, 494-502.
31. Ge, Y., Caufield, P. W., Fisch, G. S., and Li, Y. (2008). Streptococcus mutans and Streptococcus sanguinis colonization correlated with caries experience in children. Caries Res. 42, 444-448. doi: 10.1159/000159608
32. Griffith, F. (1928). The significance of pneumococcal types. J. Hyg. (Lond.) 27, 113-159. doi: 10.1017/S0022172400031879
33. Han, J. K., and Kerschner, J. E. (2001). Streptococcus milleri: an organism for head and neck infections and abscess. Arch. Otolaryngol. HeadNeck Surg. 127, 650-654. doi: 10.1001/archotol.127.6.650
34. Hannan, S., Ready, D., Jasni, A. S., Rogers, M., Pratten, J., and Roberts, A. P. (2010). Transfer of antibiotic resistance by transformation with eDNA within oral biofilms. FEMS Immunol. Med. Microbiol. 59, 345-349. doi: 10.1111/j.1574- 695X.2010.00661.x
35. Hansman, D., and Bullen, M. M. (1967). A resistant pneumococcus. Lancet 290, 264-265. doi: 10.1016/S0140-6736(67)92346-X
36. Hardie, J. M. (1992). Oral microbiology: current concepts in the microbiol- ogy of dental caries and periodontal disease. Br. Dent. J. 172, 271-278. doi: 10.1038/sj.bdj.4807849
37. Hartley,D. L., Jones,K.R.,Tobian, J.A., LeBlanc,D. J., andMacrina, F. L. (1984).Dis- seminated tetracycline resistance in oral streptococci: implication of a conjugative transposon. Infect. Immun. 45, 13-17.
38. Heimdahl, A., Hall, G., Hedberg, M., Sandberg, H., Söder, P. O., Tunér, K., et al. (1990). Detection and quantitation by lysis-filtration of bacteremia after different oral surgical procedures. J. Clin. Microbiol. 28, 2205-2209.
39. Henderson-Begg, S. K., Roberts, A. P., and Hall, L. M. (2009). Diversity of putative Tn5253-like elements in Streptococcus pneumoniae. Int. J. Antimicrob. Agents 33, 364-367. doi: 10.1016/j.ijantimicag.2008.10.002
40. Huyghe, A., François, P., Mombelli, A., Tangomo, M., Girard, M., Baratti-Mayer, D., et al. (2013). Microarray analysis of microbiota of gingival lesions in noma patients. PLoS Negl. Trop. Dis. 7:e2453. doi: 10.1371/journal.pntd.0002453
41. Iannelli, F., Santoro, F., Oggioni, M. R., and Pozzi, G. (2014). Nucleotide sequence analysis of integrative conjugative element Tn5253 of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 58, 1235-1239. doi: 10.1128/AAC.01764-13
42. Jaworski, D. D., and Clewell, D. B. (1994). Evidence that coupling sequences play a frequency-determining role in conjugative transposition of Tn916 in Enterococcus faecalis. J. Bacteriol. 176, 3328-3335.
43. Joloba, M. L., Kidenya, B. R., Kateete, D. P., Katabazi, F. A., Muwanguzi, J. K., Asiimwe, B. B., et al. (2010). Comparison of transformation frequencies among selected Streptococcus pneumoniae serotypes. Int. J. Antimicrob. Agents 36, 124- 128. doi: 10.1016/j.ijantimicag.2010.03.024
44. KeestraJ. A., Grosjean, I., Coucke,W., Quirynen,M., and Teughels,W. (2014). Non- surgical periodontal therapy with systemic antibiotics in patients with untreated chronic periodontitis: a systematic review and meta-analysis. J. Periodontal Res. doi: 10.1111/jre.12221 [Epub ahead of print].
