A genomic approach to understand interactions between Streptococcus pneumoniae and its bacteriophages

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Leprohon, Philippe ^a,b   Gingras, Hélène ^a,b   Ouennane, Siham ^b   Moineau, Sylvain ^b   Ouellette, Marc ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Bacteriophage; GntR regulator; Resistance; Streptococcus pneumoniae; Whole genome sequencing

Indexed keywords

RESTRICTION ENDONUCLEASE;

ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE DP 1; BACTERIOPHAGE SOCP; BACTERIUM MUTANT; CONTROLLED STUDY; CROSS RESISTANCE; GENE INACTIVATION; GENE MUTATION; GENE SEQUENCE; NONHUMAN; STREPTOCOCCUS PNEUMONIAE; VIRUS ATTACHMENT; VIRUS GENOME; VIRUS REPLICATION; ADSORPTION; GENETICS; GENOMICS; HOST PATHOGEN INTERACTION; MUTATION; PHYSIOLOGY; VIROLOGY;

ADSORPTION; BACTERIOPHAGES; GENOMICS; HOST-PATHOGEN INTERACTIONS; MUTATION; STREPTOCOCCUS PNEUMONIAE; VIRUS REPLICATION;

EID: 84960354018     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2134-8     Document Type: Article

References (78)

1. Ardanuy C, de la Campa AG, Garcia E, Fenoll A, Calatayud L, Cercenado E, et al. Spread of Streptococcus pneumoniae serotype 8-ST63 multidrug-resistant recombinant Clone, Spain. Emerg Infect Dis. 2014;20(11):1848-56.
2. Golden AR, Adam HJ, Gilmour MW, Baxter MR, Martin I, Nichol KA, et al. Assessment of multidrug resistance, clonality and virulence in non-PCV-13 Streptococcus pneumoniae serotypes in Canada, 2011-13. J Antimicrob Chemother. 2015;70(7):1960-4.
3. Jones RN, Sader HS, Mendes RE, Flamm RK. Update on antimicrobial susceptibility trends among Streptococcus pneumoniae in the United States: report of ceftaroline activity from the SENTRY Antimicrobial Surveillance Program (1998-2011). Diagn Microbiol Infect Dis. 2013;75(1):107-9.
4. McCarthy M. CDC calls for urgent action to combat rise of drug resistant pathogens. BMJ. 2013;347:f5649.
5. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis. 2013;13(12):1057-98.
6. McCullers JA, Karlstrom A, Iverson AR, Loeffler JM, Fischetti VA. Novel strategy to prevent otitis media caused by colonizing Streptococcus pneumoniae. PLoS Pathog. 2007;3(3):e28.
7. Loeffler JM, Djurkovic S, Fischetti VA. Phage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia. Infect Immun. 2003;71(11):6199-204.
8. Doehn JM, Fischer K, Reppe K, Gutbier B, Tschernig T, Hocke AC, et al. Delivery of the endolysin Cpl-1 by inhalation rescues mice with fatal pneumococcal pneumonia. J Antimicrob Chemother. 2013;68(9):2111-7.
9. Witzenrath M, Schmeck B, Doehn JM, Tschernig T, Zahlten J, Loeffler JM, et al. Systemic use of the endolysin Cpl-1 rescues mice with fatal pneumococcal pneumonia. Crit Care Med. 2009;37(2):642-9.
10. Diaz E, Lopez R, Garcia JL. EJ-1, a temperate bacteriophage of Streptococcus pneumoniae with a Myoviridae morphotype. J Bacteriol. 1992;174(17):5516-25.
11. Gindreau E, Lopez R, Garcia P. MM1, a temperate bacteriophage of the type 23F Spanish/USA multiresistant epidemic clone of Streptococcus pneumoniae: structural analysis of the site-specific integration system. J Virol. 2000;74(17):7803-13.
12. McDonnell M, Lain R, Tomasz A. "Diplophage": a bacteriophage of Diplococcus pneumoniae. Virology. 1975;63(2):577-82.
13. Obregon V, Garcia P, Lopez R, Garcia JL. VO1, a temperate bacteriophage of the type 19A multiresistant epidemic 8249 strain of Streptococcus pneumoniae: analysis of variability of lytic and putative C5 methyltransferase genes. Microb Drug Resist. 2003;9(1):7-15.
14. Romero A, Lopez R, Lurz R, Garcia P. Temperate bacteriophages of Streptococcus pneumoniae that contain protein covalently linked to the 5' ends of their DNA. J Virol. 1990;64(10):5149-55.
