Two T7-like Bacteriophages, K5-2 and K5-4, Each Encodes Two Capsule Depolymerases: Isolation and Functional Characterization

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Hsieh, Pei Fang ^a   Lin, Hsiao Hsuan ^a,b   Lin, Tzu Lung ^a   Chen, Yi Yin ^c   Wang, Jin Town ^a,d  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSULAR-POLYSACCHARIDE GALACTOHYDROLASE; GLYCOSIDASE; VIRAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; BACTERIOPHAGE; BACTERIUM IDENTIFICATION; CLASSIFICATION; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KLEBSIELLA INFECTION; KLEBSIELLA PNEUMONIAE; METABOLISM; MICROBIOLOGY; MORTALITY; MOUSE; MUTATION; OPEN READING FRAME; PATHOGENICITY; VIROLOGY; VIRUS GENOME;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL TYPING TECHNIQUES; BACTERIOPHAGES; GENE EXPRESSION; GENOME, VIRAL; GLYCOSIDE HYDROLASES; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MICE; MUTATION; OPEN READING FRAMES; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS;

EID: 85021763893     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-04644-2     Document Type: Article

References (68)

1. Podschun, R. & Ullmann, U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 11, 589-603 (1998).
2. Ramphal, R. & Ambrose, P. G. Extended-spectrum beta-lactamases and clinical outcomes: current data. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 42(Suppl 4), S164-172, doi: 10.1086/500663 (2006).
3. Ko, W. C. et al. Community-Acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerging infectious diseases 8, 160-166 (2002).
4. Tsai, F. C., Huang, Y. T., Chang, L. Y. & Wang, J. T. Pyogenic liver abscess as endemic disease, Taiwan. Emerging infectious diseases 14, 1592-1600 (2008).
5. Cheng, D. L., Liu, Y. C., Yen, M. Y., Liu, C. Y. & Wang, R. S. Septic metastatic lesions of pyogenic liver abscess. Their association with Klebsiella pneumoniae bacteremia in diabetic patients. Arch Intern Med 151, 1557-1559 (1991).
6. Chiu, C. T., Lin, D. Y. & Liaw, Y. F. Metastatic septic endophthalmitis in pyogenic liver abscess. J Clin Gastroenterol 10, 524-527 (1988).
7. Fung, C. P. et al. A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis? Gut 50, 420-424 (2002).
8. Liu, Y. C., Cheng, D. L. & Lin, C. L. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med 146, 1913-1916 (1986).
9. Fang, C. T. et al. Klebsiella pneumoniae genotype K1: An emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 45, 284-293 (2007).
10. Chung, D. R. et al. Emerging invasive liver abscess caused by K1 serotype Klebsiella pneumoniae in Korea. J Infect 54, 578-583 (2007).
11. Cortes, G. et al. Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infection and immunity 70, 2583-2590 (2002).
12. Fang, C. T., Chuang, Y. P., Shun, C. T., Chang, S. C. & Wang, J. T. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. The Journal of experimental medicine 199, 697-705 (2004).
13. Lin, Y. T., Wang, Y. P., Wang, F. D. & Fung, C. P. Community-onset Klebsiella pneumoniae pneumonia in Taiwan: clinical features of the disease and associated microbiological characteristics of isolates from pneumonia and nasopharynx. Frontiers in microbiology 9, 122, doi: 10.3389/fmicb.2015.00122 (2015).
14. Lee, I. R. et al. Differential host susceptibility and bacterial virulence factors driving Klebsiella liver abscess in an ethnically diverse population. Scientific reports 6, 29316, doi: 10.1038/srep29316 (2016).
15. Chang, S. C., Fang, C. T., Hsueh, P. R., Chen, Y. C. & Luh, K. T. Klebsiella pneumoniae isolates causing liver abscess in Taiwan. Diagnostic microbiology and infectious disease 37, 279-284 (2000).