45. Keijser, B. J., Zaura, E.,Huse, S.M., van derVossen, J.M., Schuren, F. H.,Montijn, R. C., et al. (2008). Pyrosequencing analysis of the oral microflora of healthy adults. J. Dent. Res. 87, 1016-1020. doi: 10.1177/154405910808701104
46. Kuriyama, T., Williams, D. W., Yanagisawa, M., Iwahara, K., Shimizu, C., Nakagawa, K., et al. (2007). Antimicrobial susceptibility of 800 anaerobic isolates from patients with dentoalveolar infection to 13 oral antibiotics. Oral Microbiol. Immunol. 22, 285-288. doi: 10.1111/j.1399-302X.2007.00365.x
47. Lancaster, H., Roberts, A. P., Bedi, R.,Wilson, M., and Mullany, P. (2004). Charac- terization of Tn916S, a Tn916-like element containing the tetracycline resistance determinant tet(S). J. Bacteriol. 186, 4395-4398. doi: 10.1128/JB.186.13.4395- 4398.2004
48. Le Polain de Waroux, O., Flasche, S., Prieto-Merino, D., and Edmunds, W. J. (2014). Age-dependent prevalence of nasopharyngeal carriage of Streptococcus pneumoniae before conjugate vaccine introduction: a prediction model based on a meta-analysis. PLoS ONE 9:e86136. doi: 10.1371/journal.pone.0086136
49. Li, Y., Tomita, H., Lv, Y., Liu, J., Xue, F., Zheng, B., et al. (2011). Molecular charac- terization of erm(B)- and mef(E)-mediated erythromycin-resistant Streptococcus pneumoniae in China and complete DNA sequence of Tn2010. J. Appl.Microbiol. 110, 254-265. doi: 10.1111/j.1365-2672.2010.04875.x
50. Lucas, V. S., Gafan, G., Dewhurst, S., and Roberts, G. J. (2008). Prevalence, inten- sity and nature of bacteraemia after toothbrushing. J. Dent. 36, 481-487. doi: 10.1016/j.jdent.2008.03.005
51. Martin, B., Soulet, A. L., Mirouze, N., Prudhomme, M., Mortier-Barrière, I., Granadel, C., et al. (2013). ComE/ComEP interplay dictates activation or extinc- tion status of pneumococcal X-state (competence). Mol. Microbiol. 87, 394-411. doi: 10.1111/mmi.12104
52. McDougal, L. K., Tenover, F. C., Lee, L. N., Rasheed, J. K., Patterson, J. E., Jorgensen, J. H., et al. (1998). Detection of Tn917-like sequences within a Tn916-like con- jugative transposon (Tn3872) in erythromycin-resistant isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 42, 2312-2318.
53. McGee, L., McDougal, L., Zhou, J., Spratt, B. G., Tenover, F. C., George, R., et al. (2001). Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiol- ogy network. J. Clin. Microbiol. 39, 2565-2571. doi: 10.1128/JCM.39.7.2565- 2571.2001
54. Mingoia, M., Tili, E., Manso, E., Varaldo, P. E., and Montanari, M. P. (2011). Heterogeneity of Tn5253-like composite elements in clinical Strepto- coccus pneumoniae isolates. Antimicrob. Agents Chemother. 55, 1453-1459. doi: 10.1128/AAC.01087-10
55. Mook-Kanamori, B. B., Geldhoff, M., van der Poll, T., and van de Beek, D. (2011). Pathogenesis and pathophysiology of pneumococcal meningitis. Clin. Microbiol. Rev. 24, 557-591. doi: 10.1128/CMR.00008-11
56. Mostowy, R., Croucher, N. J., Hanage, W. P., Harris, S. R., Bentley, S., and Fraser, C. (2014). Heterogeneity in the frequency and characteristics of homolo- gous recombination in pneumococcal evolution. PLoS Genet. 10:e1004300. doi: 10.1371/journal.pgen.1004300
57. Mullany, P., Roberts, A. P., and Wang, H. (2002). Mechanism of integration and excision in conjugative transposons. Cell.Mol.LifeSci. 59, 2017-2022. doi: 10.1007/s000180200001
58. Mullany, P., Wilks, M., and Tabaqchali, S. (1991). Transfer of Tn916 and Tn916 delta E into Clostridium difficile: demonstration of a hot-spot for these elements in the C. difficile genome. FEMS Microbiol. Lett. 63, 191-194.
59. Mullany, P., Williams, R., Langridge, G. C., Turner, D. J., Whalan, R., Clayton, C., et al. (2012). Behavior and target site selection of conjugative transposon Tn916 in two different strains of toxigenic Clostridium difficile. Appl. Environ.Microbiol. 78, 2147-2153. doi: 10.1128/AEM.06193-11
60. Nabavizadeh, M. R., Sahebi, S., and Nadian, I. (2011). Antibiotic prescription for endodontic treatment: general dentist knowledge + practice in shiraz. Iran. Endod. J. 6, 54-59.
