Streptococcus pneumoniae R6 interspecies transformation: Genetic analysis of penicillin resistance determinants and genome-wide recombination events

Molecular Microbiology

Volumn 86, Issue 3, 2012, Pages 692-706

  Sauerbier, Julia ^a   Maurer, Patrick ^a   Rieger, Martin ^a   Hakenbeck, Regine ^a  

^a University of Koblenz Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 2B;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM TRANSFORMATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC RECOMBINATION; MURM GENE; NONHUMAN; PBP1B GENE; PENICILLIN BINDING PROTEIN 2B GENE; PENICILLIN RESISTANCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; BETA-LACTAMS; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PENICILLIN RESISTANCE; PENICILLIN-BINDING PROTEINS; PENICILLINS; RECOMBINATION, GENETIC; STREPTOCOCCUS PNEUMONIAE; TRANSFORMATION, BACTERIAL;

STREPTOCOCCUS MITIS; STREPTOCOCCUS PNEUMONIAE;

EID: 84868150670     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12009     Document Type: Article

References (59)

1. Attaiech, L., Olivier, A., Mortier-Barriere, I., Soulet, A.L., Granadel, C., Martin, B., etal. (2011) Role of the single-stranded DNA-binding protein SsbB in pneumococcal transformation: maintenance of a reservoir for genetic plasticity. PLoS Genet 7: e1002156.
2. Cafini, F., del Campo, R., Alou, L., Sevillano, D., Morosini, M.I., Baquero, F., etal. (2005) Alterations of the penicillin-binding proteins and murM alleles of clinical Streptococcus pneumoniae isolates with high-level resistance to amoxicillin in Spain. J Antimicrob Chemother 57: 224-229.
3. Croucher, N.J., Harris, S.R., Barquist, L., Parkhill, J., and Bentley, S.D. (2012) A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog 8: e1002745.
4. Denapaite, D., Chi, F., Maurer, P., Nolte, O., and Hakenbeck, R. (2007) Mechanism of penicillin resistance in Streptococcus pneumoniae: targets, gene transfer, and mutations. In Molecular Biology of Streptococci. Hakenbeck, R., and Chhatwal, G.S. (eds). Wymondham, Norfolk, UK: Horizon Bioscience, pp. 290-303.
5. Denapaite, D., Brückner, R., Nuhn, M., Reichmann, P., Henrich, B., Maurer, P., etal. (2010) The genome of Streptococcus mitis B6 - what is a commensal? PLoS ONE 5: e9426.
6. Di Guilmi, A.M., Dessen, A., Dideberg, O., and Vernet, T. (2003) Functional characterization of penicillin-binding protein 1b from Streptococcus pneumoniae. J Bacteriol 185: 1650-1658.
7. Dias, R., Felix, D., and Canica, M. (2008) Diversity of penicillin binding proteins among clinical Streptococcus pneumoniae strains from Portugal. Antimicrob Agents Chemother 52: 2693-2695.
8. Dowson, C.G., Coffey, T.J., Kell, C., and Whiley, R.A. (1993) Evolution of penicillin resistance in Streptococcus pneumoniae; the role of Streptococcus mitis in the formation of a low affinity PBP2B in S. pneumoniae. Mol Microbiol 9: 635-643.
9. Ferroni, A., and Berche, P. (2001) Alterations to penicillin-binding proteins 1A, 2B and 2X amongst penicillin-resistant clinical isolates of Streptococcus pneumoniae serotype 23F from the nasopharyngeal flora of children. J Med Microbiol 50: 828-832.
10. Filipe, S., Severina, E., and Tomasz, A. (2001a) Distribution of the mosaic structured murM genes among natural populations of Streptococcus pneumoniae. J Bacteriol 182: 6798-6805.
