Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae

Frontiers in Microbiology

Volumn 6, Issue FEB, 2015, Pages

  Chancey, Scott T ^a,b   Agrawal, Sonia ^c   Schroeder, Max R ^a,b   Farley, Monica M ^a,b   Tettelin, Hervé ^c   Stephens, David S ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotic resistance; Integrative and conjugative elements; Macrolides; Mobile genetic elements; Streptococcus pneumoniae; Transposons

Indexed keywords

CLINDAMYCIN; ERYTHROMYCIN; MACROLIDE; RNA METHYLTRANSFERASE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CHILD; CONTROLLED STUDY; DNA INTEGRATION; ERM GENE; GENE INSERTION; GENE INSERTION SEQUENCE; GENE SEQUENCE; GENETIC TRANSFORMATION; GENETIC VARIABILITY; HUMAN; INFANT; MEF GENE; MEL GENE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PNEUMOCOCCAL INFECTION; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; STREPTOCOCCUS PNEUMONIAE; TN916 GENE; TRANSPOSON;

STREPTOCOCCUS PNEUMONIAE;

EID: 84927516630     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00026     Document Type: Article

References (56)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389.
2. Ambrose, K. D., Nisbet, R., and Stephens, D. S. (2005). Macrolide efflux in Streptococcus pneumoniae is mediated by a dual efflux pump (mel and mef) and is erythromycin inducible. Antimicrob. Agents Chemother. 49, 4203-4209. doi: 10.1128/AAC.49.10.4203-4209.2005.
3. Ayoubi, P., Kilic, A. O., and Vijayakumar, M. N. (1991). Tn5253, the pneumococcal omega (cat tet) BM6001 element, is a composite structure of two conjugative transposons, Tn5251 and Tn5252. J. Bacteriol. 173, 1617-1622.
4. Berge, M., Moscoso, M., Prudhomme, M., Martin, B., and Claverys, J.-P. (2002). Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Mol. Microbiol. 45, 411-421. doi: 10.1046/j.1365-2958.2002.03013.x.
5. Brown, J., Gilliland, S., and Holden, D. (2001). A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol. Microbiol. 40, 572-585. doi: 10.1046/j.1365-2958.2001.02414.x.
6. Brown, J. S., Gilliland, S. M., Spratt, B. G., and Holden, D. W. (2004). A locus contained within a variable region of pneumococcal pathogenicity Island 1 contributes to virulence in mice. Infect. Immun. 72, 1587-1593. doi: 10.1128/IAI.72.3.1587-1593.2004.
7. Caparon, M. G., and Scott, J. R. (1989). Excision and insertion of the conjugative transposon Tn916 involves a novel recombination mechanism. Cell 59, 1027-1034. doi: 10.1016/0092-8674(89)90759-9.
8. Carver, T. J., Rutherford, K. M., Berriman, M., Rajandream, M.-A., Barrell, B. G., and Parkhill, J. (2005). ACT: the Artemis Comparison Tool. Bioinformatics (Oxford, England) 21, 3422-3423. doi: 10.1093/bioinformatics/bti553.
9. Chancey, S. T., Zhou, X., Zähner, D., and Stephens, D. S. (2011). Induction of efflux-mediated macrolide resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 55, 3413-3422. doi: 10.1128/AAC.00060-11.
10. Claverys, J.-P., Prudhomme, M., and Martin, B. (2006). Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu. Rev. Microbiol. 60, 451-475. doi: 10.1146/annurev.micro.60.080805.142139.
11. Cochetti, I., Tili, E., Mingoia, M., Varaldo, P. E., and Montanari, M. P. (2008). erm(B)-Carrying elements in tetracycline-resistant pneumococci and correspondence between Tn1545 and Tn6003. Antimicrob. Agents Chemother. 52, 1285-1290. doi: 10.1128/AAC.01457-07.
12. 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.
13. Croucher, N. J., Hanage, W. P., Harris, S. R., McGee, L., van der Linden, M., de Lencastre, H., et al. (2014). Variable recombination dynamics during the emergence, transmission and 'disarming' of a multidrug-resistant pneumococcal clone. BMC Biol. 12:49. doi: 10.1186/1741-7007-12-49.
14. 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.
15. Del Grosso, M., Camilli, R., Barbabella, G., Blackman Northwood, J., Farrell, D. J., and Pantosti, A. (2011). Genetic resistance elements carrying mef subclasses other than mef(A) in Streptococcus pyogenes. Antimicrob. Agents Chemother. 55, 3226-3230. doi: 10.1128/AAC.01713-10.
16. 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.