61. Nguyen, D. H., and Martin, J. T. (2008). Common dental infections in the primary care setting. Am. Fam. Physician 77, 797-802.
62. Nobbs, A. H., Lamont, R. J., and Jenkinson, H. F. (2009). Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73, 407-450. doi: 10.1128/MMBR.00014-09
63. Novais, C., Freitas, A. R., Silveira, E., Baquero, F., Peixe, L., Roberts, A. P., et al. (2012a). A tet(S/M) hybrid from CTn6000 and CTn916 recombination. Microbiology 158, 2710-2711. doi: 10.1099/mic.0.062729-0
64. Novais, C., Freitas, A. R., Silveira, E., Baquero, F., Peixe, L., Roberts, A. P., et al. (2012b). Different genetic supports for the tet(S) gene in enterococci. Antimicrob. Agents Chemother. 56, 6014-6018. doi: 10.1128/AAC.00758-12
65. Ochiai, K., Kurita-Ochiai, T., Kamino, Y., and Ikeda, T. (1993). Effect of co- aggregation on the pathogenicity of oral bacteria. J.Med. Microbiol. 39, 183-190. doi: 10.1099/00222615-39-3-183
66. Oggioni, M. R., Trappetti, C., Kadioglu, A., Cassone, M., Iannelli, F., Ricci, S., et al. (2006). Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol. Microbiol. 61, 1196-1210. doi: 10.1111/j.1365- 2958.2006.05310.x
67. Olsen, I., Tribble, G. D., Fiehn, N. E., andWang, B. Y. (2013). Bacterial sex in dental plaque. J. Oral Microbiol. 3, 5. doi: 10.3402/jom.v5i0.20736
68. Palmieri, C., Mingoia, M., Massidda, O., Giovanetti, E., and Varaldo, P. E. (2012). Streptococcus pneumoniae transposon Tn1545/Tn6003 changes to Tn6002 due to spontaneous excision in circular form of the erm(B)- and aphA3-containing macrolide-aminoglycoside-streptothricin (MAS) element. Antimicrob. Agents Chemother. 56, 5994-5997. doi: 10.1128/AAC.01487-12
69. Pearce, C., Bowden, G. H., Evans, M., Fitzsimmons, S. P., Johnson, J., Sheridan, M. J., et al. (1995). Identification of pioneer viridans streptococci in the oral cavity of human neonates. J.Med.Microbiol. 42, 67-72. doi: 10.1099/00222615-42-1-67
70. Peterson, S. N., Sung, C. K., Cline, R., Desai, B. V., Snesrud, E. C., Luo, P., et al. (2004). Identification of competence pheromone responsive genes in Streptococ- cus pneumoniae by use of DNA microarrays. Mol. Microbiol. 51, 1051-1070. doi: 10.1046/j.1365-2958.2003.03907.x
71. Provvedi, R., Manganelli, R., and Pozzi, G. (1996). Characterization of conjugative transposon Tn5251 of Streptococcus pneumoniae. FEMSMicrobiol. Lett. 135, 231- 236. doi: 10.1111/j.1574-6968.1996.tb07994.x
72. Prudhomme, M., Attaiech, L., Sanchez, G., Martin, B., and Claverys, J. P. (2006). Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313, 89-92. doi: 10.1126/science.1127912
73. Quintero, B., Araque, M., van der Gaast-de Jongh, C., and Hermans, P. W. (2011). Genetic diversity of Tn916-related transposons among drug-resistant Strepto- coccus pneumoniae isolates colonizing healthy children in Venezuela. Antimicrob. Agents Chemother. 55, 4930-4932. doi: 10.1128/AAC.00242-11
74. Ready, D., Pratten, J., Roberts, A. P., Bedi, R., Mullany, P., and Wilson, M. (2006). Potential role of Veillonella spp. as a reservoir of transferable tetracycline resis- tance in the oral cavity. Antimicrob. Agents Chemother. 50, 2866-2868. doi: 10.1128/AAC.00217-06
75. Roberts, A. P., Chandler, M., Courvalin, P., Guédon, G., Mullany, P., Pembroke, T., et al. (2008). Revised nomenclature for transposable genetic elements. Plasmid 60, 167-173. doi: 10.1016/j.plasmid.2008.08.001
76. Roberts, A. P., Cheah, G., Ready, D., Pratten, J.,Wilson,M., andMullany, P. (2001a). Transfer of Tn916-like elements inmicrocosmdental plaques. Antimicrob. Agents Chemother. 45, 2943-2946. doi: 10.1128/AAC.45.10.2943-2946.2001
77. Roberts, A. P., Johanesen, P. A., Lyras, D., Mullany, P., and Rood, J. I. (2001b). Comparison of Tn5397 from Clostridium difficile,Tn916 from Enterococcus fae- calis and the CW459tet(M) element fromClostridiumperfringens shows that they have similar conjugation regions but different insertion and excision modules. Microbiology 147, 1243-1251.