16. Kang, C. I. et al. Community-Acquired versus nosocomial Klebsiella pneumoniae bacteremia: clinical features, treatment outcomes, and clinical implication of antimicrobial resistance. Journal of Korean medical science 21, 816-822, doi: 10.3346/jkms.2006.21.5.816 (2006).
17. Su, S. C. et al. Community-Acquired liver abscess caused by serotype K1 Klebsiella pneumoniae with CTX-M-15-Type extended-spectrum beta-lactamase. Antimicrobial agents and chemotherapy 52, 804-805, doi: 10.1128/AAC.01269-07 (2008).
18. Gupta, N., Limbago, B. M., Patel, J. B. & Kallen, A. J. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 53, 60-67, doi: 10.1093/cid/cir202 (2011).
19. Brisse, S. et al. Wzi Gene sequencing, a rapid method for determination of capsular type for Klebsiella strains. J Clin Microbiol 51, 4073-4078, doi: 10.1128/JCM.01924-13 (2013).
20. MA, Ø. I. F.-A. New Klebsiella capsular antigen K82 and the deletion of five of those previously assigned. International journal of systematic bacteriology 27, 386-387 (1977).
21. Pan, Y. J. et al. Capsular polysaccharide synthesis regions in Klebsiella pneumoniae serotype K57 and a new capsular serotype. J Clin Microbiol 46, 2231-2240, doi: 10.1128/JCM.01716-07 (2008).
22. Hsu, C. R., Lin, T. L., Pan, Y. J., Hsieh, P. F. & Wang, J. T. Isolation of a bacteriophage specific for a new capsular type of Klebsiella pneumoniae and characterization of its polysaccharide depolymerase. PloS one 8, e70092, doi: 10.1371/journal.pone.0070092 (2013).
23. Chuang, Y. P., Fang, C. T., Lai, S. Y., Chang, S. C. & Wang, J. T. Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. The Journal of infectious diseases 193, 645-654, doi:JID35150 [pii]10.1086/499968 (2006).
24. Struve, C., Bojer, M., Nielsen, E. M., Hansen, D. S. & Krogfelt, K. A. Investigation of the putative virulence gene magA in a worldwide collection of 495 Klebsiella isolates: magA is restricted to the gene cluster of Klebsiella pneumoniae capsule serotype K1. Journal of medical microbiology 54, 1111-1113, doi: 10.1099/jmm.0.46165-0 (2005).
25. Pan, Y. J. et al. Capsular types of Klebsiella pneumoniae revisited by wzc sequencing. PloS one 8, e80670, doi: 10.1371/journal.pone.0080670 (2013).
26. Wyres, K. L. et al. Identification of Klebsiella capsule synthesis loci from whole genome data. Microbial genomics 2, e000102, doi: 10.1099/mgen.0.000102 (2016).
27. Kubler-Kielb, J. et al. The capsular polysaccharide and lipopolysaccharide structures of two carbapenem resistant Klebsiella pneumoniae outbreak isolates. Carbohydr Res 369, 6-9, doi: 10.1016/j.carres.2012.12.018 (2013).
28. Diago-Navarro, E. et al. Carbapenem-resistant Klebsiella pneumoniae exhibit variability in capsular polysaccharide and capsule associated virulence traits. The Journal of infectious diseases 210, 803-813, doi: 10.1093/infdis/jiu157 (2014).
29. Deleo, F. R. et al. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. Proc Natl Acad Sci USA 111, 4988-4993, doi: 10.1073/pnas.1321364111 (2014).
30. Rieger-Hug, D. & Stirm, S. Comparative study of host capsule depolymerases associated with Klebsiella bacteriophages. Virology 113, 363-378 (1981).
31. van Dam, J. E. et al. A bacteriophage-Associated lyase acting on Klebsiella serotype K5 capsular polysaccharide. Carbohydr Res 142, 338-343 (1985).
32. Sechter, I., Mestre, F. & Hansen, D. S. Twenty-Three years of Klebsiella phage typing: A review of phage typing of 12 clusters of nosocomial infections, and a comparison of phage typing with K serotyping. Clin Microbiol Infect 6, 233-238 (2000).