17. Del Grosso, M., Camilli, R., Libisch, B., Fuzi, M., and Pantosti, A. (2009). New composite genetic element of the Tn916 family with dual macrolide resistance genes in a Streptococcus pneumoniae isolate belonging to clonal complex 271. Antimicrob. Agents Chemother. 53, 1293-1294. doi: 10.1128/AAC.01066-08.
18. Del Grosso, M., Northwood, J. G. E., Farrell, D. J., and Pantosti, A. (2007). The macrolide resistance genes erm(B) and mef(E) are carried by Tn2010 in dual-gene Streptococcus pneumoniae isolates belonging to clonal complex CC271. Antimicrob. Agents Chemother. 51, 4184-4186. doi: 10.1128/AAC.00598-07.
19. Del Grosso, M., Scotto d'Abusco, A., Lannelli, 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.
20. Denapaite, D., Bruckner, R., Nuhn, M., Reichmann, P., Henrich, B., Maurer, P., et al. (2010). The genome of Streptococcus mitis B6-what is a commensal? PLoS ONE 5:e9426. doi: 10.1371/journal.pone.0009426.
21. Enright, M. C., and Spratt, B. G. (1998). A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144, 3049-3060. doi: 10.1099/00221287-144-11-3049.
22. Farley, M. M., Baughman, W., and Arnold, K. E. (2002). The Georgia emerging infections program: monitoring trends in invasive pneumococcal disease. J. Med. Assoc. Ga. 91, 20-23.
23. Gardner, S. N., and Hall, B. G. (2013). When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS ONE 8:e81760. doi: 10.1371/journal.pone.0081760.
24. Gay, K., Baughman, W., Miller, Y., Jackson, D., Whitney, C. G., Schuchat, A., et al. (2000). The emergence of Streptococcus pneumoniae resistant to macrolide antimicrobial agents: a 6-year population-based assessment. J. Infect. Dis. 182, 1417-1424. doi: 10.1086/315853.
25. Gay, K., and Stephens, D. S. (2001). Structure and dissemination of a chromosomal insertion element encoding macrolide efflux in Streptococcus pneumoniae. J. Infect. Dis. 184, 56-65. doi: 10.1086/321001.
26. Henderson-Begg, S. K., Roberts, A. P., and Hall, L. M. C. (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.
27. Holden, M. T. G., Heather, Z., Paillot, R., Steward, K. F., Webb, K., Ainslie, F., et al. (2009). Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog. 5:e1000346. doi: 10.1371/journal.ppat.1000346.
28. 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.
29. Klugman, K., and Lonks, J. (2005). Hidden epidemic of macrolide-resistant pneumococci. Emerging Infect. Dis. 11, 802-807. doi: 10.3201/eid1106.050147.
30. Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C., et al. (2004). Versatile and open software for comparing large genomes. Genome Biol. 5:R12. doi: 10.1186/gb-2004-5-2-r12.
31. Leclercq, R., and Courvalin, P. (1991). Intrinsic and unusual resistance to macrolide, lincosamide, and streptogramin antibiotics in bacteria. Antimicrob. Agents Chemother. 35, 1273-1276. doi: 10.1128/AAC.35.7.1273.
32. Lu, F., and Churchward, G. (1995). Tn916 target DNA sequences bind the C-terminal domain of integrase protein with different affinities that correlate with transposon insertion frequency. J. Bacteriol. 177, 1938-1946.
33. McCormick, A. W., Whitney, C. G., Farley, M. M., Lynfield, R., Harrison, L. H., Bennett, N. M., et al. (2003). Geographic diversity and temporal trends of antimicrobial resistance in Streptococcus pneumoniae in the United States. Nat. Med. 9, 424-430. doi: 10.1038/nm839.
34. 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 conjugative transposon (Tn3872) in erythromycin-resistant isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 42, 2312-2318.
35. 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 epidemiology network. J. Clin. Microbiol. 39, 2565-2571. doi: 10.1128/JCM.39.7.2565-2571.2001.
36. Mingoia, M., Morici, E., Morroni, G., Giovanetti, E., Del Grosso, M., Pantosti, A., et al. (2014). Tn5253 Family Integrative and Conjugative Elements Carrying mef(I) and catQ Determinants in Streptococcus pneumoniae and Streptococcus pyogenes. Antimicrob. Agents Chemother. 58, 5886-5893. doi: 10.1128/AAC.03638-14.
37. Mingoia, M., Vecchi, M., Cochetti, I., Tili, E., Vitali, L. A., Manzin, A., et al. (2007). Composite structure of Streptococcus pneumoniae containing the erythromycin efflux resistance gene mef(I) and the chloramphenicol resistance gene catQ. Antimicrob. Agents Chemother. 51, 3983-3987. doi: 10.1128/AAC.00790-07.
