Identification and characterization of a novel flagellum-dependent Salmonella-infecting bacteriophage, iEPS5

Applied and Environmental Microbiology

Volumn 79, Issue 16, 2013, Pages 4829-4837

  Choi, Younho ^a   Shin, Hakdong ^a   Lee, Ju Hoon ^b   Ryua, Sangryeol ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

COUNTER-CLOCKWISE; DOUBLE STRANDED DNA; FLAGELLAR FILAMENTS; GENOME SEQUENCING; INSERTION MUTANTS; OPEN READING FRAME; PHAGE ADSORPTIONS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

ADSORPTION; BACTERIOPHAGES; CELLS; DNA; SALMONELLA;

MUTAGENESIS;

VIRUS DNA;

ADSORPTION; BACTERIOPHAGE; DNA; GENE EXPRESSION; GENOME; MICROBIAL COMMUNITY; MUTATION; PATHOGEN;

ARTICLE; BACTERIOPHAGE; DNA SEQUENCE; FLAGELLUM; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; SALMONELLA PHAGE; SALMONELLA TYPHIMURIUM; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIROLOGY; VIRUS GENOME;

DNA, VIRAL; FLAGELLA; GENOME, VIRAL; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; SALMONELLA PHAGES; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS, DNA; SIPHOVIRIDAE;

EID: 84880996473     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00706-13     Document Type: Article

References (61)