15. Romero P, Croucher NJ, Hiller NL, Hu FZ, Ehrlich GD, Bentley SD, et al. Comparative genomic analysis of ten Streptococcus pneumoniae temperate bacteriophages. J Bacteriol. 2009;191(15):4854-62.
16. Ronda C, Lopez R, Garcia E. Isolation and characterization of a new bacteriophage, Cp-1, infecting Streptococcus pneumoniae. J Virol. 1981;40(2):551-9.
17. Ronda C, Lopez R, Tomasz A, Portoles A. Transfection of Streptococcus pneumoniae with bacteriophage DNA. J Virol. 1978;26(2):221-5.
18. Tiraby JG, Tiraby E, Fox MS. Pneumococcal bacteriophages. Virology. 1975;68(2):566-9.
19. Bernheimer HP. Lysogenic pneumococci and their bacteriophages. J Bacteriol. 1979;138(2):618-24.
20. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, et al. Rapid pneumococcal evolution in response to clinical interventions. Science. 2011;331(6016):430-4.
21. Ramirez M, Severina E, Tomasz A. A high incidence of prophage carriage among natural isolates of Streptococcus pneumoniae. J Bacteriol. 1999;181(12):3618-25.
22. Loeffler JM, Fischetti VA. Lysogeny of Streptococcus pneumoniae with MM1 phage: improved adherence and other phenotypic changes. Infect Immun. 2006;74(8):4486-95.
23. Sabri M, Hauser R, Ouellette M, Liu J, Dehbi M, Moeck G, et al. Genome annotation and intraviral interactome for the Streptococcus pneumoniae virulent phage Dp-1. J Bacteriol. 2011;193(2):551-62.
24. Martin AC, Lopez R, Garcia P. Analysis of the complete nucleotide sequence and functional organization of the genome of Streptococcus pneumoniae bacteriophage Cp-1. J Virol. 1996;70(6):3678-87.
25. Ouennane S, Leprohon P, Moineau S. Diverse virulent pneumophages infect Streptococcus mitis. PLoS One. 2015;10(2):e0118807.
26. Samson JE, Magadan AH, Sabri M, Moineau S. Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol. 2013;11(10):675-87.
27. Bernheimer HP, Tiraby JG. Inhibition of phage infection by pneumococcus capsule. Virology. 1976;73(1):308-9.
28. Bender MH, Cartee RT, Yother J. Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J Bacteriol. 2003;185(20):6057-66.
29. Lopez R, Ronda C, Tomasz A, Portoles A. Properties of "diplophage": a lipid-containing bacteriophage. J Virol. 1977;24(1):201-10.
30. Bishop-Lilly KA, Plaut RD, Chen PE, Akmal A, Willner KM, Butani A, et al. Whole genome sequencing of phage resistant Bacillus anthracis mutants reveals an essential role for cell surface anchoring protein CsaB in phage AP50c adsorption. Virol J. 2012;9:246.
31. Castillo D, Christiansen RH, Dalsgaard I, Madsen L, Middelboe M. Bacteriophage resistance mechanisms in the fish pathogen Flavobacterium psychrophilum: linking genomic mutations to changes in bacterial virulence factors. Appl Environ Microbiol. 2015;81(3):1157-67.
32. Denes T, den Bakker HC, Tokman JI, Guldimann C, Wiedmann M. Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption. Appl Environ Microbiol. 2015;81(13):4295-305.
33. Billal DS, Feng J, Leprohon P, Legare D, Ouellette M. Whole genome analysis of linezolid resistance in Streptococcus pneumoniae reveals resistance and compensatory mutations. BMC Genomics. 2011;12:512.
34. Fani F, Brotherton MC, Leprohon P, Ouellette M. Genomic analysis and reconstruction of cefotaxime resistance in Streptococcus pneumoniae. J Antimicrob Chemother. 2013;68(8):1718-27.
35. Fani F, Leprohon P, Legare D, Ouellette M. Whole genome sequencing of penicillin-resistant Streptococcus pneumoniae reveals mutations in penicillin-binding proteins and in a putative iron permease. Genome Biol. 2011;12(11):R115.
36. Fani F, Leprohon P, Zhanel GG, Bergeron MG, Ouellette M. Genomic analyses of DNA transformation and penicillin resistance in Streptococcus pneumoniae clinical isolates. Antimicrob Agents Chemother. 2014;58(3):1397-403.