33. Pieroni, P., Rennie, R. P., Ziola, B. & Deneer, H. G. The use of bacteriophages to differentiate serologically cross-reactive isolates of Klebsiella pneumoniae. Journal of medical microbiology 41, 423-429 (1994).
34. Karamoddini, M. K. et al. Antibacterial efficacy of lytic bacteriophages against antibiotic-resistant Klebsiella species. TheScientificWorldJournal 11, 1332-1340, doi: 10.1100/tsw.2011.114 (2011).
35. Vinodkumar, C. S., Neelagund, Y. F. & Kalsurmath, S. Bacteriophage in the treatment of experimental septicemic mice from a clinical isolate of multidrug resistant Klebsiella pneumoniae. The Journal of communicable diseases 37, 18-29 (2005).
36. Slopek, S., Durlakowa, I., Weber-Dabrowska, B., Dabrowski, M. & Kucharewicz-Krukowska, A. Results of bacteriophage treatment of suppurative bacterial infections. III. Detailed evaluation of the results obtained in further 150 cases. Archivum immunologiae et therapiae experimentalis 32, 317-335 (1984).
37. Mushtaq, N., Redpath, M. B., Luzio, J. P. & Taylor, P. W. Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrobial agents and chemotherapy 48, 1503-1508 (2004).
38. Scorpio, A., Tobery, S. A., Ribot, W. J. & Friedlander, A. M. Treatment of experimental anthrax with recombinant capsule depolymerase. Antimicrobial agents and chemotherapy 52, 1014-1020, doi: 10.1128/AAC.00741-07 (2008).
39. Niemann, H., Frank, N. & Stirm, S. Klebsiella serotype-13 capsular polysaccharide: primary structure and depolymerization by a bacteriophage-borne glycanase. Carbohydr Res 59, 165-177 (1977).
40. Altmann, F., Christian, R., Czerny, T., Nimmich, W. & Marz, L. Bacteriophage-Associated glycan hydrolases specific for Escherichia coli capsular serotype K12. European journal of biochemistry/FEBS 189, 307-312 (1990).
41. Niemann, H., Kwiatkowski, B., Westphal, U. & Stirm, S. Klebsiella serotype 25 capsular polysaccharide: primary structure and depolymerization by a bacteriophage-borne glycanase. Journal of bacteriology 130, 366-374 (1977).
42. Lin, T. L. et al. Isolation of a bacteriophage and its depolymerase specific for K1 capsule of Klebsiella pneumoniae: implication in typing and treatment. The Journal of infectious diseases 210, 1734-1744, doi: 10.1093/infdis/jiu332 (2014).
43. Pan, Y. J. et al. Identification of capsular types in carbapenem-resistant Klebsiella pneumoniae strains by wzc sequencing and implications for capsule depolymerase treatment. Antimicrobial agents and chemotherapy 59, 1038-1047, doi: 10.1128/AAC.03560-14 (2015).
44. Humphries, J. C. Enzymic activity of bacteriophage-culture lysates; a capsule lysin active against Klebsiella pneumoniae type A. Journal of bacteriology 56, 683-693 (1948).
45. Krwawicz, J., Czajkowska, A., Felczak, M. & Pietrzykowska, I. UV-And MMS-induced mutagenesis of lambdaO(am)8 phage under nonpermissive conditions for phage DNA replication. Acta Biochim Pol 50, 921-939 (2003).
46. Hughes, K. A., Sutherland, I. W. & Jones, M. V. Biofilm susceptibility to bacteriophage attack: The role of phage-borne polysaccharide depolymerase. Microbiology 144(Pt 11), 3039-3047, doi: 10.1099/00221287-144-11-3039 (1998).
47. Pan, Y. J. et al. Klebsiella Phage PhiK64-1 Encodes Multiple Depolymerases for Multiple Host Capsular Types. Journal of virology 91, doi: 10.1128/JVI.02457-16 (2017).
