Genomic characterization of JG068, a novel virulent podovirus active against Burkholderia cenocepacia

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Lynch, Karlene H ^a   Abdu, Ashraf H ^a   Schobert, Max ^b   Dennis, Jonathan J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

symbol KMV like phages; Autographivirinae; Burkholderia cepacia complex; Galleria mellonella; Phage therapy; SAR endolysin

Indexed keywords

AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIOPHAGE JG068; BACTERIUM ISOLATE; BURKHOLDERIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA DOLOSA; BURKHOLDERIA MULTIVORANS; BURKHOLDERIA STABILIS; CONTROLLED STUDY; DNA BINDING; ESCHERICHIA COLI; GALLERIA MELLONELLA; GENE LOCUS; GENE SEQUENCE; GENOMICS; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORGANISMAL INTERACTION; PROMOTER REGION; SEQUENCE HOMOLOGY; DNA SEQUENCE; GENETICS; HOST RANGE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PODOVIRIDAE; REGULATOR GENE; SEWAGE; TRANSCRIPTION INITIATION SITE; ULTRASTRUCTURE; VIRION; VIROLOGY; VIRULENCE; VIRUS GENOME;

BACTERIA (MICROORGANISMS); BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA DOLOSA; BURKHOLDERIA MULTIVORANS; BURKHOLDERIA PSEUDOMALLEI; BURKHOLDERIA STABILIS; CAULOBACTER; ESCHERICHIA COLI; GALLERIA MELLONELLA; NEGIBACTERIA; RALSTONIA; T7-LIKE VIRUSES;

SEWAGE; VIRUS PROTEIN;

BASE SEQUENCE; BURKHOLDERIA CENOCEPACIA; GENOME, VIRAL; HOST SPECIFICITY; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PODOVIRIDAE; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SEWAGE; SOIL MICROBIOLOGY; TERMINATOR REGIONS, GENETIC; TRANSCRIPTION INITIATION SITE; VIRAL PROTEINS; VIRION; VIRULENCE;

EID: 84883128337     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-574     Document Type: Article

References (67)

