Commensal streptococci serve as a reservoir for β-lactam resistance genes in Streptococcus pneumoniae

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 6, 2015, Pages 3529-3540

  Jensen, Anders ^a   Valdórsson, Oskar ^a   Frimodt Møller, Niels ^b   Hollingshead, Susan ^c   Kilian, Mogens ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b Rigshospitalet   (Denmark)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BETA LACTAM ANTIBIOTIC; CEFALOTIN; CEFOTAXIME; CEFUROXIME; GAMMA GLUTAMYLTRANSFERASE; NUCLEOTIDE; OXACILLIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 1A; PENICILLIN BINDING PROTEIN 2B; PENICILLIN BINDING PROTEIN 2X; PENICILLIN G; PIPERACILLIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA LACTAM;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; HOMOLOGOUS RECOMBINATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST;

BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; MICROBIAL SENSITIVITY TESTS; STREPTOCOCCUS PNEUMONIAE;

EID: 84945292611     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00429-15     Document Type: Article

References (55)

1. Mitchell TJ. 2003. The pathogenesis of streptococcal infections: from tooth decay to meningitis. Nat Rev Microbiol 1:219-230. http://dx.doi.org/10.1038/nrmicro771.
2. Carapetis JR, Steer AC, Mulholland EK, Weber M. 2005. The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685-694. http://dx.doi.org/10.1016/S1473-3099(05)70267-X.
3. Henriques-Normark B. 2007. Molecular epidemiology and mechanisms for antibiotic resistance in Streptococcus pneumoniae, p 269-290. In Hakenbeck R, Chhatwal GS (ed), Molecular biology of streptococci. Horizon Press, Wymondham, Norfolk, United Kingdom.
4. Anonymous. 2013. Centers for Disease Control and Prevention. Streptococcus pneumoniae. Active Bacterial Core Surveillance report, Emerging Infections Program Network 2013. http://www.cdc.gov/abcs/reports-findings/survreports/spneu13.pdf.
5. Granizo JJ, Aguilar L, Casal J, García-Rey C, Dal-Ré R, Baquero F. 2000. Streptococcus pneumoniae resistance to erythromycin and penicillin in relation to macrolide and beta-lactam consumption in Spain (1979-1997). J Antimicrob Chemother 46:767-773. http://dx.doi.org/10.1093/jac/46.5.767.
6. Carratalá J, Alcaide F, Fernández-Sevilla A, Corbella X, Lińares J, Gudiol F. 1995. Bacteremia due to viridans streptococci that are highly resistant to penicillin: increase among neutropenic patients with cancer. Clin Infect Dis 20:1169-1173. http://dx.doi.org/10.1093/clinids/20.5.1169.
7. Doern GV, Ferraro MJ, Brueggemann AB, Ruoff KL. 1996. Emergence of high rates of antimicrobial resistance among viridans group streptococci in the United States. Antimicrob Agents Chemother 40:891-894.
8. Hakenbeck R, Bruckner R, Denapaite D, Maurer P. 2012. Molecular mechanisms of beta-lactam resistance in Streptococcus pneumoniae. Future Microbiol 7:395-410. http://dx.doi.org/10.2217/fmb.12.2.
9. Dowson CG, Hutchison A, Brannigan JA, George RC, Hansman D, Linares J, Tomasz A, Smith JM, Spratt BG. 1989. Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci U S A 86:8842-8846. http://dx.doi.org/10.1073/pnas.86.22.8842.
10. Laible G, Spratt BG, Hakenbeck R. 1991. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol 5:1993-2002. http://dx.doi.org/10.1111/j.1365-2958.1991.tb00821.x.
11. Martin C, Sibold C, Hakenbeck R. 1992. Relatedness of penicillinbinding protein 1a genes from different clones of penicillin-resistant Streptococcus pneumoniae isolated in South Africa and Spain. EMBO J 11:3831-3836.
12. Dowson CG, Hutchison A, Woodford N, Johnson AP, George RC, Spratt BG. 1990. Penicillin-resistant viridans streptococci have obtained altered penicillin-binding protein genes from penicillin-resistant strains of Streptococcus pneumoniae. Proc Natl Acad Sci U S A 87:5858-5862. http://dx.doi.org/10.1073/pnas.87.15.5858.