11. Filipe, S.R., and Tomasz, A. (2000) Inhibition of the expression of penicillin-resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc Natl Acad Sci USA 97: 4891-4896.
12. Filipe, S.R., Severina, E., and Tomasz, A. (2001b) Functional analysis of Streptococcus pneumoniae MurM reveals the region responsible for its specificity in the synthesis of branched cell wall peptides. J Biol Chem 276: 39618-39628.
13. Filipe, S.R., Severina, E., and Tomasz, A. (2002) The murMN operon: a functional link between antibiotic resistance and antibiotic tolerance in Streptococcus pneumoniae. Proc Natl Acad Sci USA 99: 1550-1555.
14. Goffin, C., and Ghuysen, J.-M. (2002) Biochemistry and comparative genomics of SxxK superfamily acyltransferases offer a clue to the mycobacterial paradox: presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent. Microbiol Mol Biol Rev 66: 706-738.
15. Golubchik, T., Brueggemann, A.B., Street, T., Gertz, R.E., Jr, Spencer, C.C., Ho, T., etal. (2012) Pneumococcal genome sequencing tracks a vaccine escape variant formed through a multi-fragment recombination event. Nat Genet 44: 352-355.
16. Grebe, T., and Hakenbeck, R. (1996) Penicillin-binding proteins 2b and 2x of Streptococcus pneumoniae are primary resistance determinants for different classes of β-lactam antibiotics. Antimicrob Agents Chemother 40: 829-834.
17. Grebe, T., Paik, J., and Hakenbeck, R. (1997) A novel resistance mechanism for β-lactams in Streptococcus pneumoniae involves CpoA, a putative glycosyltransferases. J Bacteriol 179: 3342-3349.
18. Guenzi, E., Gasc, A.M., Sicard, M.A., and Hakenbeck, R. (1994) A two-component signal-transducing system is involved in competence and penicillin susceptibility in laboratory mutants of Streptococcus pneumoniae. Mol Microbiol 12: 505-515.
19. Hakenbeck, R., Tornette, S., and Adkinson, N.F. (1987) Interaction of non-lytic β-lactams with penicillin-binding proteins in Streptococcus pneumoniae. J Gen Microbiol 133: 755-760.
20. Hakenbeck, R., Martin, C., Dowson, C., and Grebe, T. (1994) Penicillin-binding protein 2b of Streptococcus pneumoniae in piperacillin-resistant laboratory mutants. J Bacteriol 176: 5574-5577.
21. r penicillin-binding protein variants during transfer of high-level β-lactam resistance from Streptococcus mitis to Streptococcus pneumoniae. J Bacteriol 180: 1831-1840.
22. Hakenbeck, R., Brückner, R., Denapaite, D., and Maurer, P. (2012) Molecular mechanism of beta-lactam resistance in Streptococcus pneumoniae. Future Microbiol 7: 395-410.
23. Halfmann, A., Kovács, M., Hakenbeck, R., and Brückner, R. (2007) Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of fifteen promoters drive expression of small noncoding RNAs. Mol Microbiol 66: 110-126.
24. Henriques-Normark, B. (2007) Molecular epidemiology and mechanisms for antibiotic resistance in Streptococcus pneumoniae. In Molecular Biology of Streptococci. Hakenbeck, R., and Chhatwal, G.S. (eds). Wymondham, Norfolk, UK: Horizon Press, pp. 269-290.
25. Hiller, N.L., Ahmed, A., Powell, E., Martin, D.P., Eutsey, R., Earl, J., etal. (2010) Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog 6: e1001108.
26. Hoskins, J., Matsushima, P., Mullen, D.L., Tang, J., Zhao, G., Meier, T.I., etal. (1999) Gene disruption studies of penicillin-binding proteins 1a, 1b and 2a in Streptococcus pneumoniae. J Bacteriol 181: 6552-6555.
27. Hoskins, J., Alborn, W.E., Jr, Arnold, J., Blaszczak, L.C., Burgett, S., DeHoff, B.S., etal. (2001) Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183: 5709-5717.