1. Falagas ME, Bliziotis IA, Kasiakou SK, Samonis G, Athanassopoulou P, Michalopoulos A. Outcome of infections due to pandrug-resistant (PDR) Gram-negative bacteria. BMC Infect Dis 2005, 5:24. 10.1186/1471-2334-5-24, 1087841, 15819983.
2. Merril CR, Scholl D, Adhya SL. The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov 2003, 2:489-497. 10.1038/nrd1111, 12776223.
3. Bruttin A, Brüssow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 2005, 49:2874-2878. 10.1128/AAC.49.7.2874-2878.2005, 1168693, 15980363.
4. Merabishvili M, Pirnay J-P, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Van Parys L, Lavigne R, Volckaert G, Mattheus W, Verween G, De Corte P, Rose T, Jennes S, Zizi M, De Vos D, Vaneechoutte M. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS ONE 2009, 4:e4944. 10.1371/journal.pone.0004944, 2654153, 19300511.
5. Rhoads DD, Wolcott RD, Kuskowski MA, Wolcott BM, Ward LS, Sulakvelidze A. Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care 2009, 18:237-243.
6. Wright A, Hawkins CH, Änggård EE, Harper DR. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; A preliminary report of efficacy. Clin Otolaryngol 2009, 34:349-357. 10.1111/j.1749-4486.2009.01973.x, 19673983.
7. Mahenthiralingam E, Urban TA, Goldberg JB. The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 2005, 3:144-156. 10.1038/nrmicro1085, 15643431.
8. Zhou J, Chen Y, Tabibi S, Alba L, Garber E, Saiman L. Antimicrobial susceptibility and synergy studies of Burkholderia cepacia complex isolated from patients with cystic fibrosis. Antimicrob Agents Chemother 2007, 51:1085-1088. 10.1128/AAC.00954-06, 1803131, 17158942.
9. Adachi N, Tsukamoto S, Inoue Y, Azegami K. Control of bacterial seedling rot and seedling blight of rice by bacteriophage. Plant Dis 2012, 96:1033-1036.
10. Seed KD, Dennis JJ. Experimental bacteriophage therapy increases survival of Galleria mellonella larvae infected with clinically relevant strains of the Burkholderia cepacia complex. Antimicrob Agents Chemother 2009, 53:2205-2208. 10.1128/AAC.01166-08, 2681512, 19223640.
11. Lynch KH, Seed KD, Stothard P, Dennis JJ. Inactivation of Burkholderia cepacia complex phage KS9 gp41 identifies the phage repressor and generates lytic virions. J Virol 2010, 84:1276-1288. 10.1128/JVI.01843-09, 2812329, 19939932.
12. Carmody LA, Gill JJ, Summer EJ, Sajjan US, Gonzalez CF, Young RF, LiPuma JJ. Efficacy of bacteriophage therapy in a model of Burkholderia cenocepacia pulmonary infection. J Infect Dis 2010, 201:264-271. 10.1086/649227, 2814432, 20001604.
13. Lynch KH, Dennis JJ. Cangene gold medal award lecture - Genomic analysis and modification of Burkholderia cepacia complex bacteriophages. Can J Microbiol 2012, 58:221-235. 10.1139/w11-135, 22339239.
14. Lynch KH, Dennis JJ. Genomics of Burkholderia phages. Burkholderia: From Genomes to Function Hethersett: Horizon Scientific Press, Coenye T, Mahenthiralingam E, In press.
15. Summer EJ, Gonzalez CF, Bomer M, Carlile T, Embry A, Kucherka AM, Lee J, Mebane L, Morrison WC, Mark L, King MD, LiPuma JJ, Vidaver AK, Young R. Divergence and mosaicism among virulent soil phages of the Burkholderia cepacia complex. J Bacteriol 2006, 188:255-268. 10.1128/JB.188.1.255-268.2006, 1317576, 16352842.
16. Robinson SM, Hall J, Das A, Rosenbloom A, Gonzalez C, Young R, Summer EJ. M-015. Genomic analysis of virulent soil phages of Burkholderia http://ieg.ou.edu/asm2006/data/papers/M_015.htm.
17. Pirnay J-P, Verbeken G, Rose T, Jennes S, Zizi M, Huys I, Lavigne R, Merabishvili M, Vaneechoutte M, Buckling A, De Vos D. Introducing yesterday's phage therapy in today's medicine. Future Virol 2012, 7:379-390.
18. Seed KD, Dennis JJ. Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 2008, 76:1267-1275. 10.1128/IAI.01249-07, 2258804, 18195031.
19. Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JRW, Taylor P, Vandamme P. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 2000, 38:910-913. 86244, 10655415.
20. Coenye T, Vandamme P, LiPuma JJ, Govan JRW, Mahenthiralingam E. Updated version of the Burkholderia cepacia complex experimental strain panel. J Clin Microbiol 2003, 41:2797-2798. 10.1128/JCM.41.6.2797-2798.2003, 156479, 12791937.
21. Broad Institute Burkholderia dolosa database http://www.broadinstitute.org/annotation/genome/burkholderia_dolosa, Broad Institute.