13. Chi F, Nolte O, Bergmann C, Ip M, Hakenbeck R. 2007. Crossing the barrier: evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, S. mitis and S. oralis. Int J Med Microbiol 297:503-512. http://dx.doi.org/10.1016/j.ijmm.2007.02.009.
14. Dowson CG, Coffey TJ, Kell C, Whiley RA. 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. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01723.x.
15. Reichmann P, Konig A, Linares J, Alcaide F, Tenover FC, McDougal L, Swidsinski S, Hakenbeck R. 1997. A global gene pool for high-level cephalosporin resistance in commensal Streptococcus species and Streptococcus pneumoniae. J Infect Dis 176:1001-1012. http://dx.doi.org/10.1086/516532.
16. Sibold C, Henrichsen J, Konig A, Martin C, Chalkley L, 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. http://dx.doi.org/10.1111/j.1365-2958.1994.tb01089.x.
17. Kilian M, Riley DR, Jensen A, Bruggemann H, Tettelin H. 2014. Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. mBio 5:e01490-14. http://dx.doi.org/10.1128/mBio.01490-14.
18. Amoroso A, Demares D, Mollerach M, Gutkind G, Coyette J. 2001. All detectable high-molecular-mass penicillin-binding proteins are modified in a high-level beta-lactam-resistant clinical isolate of Streptococcus mitis. Antimicrob Agents Chemother 45:2075-2081. http://dx.doi.org/10.1128/AAC.45.7.2075-2081.2001.
19. König A, Reinert RR, Hakenbeck R. 1998. Streptococcus mitis with unusually high level resistance to beta-lactam antibiotics. Microb Drug Resist 4:45-49. http://dx.doi.org/10.1089/mdr.1998.4.45.
20. Nakayama A, Takao A. 2003. Beta-lactam resistance in Streptococcus mitis isolated from saliva of healthy subjects. J Infect Chemother 9:321-327. http://dx.doi.org/10.1007/s10156-003-0286-Y.
21. Chewapreecha C, Marttinen P, Croucher NJ, Salter SJ, Harris SR, Mather AE, Hanage WP, Goldblatt D, Nosten FH, Turner C, Turner P, Bentley SD, Parkhill J. 2014. Comprehensive identification of single nucleotide polymorphisms associated with beta-lactam resistance within pneumococcal mosaic genes. PLoS Genet 10:e1004547. http://dx.doi.org/10.1371/journal.pgen.1004547.
22. Hsieh YC, Su LH, Hsu MH, Chiu CH. 2013. Alterations of penicillinbinding proteins in pneumococci with stepwise increase in beta-lactam resistance. Pathog Dis 67:84-88. http://dx.doi.org/10.1111/2049-632x.12018.
23. Bruckner LB, Korones DN, Karnauchow T, Hardy DJ, Gigliotti F. 2002. High incidence of penicillin resistance among alpha-hemolytic streptococci isolated from the blood of children with cancer. J Pediatr 140:20-26. http://dx.doi.org/10.1067/mpd.2002.118886.
24. Cole MF, Bryan S, Evans MK, Pearce CL, Sheridan MJ, Sura PA, Wientzen RL, Bowden GH. 1999. Humoral immunity to commensal oral bacteria in human infants: salivary secretory immunoglobulin A antibodies reactive with Streptococcus mitis biovar 1, Streptococcus oralis, Streptococcus mutans, and Enterococcus faecalis during the first two years of life. Infect Immun 67:1878-1886.
25. Razonable RR, Litzow MR, Khaliq Y, Piper KE, Rouse MS, Patel R. 2002. Bacteremia due to viridans group Streptococci with diminished susceptibility to levofloxacin among neutropenic patients receiving levofloxacin prophylaxis. Clin Infect Dis 34:1469-1474. http://dx.doi.org/10.1086/340352.
26. Bishop CJ, Aanensen DM, Jordan GE, Kilian M, Hanage WP, Spratt BG. 2009. Assigning strains to bacterial species via the internet. BMC Biol 7:3. http://dx.doi.org/10.1186/1741-7007-7-3.