28. König, A., Reinert, R.R., and Hakenbeck, R. (1998) Streptococcus mitis with unusual high level resistance to β-lactam antibiotics. Microb Drug Resist 4: 45-49.
29. Kosowska, K., Jacobs, M.R., Bajaksouzian, S., Koeth, L., and Appelbaum, P.C. (2004) Alterations of penicillin-binding proteins 1A, 2X, and 2B in Streptococcus pneumoniae isolates for which amoxicillin MICs are higher than penicillin MICs. Antimicrob Agents Chemother 48: 4020-4022.
30. Lacks, S., and Hotchkiss, R.D. (1960) A study of the genetic material determining an enzyme activity in pneumococcus. Biochim Biophys Acta 39: 508-517.
31. Laible, G., and Hakenbeck, R. (1987) Penicillin-binding proteins in β-lactam-resistant laboratory mutants of Streptococcus pneumoniae. Mol Microbiol 1: 355-363.
32. Lanie, J.A., Ng, W.L., Kazmierczak, K.M., Andrzejewski, T.M., Davidsen, T.M., Wayne, K.J., etal. (2007) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 297: 503-512.
33. LeBlanc, D.J., Lee, L.N., and Inamine, J.M. (1991) Cloning and nucleotide base sequence analysis of a spectinomycin adenyltransferase AAD(9) determinant from Enterococcus faecalis. Antimicrob Agents Chemother 35: 1804-1810.
34. Lloyd, A.J., Gilbey, A.M., Blewett, A.M., De, P.G., El, Z.A., Levesque, R.C., etal. (2008) Characterization of tRNA-dependent peptide bond formation by MurM in the synthesis of Streptococcus pneumoniae peptidoglycan. J Biol Chem 283: 6402-6417.
35. Martin, B., Humbert, O., Càmara, M., Guenzi, E., Walker, J., Mitchell, T., etal. (1992) A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 20: 3479-3483.
36. Mascher, T., Merai, M., Balmelle, N., de Saizieu, A., and Hakenbeck, R. (2003) The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. J Bacteriol 185: 60-70.
37. Maurer, P., Koch, B., Zerfaß, I., Krauß, J., van der Linden, M., Frère, J.-M., etal. (2008) Penicillin-binding protein 2x of Streptococcus pneumoniae: three new mutational pathways for remodelling an essential enzyme into a resistance determinant. J Mol Biol 376: 1403-1416.
38. Müller, M., Marx, P., Hakenbeck, R., and Brückner, R. (2011) Effect of new alleles of the histidine kinase gene ciaH on the activity of the response regulator CiaR in Streptococcus pneumoniae R6. Microbiology 157: 3104-3112.
39. Muñóz, R., Dowson, C.G., Daniels, M., Coffey, T.J., Martin, C., Hakenbeck, R., and Spratt, B.G. (1992) Genetics of resistance to third-generation cephalosporins in clinical isolates of Streptococcus pneumoniae. Mol Microbiol 6: 2461-2465.
40. Oggioni, M.R., and Claverys, J. (1999) Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology 145: 2647-2653.
41. Ottolenghi, E., and Hotchkiss, R.D. (1962) Release of genetic transforming agent from pneumococcal cultures during growth and disintegration. J Exp Med 116: 491-519.
42. Pagliero, E., Chesnel, L., Hopkins, J., Croizé, J., Dideberg, O., Vernet, T., and Di Guilmi, A.M. (2004) Biochemical characterization of Streptococcus pneumoniae penicillin-binding protein 2b and its implication in beta-lactam resistance. Antimicrob Agents Chemother 48: 1848-1855.
43. Paik, J., Kern, I., Lurz, R., and Hakenbeck, R. (1999) Mutational analysis of the Streptococcus pneumoniae bimodular class A penicillin-binding proteins. J Bacteriol 181: 3852-3856.