37. Feng J, Lupien A, Gingras H, Wasserscheid J, Dewar K, Legare D, et al. Genome sequencing of linezolid-resistant Streptococcus pneumoniae mutants reveals novel mechanisms of resistance. Genome Res. 2009;19(7):1214-23.
38. Lupien A, Billal DS, Fani F, Soualhine H, Zhanel GG, Leprohon P, et al. Genomic characterization of ciprofloxacin resistance in a laboratory-derived mutant and a clinical isolate of Streptococcus pneumoniae. Antimicrob Agents Chemother. 2013;57(10):4911-9.
39. Lupien A, Gingras H, Bergeron MG, Leprohon P, Ouellette M. Multiple mutations and increased RNA expression in tetracycline-resistant Streptococcus pneumoniae as determined by genome-wide DNA and mRNA sequencing. J Antimicrob Chemother. 2015;70(7):1946-59.
40. Sung CK, Li H, Claverys JP, Morrison DA. An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl Environ Microbiol. 2001;67(11):5190-6.
41. Hoskisson PA, Rigali S. Chapter 1: Variation in form and function the helix-turn-helix regulators of the GntR superfamily. Adv Appl Microbiol. 2009;69:1-22.
42. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol. 2010;8(5):317-27.
43. Aravind L, Anantharaman V. HutC/FarR-like bacterial transcription factors of the GntR family contain a small molecule-binding domain of the chorismate lyase fold. FEMS Microbiol Lett. 2003;222(1):17-23.
44. Arai H, Akahira S, Ohishi T, Kudo T. Adaptation of Comamonas testosteroni TA441 to utilization of phenol by spontaneous mutation of the gene for a trans-acting factor. Mol Microbiol. 1999;33(6):1132-40.
45. Gorelik M, Lunin VV, Skarina T, Savchenko A. Structural characterization of GntR/HutC family signaling domain. Protein Sci. 2006;15(6):1506-11.
46. Bidossi A, Mulas L, Decorosi F, Colomba L, Ricci S, Pozzi G, et al. A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS One. 2012;7(3):e33320.
47. Jeong JK, Kwon O, Lee YM, Oh DB, Lee JM, Kim S, et al. Characterization of the Streptococcus pneumoniae BgaC protein as a novel surface beta-galactosidase with specific hydrolysis activity for the Galbeta1-3GlcNAc moiety of oligosaccharides. J Bacteriol. 2009;191(9):3011-23.
48. Terra VS, Homer KA, Rao SG, Andrew PW, Yesilkaya H. Characterization of novel beta-galactosidase activity that contributes to glycoprotein degradation and virulence in Streptococcus pneumoniae. Infect Immun. 2010;78(1):348-57.
49. Sijtsma L, Sterkenburg A, Wouters JT. Properties of the Cell Walls of Lactococcus lactis subsp. cremoris SK110 and SK112 and Their Relation to Bacteriophage Resistance. Appl Environ Microbiol. 1988;54(11):2808-11.
50. Ugalde RA, Coira JA, Brill WJ. Biosynthesis of a galactose-and galacturonic acid-containing polysaccharide in Rhizobium meliloti. J Bacteriol. 1986;168(1):270-5.
51. Ugalde RA, Handelsman J, Brill WJ. Role of galactosyltransferase activity in phage sensitivity and nodulation competitiveness of Rhizobium meliloti. J Bacteriol. 1986;166(1):148-54.
52. Sijtsma L, Wouters JT, Hellingwerf KJ. Isolation and characterization of lipoteichoic acid, a cell envelope component involved in preventing phage adsorption, from Lactococcus lactis subsp. cremoris SK110. J Bacteriol. 1990;172(12):7126-30.
53. Lopez R, Garcia E, Garcia P, Ronda C, Tomasz A. Choline-containing bacteriophage receptors in Streptococcus pneumoniae. J Bacteriol. 1982;151(3):1581-90.
54. Larson TJ, Ehrmann M, Boos W. Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem. 1983;258(9):5428-32.
55. Fan X, Goldfine H, Lysenko E, Weiser JN. The transfer of choline from the host to the bacterial cell surface requires glpQ in Haemophilus influenzae. Mol Microbiol. 2001;41(5):1029-36.