78. Roberts, A. P., Davis, I. J., Seville, L., Villedieu, A., and Mullany, P. (2006). Charac- terization of the ends and target site of a novel tetracycline resistance-encoding conjugative transposon from Enterococcus faecium 664.1H1. J. Bacteriol. 188, 4356-4361. doi: 10.1128/JB.00129-06
79. Roberts, A. P., and Kreth, J. (2014). The impact of horizontal gene transfer on the adaptive ability of the human oral microbiome. Front. Cell. Infect. Microbiol. 4:124. doi: 10.3389/fcimb.2014.00124
80. Roberts, A. P., and Mullany, P. (2006). Genetic basis of horizontal gene trans- fer among oral bacteria. Periodontol. 2000 42, 36-46. doi: 10.1111/j.1600- 0757.2006.00149.x
81. Roberts, A. P., and Mullany, P. (2009). A modular master on the move: the Tn916 family of mobile genetic elements. Trends Microbiol. 17, 251-258. doi: 10.1016/j.tim.2009.03.002
82. Roberts, A. P., and Mullany, P. (2010). Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev. Anti Infect. Ther. 8, 1441-1450. doi: 10.1586/eri.10.106
83. Roberts, A. P., and Mullany, P. (2011). Tn916-like genetic elements: a diverse group of modular mobile elements conferring antibiotic resis- tance. FEMS Microbiol. Rev. 35, 856-871. doi: 10.1111/j.1574-6976.2011. 00283.x
84. Roberts, A. P., Pratten, J., Wilson, M., and Mullany, P. (1999). Transfer of a con- jugative transposon, Tn5397 in a model oral biofilm. FEMS Microbiol. Lett. 177, 63-66. doi: 10.1111/j.1574-6968.1999.tb13714.x
85. Robertson,D., and Smith,A. J. (2009).Microbiology of acute dental abscess. J.Med. Microbiol. 58, 155-162. doi: 10.1099/jmm.0.003517-0
86. Santoro, F., Oggioni, M. R., Pozzi, G., and Iannelli, F. (2010). Nucleotide sequence and functional analysis of the tet(M)-carrying conjugative transpo- son Tn5251 of Streptococcus pneumoniae. FEMS Microbiol. Lett. 308, 150-158. doi: 10.1111/j.1574-6968.2010.02002.x
87. Scott, J. R., Bringel, F., Marra, D., van Alstine, G., and Rudy, C. K. (1994). Conjugative transposition of Tn916: preferred targets and evidence for conjugative transfer of a single strand and for a double-stranded circular intermediate. Mol. Microbiol. 11, 1099-1108. doi: 10.1111/j.1365-2958.1994. tb00386.x
88. Scott, J. R., Kirchman, P. A., and Caparon, M. G. (1988). An intermediate in trans- position of the conjugative transposon Tn916. Proc. Natl. Acad. Sci. U.S.A. 85, 4809-4813. doi: 10.1073/pnas.85.13.4809
89. Seville, L. A., Patterson, A. J., Scott, K. P.,Mullany, P., Quail,M. A., Parkhill, J., et al. (2009). Distribution of tetracycline and erythromycin resistance genes among human oral and fecal metagenomic DNA. Microb. Drug Resist. 15, 159-166. doi: 10.1089/mdr.2009.0916
90. Shoemaker, N. B., Smith, M. D., and Guild, W. R. (1979). Organization and transfer of heterologous chloramphenicol and tetracycline resistance genes in pneumococcus. J. Bacteriol. 139, 432-441.