22. Seed KD, Dennis JJ. Isolation and characterization of bacteriophages of the Burkholderia cepacia complex. FEMS Microbiol Lett 2005, 251:273-280. 10.1016/j.femsle.2005.08.011, 16140471.
23. Goudie AD, Lynch KH, Seed KD, Stothard P, Shrivastava S, Wishart DS, Dennis JJ. Genomic sequence and activity of KS10, a transposable phage of the Burkholderia cepacia complex. BMC Genomics 2008, 9:615. 10.1186/1471-2164-9-615, 2628397, 19094239.
24. Lynch KH, Stothard P, Dennis JJ. Genomic analysis and relatedness of P2-like phages of the Burkholderia cepacia complex. BMC Genomics 2010, 11:599. 10.1186/1471-2164-11-599, 3091744, 20973964.
25. Lynch KH, Stothard P, Dennis JJ. Characterization of DC1, a broad-host-range Bcep22-like podovirus. Appl Environ Microbiol 2012, 78:889-891. 10.1128/AEM.07097-11, 3264122, 22139000.
26. Lynch KH, Stothard P, Dennis JJ. Comparative analysis of two phenotypically-similar but genomically-distinct Burkholderia cenocepacia-specific bacteriophages. BMC Genomics 2012, 13:223. 10.1186/1471-2164-13-223, 3483164, 22676492.
27. Loutet SA, Flannagan RS, Kooi C, Sokol PA, Valvano MA. A complete lipopolysaccharide inner core oligosaccharide is required for resistance of Burkholderia cenocepacia to antimicrobial peptides and bacterial survival in vivo. J Bacteriol 2006, 188:2073-2080. 10.1128/JB.188.6.2073-2080.2006, 1428139, 16513737.
28. Ortega X, Silipo A, Saldfas MS, Bates CC, Molinaro A, Valvano MA. Biosynthesis and structure of the Burkholderia cenocepacia K56-2 lipopolysaccharide core oligosaccharide: Truncation of the core oligosaccharide leads to increased binding and sensitvity to polymyxin B. J Biol Chem 2009, 284:21738-21751. 10.1074/jbc.M109.008532, 2755896, 19525227.
29. Ackermann H-W. Frequency of morphological phage descriptions in the year 2000. Arch Virol 2001, 146:843-857. 10.1007/s007050170120, 11448025.
30. Casjens SR, Gilcrease EB. Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol Biol 2009, 502:91-111. 10.1007/978-1-60327-565-1_7, 3082370, 19082553.
31. Summer EJ. Preparation of a phage DNA fragment library for whole genome shotgun sequencing. Methods Mol Biol 2009, 502:27-46. 10.1007/978-1-60327-565-1_4, 19082550.
32. Lavigne R, Burkal'tseva MV, Robben J, Sykilinda NN, Kurochkina LP, Grymonprez B, Jonckx B, Krylov VN, Mesyanzhinov VV, Volckaert G. The genome of bacteriophage φ{symbol}KMV, a T7-like virus infecting Pseudomonas aeruginosa. Virology 2003, 312:49-59. 10.1016/S0042-6822(03)00123-5, 12890620.
33. Ceyssens P-J, Lavigne R, Mattheus W, Chibeu A, Hertveldt K, Mast J, Robben J, Volckaert G. Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: establishment of the φ{symbol}KMV subgroup within the T7 supergroup. J Bacteriol 2006, 188:6924-6931. 10.1128/JB.00831-06, 1595506, 16980495.
34. Adriaenssens EM, Ceyssens P-J, Dunon V, Ackermann H-W, Van Vaerenbergh J, Maes M, De Proft M, Lavigne R. Bacteriophages LIMElight and LIMEzero of Pantoea agglomerans, belonging to the "φ{symbol}KMV-like viruses". Appl Environ Microbiol 2011, 77:3443-3450. 10.1128/AEM.00128-11, 3126476, 21421778.
35. Lavigne R, Seto D, Mahadevan P, Ackermann H-W, Kropinski AM. Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 2008, 159:406-414. 10.1016/j.resmic.2008.03.005, 18555669.
36. Abbasifar R, Kropinski AM, Sabour PM, Ackermann H-W, Alanis Villa A, Abbasifar A, Griffiths MW. The genome of Cronobacter sakazakii bacteriophage vB_CsaP_GAP227 suggests a new genus within the Autographivirinae. Genome Announc 2013, 1:e00122-12. 10.1128/genomeA.00122-12, 3569369, 23409275.
37. Mahadevan P, King JF, Seto D. CGUG: in silico proteome and genome parsing tool for the determination of "core" and unique genes in the analysis of genomes up to ca. 1.9 Mb. BMC Res Notes 2009, 2:168. 10.1186/1756-0500-2-168, 2738686, 19706165.
38. Molineux IJ. The T7 Group. The Bacteriophages 2006, 277-301. New York: Oxford University Press, Calendar R, 2.
39. Casjens S. Prophages and bacterial genomics: What have we learned so far?. Mol Microbiol 2003, 49:277-300. 10.1046/j.1365-2958.2003.03580.x, 12886937.
40. Kawasaki T, Shimizu M, Satsuma H, Fujiwara A, Fujie M, Usami S, Yamada T. Genomic characterization of Ralstonia solanacearum phage φ{symbol}RSB1, a T7-like wide-host-range phage. J Bacteriol 2009, 191:422-427. 10.1128/JB.01263-08, 2612426, 18952798.