1. Hyman P, Abedon ST. 2010. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 70:217-248.
2. Evans TJ, Crow MA, Williamson NR, Orme W, Thomson NR, Komitopoulou E, Salmond GP. 2010. Characterization of a broad-host-range flagellum-dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 156: 240-247.
3. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI. 2010. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol. J. Microbiol. 59:145-155.
4. Lindberg AA. 1973. Bacteriophage receptors. Annu. Rev. Microbiol. 27: 205-241.
5. Bonhivers M, Plancon L, Ghazi A, Boulanger P, le Maire M, Lambert O, Rigaud JL, Letellier L. 1998. FhuA, an Escherichia coli outer membrane protein with a dual function of transporter and channel which mediates the transport of phage DNA. Biochimie 80:363-369.
6. Hong J, Kim KP, Heu S, Lee SJ, Adhya S, Ryu S. 2008. Identification of host receptor and receptor-binding module of a newly sequenced T5-like phage EPS7. FEMS Microbiol. Lett. 289:202-209.
7. Mondigler M, Vogele RT, Heller KJ. 1995. Overproduced and purified receptor-binding protein Pb5 of bacteriophage-T5 binds to the T5 receptor protein FhuA. FEMS Microbiol. Lett. 130:293-300.
8. Kim M, Ryu S. 2011. Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar Typhimurium and Escherichia coli. Appl. Environ. Microbiol. 77: 2042-2050.
9. Incardona NL, Selvidge L. 1973. Mechanism of adsorption and eclipse of bacteriophage phi X174. II. Attachment and eclipse with isolated Escherichia coli cell wall lipopolysaccharide. J. Virol. 11:775-782.
10. Quirk AV, Sletten A, Hignett RC. 1976. Properties of phage-receptor lipopolysaccharide from Pseudomonas morsprunorum. J. Gen. Microbiol. 96:375-381.
11. Edwards S, Meynell GG. 1968. The widespread occurrence of enteric flagellar phages. J. Gen. Virol. 2:443-444.
12. Schade SZ, Adler J, Ris H. 1967. How bacteriophage chi attracts motile bacteria. J. Virol. 1:599-609.
13. Joys TM. 1965. Correlation between susceptibility to bacteriophage PBS1 and motility in Bacillus subtilis. J. Bacteriol. 90:1575-1577.
14. Samuel AD, Pitta TP, Ryu WS, Danese PN, Leung EC, Berg HC. 1999. Flagellar determinants of bacterial sensitivity to chi-phage. Proc. Natl. Acad. Sci. U. S. A. 96:9863-9866.
15. Guerrero-Ferreira RC, Viollier PH, Ely B, Poindexter JS, Georgieva M, Jensen GJ, Wright ER. 2011. Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. Proc. Natl. Acad. Sci. U. S. A. 108:9963-9968.
16. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465.
17. Macnab RM. 1986. Proton-driven bacterial flagellar motor. Methods Enzymol. 125:563-581.
18. Muramoto K, Macnab RM. 1998. Deletion analysis of MotA and MotB, components of the force-generating unit in the flagellar motor of Salmonella. Mol. Microbiol. 29:1191-1202.
19. Mariconda S, Wang Q, Harshey RM. 2006. A mechanical role for the chemotaxis system in swarming motility. Mol. Microbiol. 60:1590-1602.
20. Silversmith RE, Bourret RB. 1999. Throwing the switch in bacterial chemotaxis. Trends Microbiol. 7:16-22.
21. Hughes KT, Maloy SR. 2007. Advanced bacterial genetics: use of transposons and phage for genomic engineering. Academic Press, San Diego, CA.
22. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
23. Doublet B, Douard G, Targant H, Meunier D, Madec JY, Cloeckaert A. 2008. Antibiotic marker modifications of lambda Red and FLP helper plasmids, pKD46 and pCP20, for inactivation of chromosomal genes using PCR products in multidrug-resistant strains. J. Microbiol. Methods 75:359-361.
24. Soncini FC, Vescovi EG, Groisman EA. 1995. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J. Bacteriol. 177: 4364-4371.
25. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
26. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Park M, Lee JH, Shin H, Kim M, Choi J, Kang DH, Heu S, Ryu S. 2012. Characterization and comparative genomic analysis of a novel bacteriophage, SFP10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157:H7. Appl. Environ. Microbiol. 78:58-69.
28. Sambrook J, Russell WD. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
30. Zdobnov EM, Apweiler R. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
31. Kumar S, Nei M, Dudley J, Tamura K. 2008. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 9:299-306.
32. Kunisaki H, Tanji Y. 2010. Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli O157:H7 in anaerobic continuous culture. Appl. Microbiol. Biotechnol. 85:1533-1540.
33. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, Hou S, Layman D, Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E, Ryan E, Sun H, Florea L, Miller W, Stoneking T, Nhan M, Waterston R, Wilson RK. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
34. Kazaks A, Dislers A, Lipowsky G, Nikolajeva V, Tars K. 2012. Complete genome sequence of the Enterobacter cancerogenus bacteriophage Enc34. J. Virol. 86:11403-11404.
35. Onmus-Leone F, Hang J, Clifford RJ, Yang Y, Riley MC, Kuschner RA, Waterman PE, Lesho EP. 2013. Enhanced de novo assembly of high throughput pyrosequencing data using whole genome mapping. PLoS One 8:e61762. doi:10.1371/journal.pone.0061762.
36. Casjens SR, Gilcrease EB. 2009. Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol. Biol. 502:91-111.
37. Macnab RM. 2004. Type III flagellar protein export and flagellar assembly. Biochim. Biophys. Acta 1694:207-217.
38. Fan F, Ohnishi K, Francis NR, Macnab RM. 1997. The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol. Microbiol. 26:1035-1046.
39. Ohnishi K, Fan F, Schoenhals GJ, Kihara M, Macnab RM. 1997. The FliO, FliP, FliQ, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J. Bacteriol. 179:6092-6099.
40. Aldridge P, Karlinsey J, Hughes KT. 2003. The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol. Microbiol. 49:1333-1345.
41. Ohnishi K, Kutsukake K, Suzuki H, Iino T. 1990. Gene fliA encodes an alternative sigma factor specific for flagellar operons in Salmonella typhimurium. Mol. Gen. Genet. 221:139-147.
42. Dong T, Yu R, Schellhorn H. 2011. Antagonistic regulation of motility and transcriptome expression by RpoN and RpoS in Escherichia coli. Mol. Microbiol. 79:375-386.
43. Hengge-Aronis R. 2002. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-395.
44. Galperin MY. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188:4169-4182.
45. Andrewes FW. 1922. Studies in group-agglutination. I. The Salmonella group and its antigenic structure. J. Pathol. Bacteriol. 25:505-521.
46. Bonifield HR, Hughes KT. 2003. Flagellar phase variation in Salmonella enterica is mediated by a posttranscriptional control mechanism. J. Bacteriol. 185:3567-3574.
47. Magariyama Y, Yamaguchi S, Aizawa S. 1990. Genetic and behavioral analysis of flagellar switch mutants of Salmonella typhimurium. J. Bacteriol. 172:4359-4369.
48. Harshey RM. 2003. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57:249-273.
49. Ravid S, Matsumura P, Eisenbach M. 1986. Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the chemotaxis protein CheY. Proc. Natl. Acad. Sci. U. S. A. 83:7157-7161.
50. Togashi F, Yamaguchi S, Kihara M, Aizawa SI, Macnab RM. 1997. An extreme clockwise switch bias mutation in fliG of Salmonella typhimurium and its suppression by slow-motile mutations in motA and motB. J. Bacteriol. 179:2994-3003.
51. Yamaguchi S, Aizawa S, Kihara M, Isomura M, Jones CJ, Macnab RM. 1986. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J. Bacteriol. 168:1172-1179.
52. Hirano T, Yamaguchi S, Oosawa K, Aizawa S. 1994. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176:5439-5449.
53. Minamino T, Gonzalez-Pedrajo B, Yamaguchi K, Aizawa SI, Macnab RM. 1999. FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol. Microbiol. 34:295-304.
54. Waters RC, O'Toole PW, Ryan KA. 2007. The FliK protein and flagellar hook-length control. Protein Sci. 16:769-780.
55. Wu D, Van Valen D, Hu QC, Phillips R. 2010. Ion-dependent dynamics of DNA ejections for bacteriophage lambda. Biophys. J. 99:1101-1109.
56. Mosier-Boss PA, Lieberman SH, Andrews JM, Rohwer FL, Wegley LE, Breitbart M. 2003. Use of fluorescently labeled phage in the detection and identification of bacterial species. Appl. Spectrosc. 57:1138-1144.
57. Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T. 2006. Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol. Syst. Biol. 2:2006.0007.
58. Zhang X, Kelly SM, Bollen WS, Curtiss R, III. 1997. Characterization and immunogenicity of Salmonella typhimurium SL1344 and UK-1 delta crp and delta cdt deletion mutants. Infect. Immun. 65:5381-5387.
59. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
60. Durfee T, Nelson R, Baldwin S, Plunkett, G, III, Burland V, Mau B, Petrosino JF, Qin X, Muzny DM, Ayele M, Gibbs RA, Csorgo B, Posfai G, Weinstock GM, Blattner FR. 2008. The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J. Bacteriol. 190:2597-2606.
61. Poppe C, Smart N, Khakhria R, Johnson W, Spika J, Prescott J. 1998. Salmonella typhimurium DT104: a virulent and drug-resistant pathogen. Can. Vet. J. 39:559-565.