91. Siqueira, J. F. Jr., and Rôças, I. N. (2013). Microbiology and treatment of acute apical abscesses. Clin. Microbiol. Rev. 26, 255-273. doi: 10.1128/CMR. 00082-12
92. Starkebaum, M., Durack, D., and Beeson, P. (1977). The "incubation period" of subacute bacterial endocarditis. Yale J. Biol. Med. 50, 49-58.
93. Topazian, R. G., Goldberg, M. H., and Hupp, J. R. (eds). (2002). Oral, and Maxillofacial Infections, 4th Edn. Philadelphia, PA:WB Saunders Company.
94. Vianna, M. E., Horz, H. P., Conrads, G., Feres, M., and Gomes, B. P. (2008). Comparative analysis of endodontic pathogens using checkerboard hybridization in relation to culture. OralMicrobiol. Immunol. 23, 282-290. doi: 10.1111/j.1399- 302X.2007.00425.x
95. Wade,W. G. (2013). The oralmicrobiome in health and disease. Pharmacol. Res. 69, 137-143. doi: 10.1016/j.phrs.2012.11.006
96. Wang,H., andMullany, P. (2000). The large resolvase TndXis required and sufficient for integration and excision of derivatives of the novel conjugative transposon Tn5397. J. Bacteriol. 182, 6577-6583. doi: 10.1128/JB.182.23.6577-6583.2000
97. Wang, H., Roberts, A. P., and Mullany, P. (2000). DNA sequence of the insertional hot spot of Tn916 in the Clostridium difficile genome and discovery of a Tn916- like element in an environmental isolate integrated in the same hot spot. FEMS Microbiol. Lett. 192, 15-20. doi: 10.1111/j.1574-6968.2000.tb09352.x
98. Warburton, P. J., Palmer,R.M.,Munson,M.A., andWade,W.G. (2007).Demonstra- tion of in vivo transfer of doxycycline resistance mediated by a novel transposon. J. Antimicrob. Chemother. 60, 973-980. doi: 10.1093/jac/dkm331
99. Watson, D. A., and Musher, D. M. (1990). Interruption of capsule production in Streptococcus pneumoniae serotype 3 by insertion of transposon Tn916. Infect. Immun. 58, 3135-3138.
100. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C., and Mattick, J. S. (2002). Extra- cellular DNA required for bacterial biofilm formation. Science 295, 1487. doi: 10.1126/science.295.5559.1487
101. Wilson, W., Taubert, K. A., Gewitz, M., Lockhart, P. B., Baddour, L. M., Lev- ison, M., et al. (2008). American Heart Association. Prevention of infective endocarditis: guidelines from the American Heart Association: a guideline from the American Heart Association Rheumatic Fever, Endocarditis and Kawasaki Disease Committee, Council on Cardiovascular Disease in the Young, and the Council on Clinical Cardiology, Council on Cardiovascular Surgery and Anes- thesia, and theQuality of Care andOutcomes Research InterdisciplinaryWorking Group. J. Am. Dent. Assoc. 139(Suppl.), 3S-24S. doi: 10.14219/jada.archive. 2008.0346
102. Xu, X., Cai, L., Xiao, M., Kong, F., Oftadeh, S., Zhou, F., et al. (2010). Distribution of serotypes, genotypes, and resistance determinants among macrolide-resistant Streptococcus pneumoniae isolates. Antimicrob. Agents Chemother. 54, 1152-1159. doi: 10.1128/AAC.01268-09
103. Zhou, L., Ma, X., Gao,W., Yao, K. H., Shen, A. D., Yu, S. J., et al. (2012). Molecular characteristics of erythromycin-resistant Streptococcus pneumoniae from pedi- atric patients younger than five years in Beijing, 2010. BMC Microbiol. 12:228. doi: 10.1186/1471-2180-12-228
104. Zhou, W., Yao, K., Zhang, G., Yang, Y., Li, Y., Lv, Y., et al. (2014). Mechanism for transfer of transposon Tn2010 carrying macrolide resistance genes in Streptococ- cus pneumoniae and its effects on genome evolution. J. Antimicrob. Chemother. 69, 1470-1473. doi: 10.1093/jac/dku019