27. Hoshino T, Fujiwara T, Kilian M. 2005. Use of phylogenetic and phenotypic analyses to identify nonhemolytic streptococci isolated from bacteremic patients. J Clin Microbiol 43:6073-6085. http://dx.doi.org/10.1128/JCM.43.12.6073-6085.2005.
28. Anonymous. 2014. Breakpoint tables for interpretation of MICs and zone diameters, version 4.0. The European Committee on Antimicrobial Susceptibility Testing. http://www.eucast.org.
29. Jensen A, Kilian M. 2012. Delineation of Streptococcus dysgalactiae, its subspecies, and its clinical and phylogenetic relationship to Streptococcus pyogenes. J Clin Microbiol 50:113-126. http://dx.doi.org/10.1128/JCM.05900-11.
30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
31. Marttinen P, Hanage WP, Croucher NJ, Connor TR, Harris SR, Bentley SD, Corander J. 2012. Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 40:e6. http://dx.doi.org/10.1093/nar/gkr928.
32. Asahi Y, Takeuchi Y, Ubukata K. 1999. Diversity of substitutions within or adjacent to conserved amino acid motifs of penicillin-binding protein 2X in cephalosporin-resistant Streptococcus pneumoniae isolates. Antimicrob Agents Chemother 43:1252-1255.
33. Chesnel L, Pernot L, Lemaire D, Champelovier D, Croize J, Dideberg O, Vernet T, Zapun A. 2003. The structural modifications induced by the M339F substitution in PBP2x from Streptococcus pneumoniae further decreases the susceptibility to beta-lactams of resistant strains. J Biol Chem 278:44448-44456. http://dx.doi.org/10.1074/jbc.M305948200.
34. Granger D, Boily-Larouche G, Turgeon P, Weiss K, Roger M. 2005. Genetic analysis of pbp2x in clinical Streptococcus pneumoniae isolates in Quebec, Canada. J Antimicrob Chemother 55:832-839. http://dx.doi.org/10.1093/jac/dki118.
35. Mouz N, Di Guilmi AM, Gordon E, Hakenbeck R, Dideberg O, Vernet T. 1999. Mutations in the active site of penicillin-binding protein PBP2x from Streptococcus pneumoniae. Role in the specificity for beta-lactam antibiotics. J Biol Chem 274:19175-19180.
36. Nichol KA, Zhanel GG, Hoban DJ. 2002. Penicillin-binding protein 1A, 2B, and 2X alterations in Canadian isolates of penicillin-resistant Streptococcus pneumoniae. Antimicrob Agents Chemother 46:3261-3264. http://dx.doi.org/10.1128/AAC.46.10.3261-3264.2002.
37. Carapito R, Chesnel L, Vernet T, Zapun A. 2006. Pneumococcal betalactam resistance due to a conformational change in penicillin-binding protein 2x. J Biol Chem 281:1771-1777. http://dx.doi.org/10.1074/jbc.M511506200.
38. Denapaite D, Bruckner R, Nuhn M, Reichmann P, Henrich B, Maurer P, Schahle Y, Selbmann P, Zimmermann W, Wambutt R, Hakenbeck R. 2010. The genome of Streptococcus mitis B6-what is a commensal? PLoS One 5:e9426. http://dx.doi.org/10.1371/journal.pone.0009426.
39. Maurer P, Koch B, Zerfass I, Krauss J, van der Linden M, Frere JM, Contreras-Martel C, Hakenbeck R. 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. http://dx.doi.org/10.1016/j.jmb.2007.12.058.
40. Cafini F, del Campo R, Alou L, Sevillano D, Morosini MI, Baquero F, Prieto J, Spanish Pneumococcal Network (G03/103). 2006. 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. http://dx.doi.org/10.1093/jac/dki442.
41. du Plessis M, Bingen E, Klugman KP. 2002. Analysis of penicillinbinding protein genes of clinical isolates of Streptococcus pneumoniae with reduced susceptibility to amoxicillin. Antimicrob Agents Chemother 46: 2349-2357. http://dx.doi.org/10.1128/AAC.46.8.2349-2357.2002.