41. Lavigne R, Villegas A, Kropinksi AM. In silico characterization of DNA motifs with particular reference to promoters and terminators. Methods Mol Biol 2009, 502:113-129. 10.1007/978-1-60327-565-1_8, 19082554.
42. Lavigne R, Noben JP, Hertveldt K, Ceyssens P-J, Briers Y, Dumont D, Roucourt B, Krylov VN, Mesyanzhinov VV, Robben J, Volckaert G. The structural proteome of Pseudomonas aeruginosa bacteriophage φ{symbol}KMV. Microbiology 2006, 152:529-534. 10.1099/mic.0.28431-0, 16436440.
43. Briers Y, Peeters LM, Volckaert G, Lavigne R. The lysis cassette of bacteriophage φ{symbol}KMV encodes a signal-arrest-release endolysin and a pinholin. Bacteriophage 2011, 1:25-30. 10.4161/bact.1.1.14868, 3109451, 21687532.
44. Dobbins AT, George M, Basham DA, Ford ME, Houtz JM, Pedulla ML, Lawrence JG, Hatfull GF, Hendrix RW. Complete genomic sequence of the virulent Salmonella bacteriophage SP6. J Bacteriol 2004, 186:1933-1944. 10.1128/JB.186.7.1933-1944.2004, 374404, 15028677.
45. Walmagh M, Boczkowska B, Grymonprez B, Briers Y, Drulis-Kawa Z, Lavigne R. Characterization of five novel endolysins from Gram-negative infecting bacteriophages. Appl Microbiol Biotechnol 2012
46. Gill JJ, Summer EJ, Russell WK, Cologna SM, Carlile TM, Fuller AC, Kitsopoulos K, Mebane LM, Parkinson BN, Sullivan D, Carmody LA, Gonzalez CF, LiPuma JJ, Young R. Genomes and characterization of phages Bcep22 and BcepIL02, founders of a novel phage type in Burkholderia cenocepacia. J Bacteriol 2011, 193:5300-5313. 10.1128/JB.05287-11, 3187461, 21804006.
47. Garbe J, Bunk B, Rohde M, Schobert M. Sequencing and characterization of Pseudomonas aeruginosa phage JG004. BMC Microbiol 2011, 11:102. 10.1186/1471-2180-11-102, 3120641, 21569567.
48. Promega Corporation DNA Isolation From Lambda Lysates Using the Wizard® DNA Clean-Up System http://www.promega.ca/resources/articles/pubhub/enotes/dna-isolation-from-lambda-lysates-using-the-wizard-dna-cleanup-system, Promega Corporation.
49. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Swidan F, Thierer T, Wilson A. Geneious v5.6 http://www.geneious.com.
50. Reese MG. Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 2001, 26:51-56. 10.1016/S0097-8485(01)00099-7, 11765852.
51. Lavigne R, Sun WD, Volckaert G. PHIRE, a deterministic approach to reveal regulatory elements in bacteriophage genomes. Bioinformatics 2004, 20:629-635. 10.1093/bioinformatics/btg456, 15033869.
52. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14:1188-1190. 10.1101/gr.849004, 419797, 15173120.
53. Kingsford CL, Ayanbule K, Salzberg SL. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 2007, 8:R22. 10.1186/gb-2007-8-2-r22, 1852404, 17313685.
54. Lukashin AV, Borodovsky M. GeneMark.hmm: New solutions for gene finding. Nucleic Acids Res 1998, 26:1107-1115. 10.1093/nar/26.4.1107, 147337, 9461475.
55. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
56. Söding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33:W244-W248. 10.1093/nar/gki408, 1160169, 15980461.
57. Marchler-Bauer A, Bryant SH. CD-Search: Protein domain annotations on the fly. Nucleic Acids Res 2004, 32:W327-W331. 10.1093/nar/gkh454, 441592, 15215404.
58. NCBI ORF Finder http://www.ncbi.nlm.nih.gov/projects/gorf, NCBI.
59. GenSkew - visualization of nucleotide skew in genome sequences http://genskew.csb.univie.ac.at.
60. Vincze T, Posfai J, Roberts RJ. NEBcutter: A program to cleave DNA with restriction enzymes. Nucleic Acids Res 2003, 31:3688-3691. 10.1093/nar/gkg526, 168933, 12824395.
61. Saha S, Raghava GP. BTXpred: prediction of bacterial toxins. In Silico Biol 2007, 7:405-412.
62. Transcription Terminator Prediction http://pepper.molgenrug.nl/index.php/pepper-tools/terminator-predictie.
63. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 2001, 305:567-580. 10.1006/jmbi.2000.4315, 11152613.
64. Viklund H, Elofsson A. OCTOPUS: Improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 2008, 24:1662-1668. 10.1093/bioinformatics/btn221, 18474507.
65. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
66. Juncker AS, Willenbrock H, von Heijne G, Brunak S, Nielsen H, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 2003, 12:1652-1662. 10.1110/ps.0303703, 2323952, 12876315.
67. Silhavy TJ, Berman ML, Enquist LW. Experiments with Gene Fusions 1984, Cold Spring Harbor Laboratory: Cold Spring Harbor.