38. Munoz-Najar, U., and Vijayakumar, M. (1999). An operon that confers UV resistance by evoking the SOS mutagenic response in streptococcal conjugative transposon Tn5252. J. Bacteriol. 181, 2782-2788.
39. Myers, E. W., Sutton, G. G., Delcher, A. L., Dew, I. M., Fasulo, D. P., Flanigan, M. J., et al. (2000). A whole-genome assembly of Drosophila. Science 287, 2196-2204. doi: 10.1126/science.287.5461.2196.
40. Orvis, J., Crabtree, J., Galens, K., Gussman, A., Inman, J. M., Lee, E., et al. (2010). Ergatis: a web interface and scalable software system for bioinformatics workflows. Bioinformatics (Oxford, England) 26, 1488-1492. doi: 10.1093/bioinformatics/btq167.
41. 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.
42. 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.
43. 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.
44. Roberts, A. P., and Mullany, P. (2011). Tn916-like genetic elements: a diverse group of modular mobile elements conferring antibiotic resistance. FEMS Microbiol. Rev. 35, 856-871. doi: 10.1111/j.1574-6976.2011.00283.x.
45. Rocco, J. M., and Churchward, G. (2006). The integrase of the conjugative transposon Tn916 directs strand-and sequence-specific cleavage of the origin of conjugal transfer, oriT, by the endonuclease Orf20. J. Bacteriol. 188, 2207-2213. doi: 10.1128/JB.188.6.2207-2213.2006.
46. Rudy, C. K., Scott, J. R., and Churchward, G. (1997). DNA binding by the Xis protein of the conjugative transposon Tn916. J. Bacteriol. 179, 2567-2572.
47. Santagati, M., Lupo, A., Scillato, M., Di Martino, A., and Stefani, S. (2009). Conjugal mobilization of the Mega element carrying mef(E) from Streptococcus salivarius to Streptococcus pneumoniae. FEMS Microbiol. Lett. 290, 79-84. doi: 10.1111/j.1574-6968.2008.01408.x.
48. Sharma, D., Baughman, W., Holst, A., Thomas, S., Jackson, D., Beall, B., et al. (2013). Pneumococcal carriage and invasive disease in children before introduction of the 13-valent conjugate vaccine: comparison with the era before 7-valent conjugate vaccine. Pediatr. Infect. Dis. J. 32, e45-e53. doi: 10.1097/INF.0b013e3182788fdd.
49. Stephens, D. S., Zughaier, S. M., Whitney, C. G., Baughman, W. S., Barker, L., Gay, K., et al. (2005). Incidence of macrolide resistance in Streptococcus pneumoniae after introduction of the pneumococcal conjugate vaccine: population-based assessment. The Lancet 365, 855-863. doi: 10.1016/S0140-6736(05)71043-6.
50. Syrogiannopoulos, G. A., Grivea, I. N., Ednie, L. M., Bozdogan, B., Katopodis, G. D., Beratis, N. G., et al. (2003). Antimicrobial susceptibility and macrolide resistance inducibility of Streptococcus pneumoniae carrying erm(A), erm(B), or mef(A). Antimicrob. Agents Chemother. 47, 2699-2702. doi: 10.1128/AAC.47.8.2699-2702.2003.
51. Tettelin, H., Nelson, K. E., Paulsen, I. T., Eisen, J. A., Read, T. D., Peterson, S., et al. (2001). Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293, 498-506. doi: 10.1126/science.1061217.
52. Wattam, A. R., Abraham, D., Dalay, O., Disz, T. L., Driscoll, T., Gabbard, J. L., et al. (2014). PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42, D581-D591. doi: 10.1093/nar/gkt1099.
53. Wierzbowski, A. K., Boyd, D., Mulvey, M., Hoban, D. J., and Zhanel, G. G. (2005). Expression of the mef(E) gene encoding the macrolide efflux pump protein increases in Streptococcus pneumoniae with increasing resistance to macrolides. Antimicrob. Agents Chemother. 49, 4635-4640. doi: 10.1128/AAC.49.11.4635-4640.2005.
54. Wyres, K. L., van Tonder, A., Lambertsen, L. M., Hakenbeck, R., Parkhill, J., Bentley, S. D., et al. (2013). Evidence of antimicrobial resistance-conferring genetic elements among pneumococci isolated prior to 1974. BMC Genomics 14:500. doi: 10.1186/1471-2164-14-500.
55. Zähner, D., Zhou, X., Chancey, S. T., Pohl, J., Shafer, W. M., and Stephens, D. S. (2010). Human antimicrobial peptide LL-37 induces mefE/mel-mediated macrolide resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 54, 3516-3519. doi: 10.1128/AAC.01756-09.
56. 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 Streptococcus pneumoniae and its effects on genome evolution. J. Antimicrob. Chemother. 69, 1470-1473. doi: 10.1093/jac/dku019.