56. Schmidl SR, Otto A, Lluch-Senar M, Pinol J, Busse J, Becher D, et al. A trigger enzyme in Mycoplasma pneumoniae: impact of the glycerophosphodiesterase GlpQ on virulence and gene expression. PLoS Pathog. 2011;7(9):e1002263.
57. Figueiredo TA, Sobral RG, Ludovice AM, Almeida JM, Bui NK, Vollmer W, et al. Identification of genetic determinants and enzymes involved with the amidation of glutamic acid residues in the peptidoglycan of Staphylococcus aureus. PLoS Pathog. 2012;8(1):e1002508.
58. Munch D, Roemer T, Lee SH, Engeser M, Sahl HG, Schneider T. Identification and in vitro analysis of the GatD/MurT enzyme-complex catalyzing lipid II amidation in Staphylococcus aureus. PLoS Pathog. 2012;8(1):e1002509.
59. Zapun A, Philippe J, Abrahams KA, Signor L, Roper DI, Breukink E, et al. In vitro reconstitution of peptidoglycan assembly from the Gram-positive pathogen Streptococcus pneumoniae. ACS Chem Biol. 2013;8(12):2688-96.
60. Bui NK, Eberhardt A, Vollmer D, Kern T, Bougault C, Tomasz A, et al. Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal Biochem. 2012;421(2):657-66.
61. Sutherland E, Coe L, Raleigh EA. McrBC: a multisubunit GTP-dependent restriction endonuclease. J Mol Biol. 1992;225(2):327-48.
62. Pieper U, Pingoud A. A mutational analysis of the PD...D/EXK motif suggests that McrC harbors the catalytic center for DNA cleavage by the GTP-dependent restriction enzyme McrBC from Escherichia coli. Biochemistry. 2002;41(16):5236-44.
63. Kruger T, Wild C, Noyer-Weidner M. McrB: a prokaryotic protein specifically recognizing DNA containing modified cytosine residues. EMBO J. 1995;14(11):2661-9.
64. Pieper U, Brinkmann T, Kruger T, Noyer-Weidner M, Pingoud A. Characterization of the interaction between the restriction endonuclease McrBC from E. coli and its cofactor GTP. J Mol Biol. 1997;272(2):190-9.
65. Gast FU, Brinkmann T, Pieper U, Kruger T, Noyer-Weidner M, Pingoud A. The recognition of methylated DNA by the GTP-dependent restriction endonuclease McrBC resides in the N-terminal domain of McrB. Biol Chem. 1997;378(9):975-82.
66. Pieper U, Schweitzer T, Groll DH, Pingoud A. Defining the location and function of domains of McrB by deletion mutagenesis. Biol Chem. 1999;380(10):1225-30.
67. Pieper U, Schweitzer T, Groll DH, Gast FU, Pingoud A. The GTP-binding domain of McrB: more than just a variation on a common theme? J Mol Biol. 1999;292(3):547-56.
68. Valentino MD, McGuire AM, Rosch JW, Bispo PJ, Burnham C, Sanfilippo CM, et al. Unencapsulated Streptococcus pneumoniae from conjunctivitis encode variant traits and belong to a distinct phylogenetic cluster. Nat Commun. 2014;5:5411.
69. Donkor ES. Understanding the pneumococcus: transmission and evolution. Front Cell Infect Microbiol. 2013;3:7.
70. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, Cheng L, et al. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet. 2014;46(3):305-9.
71. Chewapreecha C, Marttinen P, Croucher NJ, Salter SJ, Harris SR, Mather AE, et al. Comprehensive identification of single nucleotide polymorphisms associated with beta-lactam resistance within pneumococcal mosaic genes. PLoS Genet. 2014;10(8):e1004547.
72. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078-9.
73. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.
74. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60.
75. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5.
76. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning. New York: Cold Spring Harbour laboratory; 1989.
77. Hoskins J, Alborn Jr WE, Arnold J, Blaszczak LC, Burgett S, DeHoff BS, et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol. 2001;183(19):5709-17.
78. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, Wayne KJ, et al. Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol. 2007;189(1):38-51.