42. Kosowska K, Jacobs MR, Bajaksouzian S, Koeth L, Appelbaum PC. 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. http://dx.doi.org/10.1128/AAC.48.10.4020-4022.2004.
43. Sanbongi Y, Ida T, Ishikawa M, Osaki Y, Kataoka H, Suzuki T, Kondo K, Ohsawa F, Yonezawa M. 2004. Complete sequences of six penicillinbinding protein genes from 40 Streptococcus pneumoniae clinical isolates collected in Japan. Antimicrob Agents Chemother 48:2244-2250. http://dx.doi.org/10.1128/AAC.48.6.2244-2250.2004.
44. Smith AM, Klugman KP. 1995. Alterations in penicillin-binding protein 2b from penicillin-resistant wild-type strains of Streptococcus pneumoniae. Antimicrob Agents Chemother 39:859-867. http://dx.doi.org/10.1128/AAC.39.4.859.
45. Smith AM, Klugman KP. 1998. Alterations in PBP 1A essential for highlevel penicillin resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 42:1329-1333.
46. Filipe SR, 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 U S A 97:4891-4896. http://dx.doi.org/10.1073/pnas.080067697.
47. Weber B, Ehlert K, Diehl A, Reichmann P, Labischinski H, Hakenbeck R. 2000. The fib locus in Streptococcus pneumoniae is required for peptidoglycan crosslinking and PBP-mediated beta-lactam resistance. Fems Microbiology Lett 188:81-85.
48. Kilian M, Poulsen K, Blomqvist T, Havarstein LS, Bek-Thomsen M, Tettelin H, Sorensen UBS. 2008. Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One 3:e2683. http://dx.doi.org/10.1371/journal.pone.0002683.
49. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, Cheng L, Pessia A, Aanensen DM, Mather AE, Page AJ, Salter SJ, Harris D, Nosten F, Goldblatt D, Corander J, Parkhill J, Turner P, Bentley SD. 2014. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46:305-309. http://dx.doi.org/10.1038/ng.2895.
50. Albarracín Orio AG, Piñas GE, Cortes PR, Cian MB, Echenique J. 2011. Compensatory evolution of pbp mutations restores the fitness cost imposed by beta-lactam resistance in Streptococcus pneumoniae. PLoS Pathog 7:e1002000. http://dx.doi.org/10.1371/journal.ppat.1002000.
51. Mostowy R, Croucher NJ, Hanage WP, Harris SR, Bentley S, Fraser C. 2014. Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution. PLoS Genet 10:e1004300. http://dx.doi.org/10.1371/journal.pgen.1004300.
52. Sauerbier J, Maurer P, Rieger M, Hakenbeck R. 2012. Streptococcus pneumoniae R6 interspecies transformation: genetic analysis of penicillin resistance determinants and genome-wide recombination events. Mol Microbiol 86:692-706. http://dx.doi.org/10.1111/mmi.12009.
53. Ghaffar F, Friedland IR, Katz K, Muniz LS, Smith JL, Davis P, Reynolds J, McCracken GH, Jr. 1999. Increased carriage of resistant nonpneumococcal alpha-hemolytic streptococci after antibiotic therapy. J Pediatr 135:618-623. http://dx.doi.org/10.1016/S0022-3476(99)70061-2.
54. Ghaffar F, Muniz LS, Katz K, Smith JL, Shouse T, Davis P, McCracken GH, Jr. 2002. Effects of large dosages of amoxicillin/clavulanate or azithromycin on nasopharyngeal carriage of Streptococcus pneumoniae, Haemophilus influenzae, nonpneumococcal alpha-hemolytic streptococci, and Staphylococcus aureus in children with acute otitis media. Clin Infect Dis 34:1301-1309. http://dx.doi.org/10.1086/340054.
55. Filipe SR, Severina E, Tomasz A. 2000. Distribution of the mosaic structured murM genes among natural populations of Streptococcus pneumoniae. J Bacteriol 182:6798-6805. http://dx.doi.org/10.1128/JB.182.23.6798-6805.2000.