44. du Plessis, M., Bingen, E., and Klugman, K.P. (2002) Analysis of penicillin-binding protein genes of clinical isolates of Streptococcus pneumoniae with reduced susceptibility to amoxicillin. Antimicrob Agents Chemother 46: 2349-2357.
45. Reichmann, P., Varon, E., Günther, E., Reinert, R.R., Lütticken, R., Marton, A., etal. (1995) Penicillin-resistant Streptococcus pneumoniae in Germany: genetic relationship to clones from other European countries. J Med Microbiol 43: 377-385.
46. Reichmann, P., König, A., Liñares, J., Alcaide, F., Tenover, F.C., McDougal, L., etal. (1997) A global gene pool for high-level cephalosporin resistance in commensal Streptococcus spp. and Streptococcus pneumoniae. J Infect Dis 176: 1001-1012.
47. Reichmann, P., Nuhn, M., Denapaite, D., Brückner, R., Henrich, B., Maurer, P., etal. (2011) Genome of Streptococcus oralis strain Uo5. J Bacteriol 193: 2888-2889.
48. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.-A., and Barrell, B. (2000) Artemis: sequence visualisation and annotation. Bioinformatics 16: 944-945.
49. Sanbongi, Y., Ida, T., Ishikawa, M., Osaki, Y., Kataoka, H., Suzuki, T., etal. (2004) Complete sequences of six penicillin-binding protein genes from 40 Streptococcus pneumoniae clinical isolates collected in Japan. Antimicrob Agents Chemother 48: 2244-2250.
50. Sauvage, E., Kerff, F., Terrak, M., Ayala, J., and Charlier, P. (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32: 234-258.
51. Severin, A., and Tomasz, A. (1996) Naturally occurring peptidoglycan variants of Streptococcus pneumoniae. J Bacteriol 178: 168-174.
52. Sibold, C., Henrichsen, J., König, A., Martin, C., Chalkley, L., and Hakenbeck, R. (1994) Mosaic pbpX genes of major clones of penicillin-resistant Streptococcus pneumoniae have evolved from pbpX genes of a penicillin-sensitive Streptococcus oralis. Mol Microbiol 12: 1013-1023.
53. Smith, A.M., and Klugman, K.P. (1995) Alterations in penicillin-binding protein 2B from penicillin-resistant wild-type strains of Streptococcus pneumoniae. Antimicrob Agents Chemother 39: 859-867.
54. Smith, A.M., and Klugman, K.P. (2001) Alterations in MurM, a cell wall muropeptide branching enzyme, increase high-level penicillin and cephalosporin resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 45: 2393-2396.
55. Smith, A.M., Feldman, C., Massidda, O., McCarthy, K., Ndiweni, D., and Klugman, K.P. (2005) Altered PBP 2A and its role in the development of penicillin, cefotaxime, and ceftriaxone resistance in a clinical isolate of Streptococcus pneumoniae. Antimicrob Agents Chemother 49: 2002-2007.
56. Sung, C.K., Li, H., Claverys, J.P., and Morrison, D.A. (2001) An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl Environ Microbiol 67: 5190-5196.
57. Tiraby, J.-G., and Fox, M.S. (1974) Marker discrimination and mutagen-induced alterations in pneumococcal transformation. Genetics 77: 449-458.
58. Weber, B., Ehlert, K., Diehl, A., Reichmann, P., Labischinski, H., and Hakenbeck, R. (2000) The fib locus in Streptococcus pneumoniae is required for peptidoglycan crosslinking and PBP-mediated beta-lactam resistance. FEMS Microbiol Lett 188: 81-85.
59. Zhao, G., Meier, T.I., Hoskins, J., and McAllister, K.A. (2000) Identification and characterization of the penicillin-binding protein 2a of Streptococcus pneumoniae and its possible role in resistance to beta-lactam antibiotics. Antimicrob Agents Chemother 44: 1745-1748.