48. Scholl, D., Rogers, S., Adhya, S. & Merril, C. R. Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. Journal of virology 75, 2509-2515, doi: 10.1128/JVI.75.6.2509-2515.2001 (2001).
49. Hsieh, P. F., Lin, T. L., Lee, C. Z., Tsai, S. F. & Wang, J. T. Serum-induced iron-Acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. The Journal of infectious diseases 197, 1717-1727, doi: 10.1086/588383 (2008).
50. Hyman, P. & Abedon, S. T. Bacteriophage host range and bacterial resistance. Advances in applied microbiology 70, 217-248, doi: 10.1016/S0065-2164(10)70007-1 (2010).
51. Brisse, S. et al. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PloS one 4, e4982, doi: 10.1371/journal.pone.0004982 (2009).
52. Bialek-Davenet, S. et al. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerging infectious diseases 20, 1812-1820, doi: 10.3201/eid2011.140206 (2014).
53. Holt, K. E. et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA 112, E3574-3581, doi: 10.1073/pnas.1501049112 (2015).
54. Hackland, P. L., Parolis, H. & Parolis, L. A. A structural investigation of the capsular polysaccharide of Klebsiella K69. Carbohydr Res 172, 209-216 (1988).
55. Ravenscroft, N., Parolis, L. A. & Parolis, H. Bacteriophage degradation of Klebsiella K30 capsular polysaccharide. An NMR investigation of the 3,4-pyruvated galactose-containing repeating oligosaccharide. Carbohydr Res 254, 333-340 (1994).
56. Chuang, C., Fan, W. C., Lin, Y. T. & Wang, F. D. The emergence of Klebsiella pneumoniae liver abscess in non-diabetic patients and the distribution of capsular types. Gut pathogens 8, 46, doi: 10.1186/s13099-016-0128-y (2016).
57. Speck, P. & Smithyman, A. Safety and efficacy of phage therapy via the intravenous route. FEMS microbiology letters 363, doi: 10.1093/femsle/fnv242 (2016).
58. Merril, C. R. et al. Long-circulating bacteriophage as antibacterial agents. Proc Natl Acad Sci USA 93, 3188-3192 (1996).
59. Chhibber, S., Kaur, S. & Kumari, S. Therapeutic potential of bacteriophage in treating Klebsiella pneumoniae B5055-mediated lobar pneumonia in mice. Journal of medical microbiology 57, 1508-1513, doi: 10.1099/jmm.0.2008/002873-0 (2008).
60. Kumari, S., Harjai, K. & Chhibber, S. Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumoniae B5055. Journal of medical microbiology 60, 205-210, doi: 10.1099/jmm.0.018580-0 (2011).
61. Verma, V., Harjai, K. & Chhibber, S. Characterization of a T7-like lytic bacteriophage of Klebsiella pneumoniae B5055: A potential therapeutic agent. Current microbiology 59, 274-281, doi: 10.1007/s00284-009-9430-y (2009).
62. Hung, C. H., Kuo, C. F., Wang, C. H., Wu, C. M. & Tsao, N. Experimental phage therapy in treating Klebsiella pneumoniae-mediated liver abscesses and bacteremia in mice. Antimicrobial agents and chemotherapy 55, 1358-1365, doi: 10.1128/AAC.01123-10 (2011).
63. Hsieh, P. F., Lin, T. L., Lee, C. Z., Tsai, S. F. & Wang, J. T. Serum-Induced Iron-Acquisition Systems and TonB Contribute to Virulence in Klebsiella pneumoniae Causing Primary Pyogenic Liver Abscess. The Journal of infectious diseases 197, 1717-1727 (2008).
64. Lin, T. L. et al. Imipenem represses CRISPR-Cas interference of DNA acquisition through H-NS stimulation in Klebsiella pneumoniae. Scientific reports 6, 31644, doi: 10.1038/srep31644 (2016).
65. Hsieh, P. F. et al. Lipopolysaccharide O1 antigen contributes to the virulence in Klebsiella pneumoniae causing pyogenic liver abscess. PloS one 7, e33155, doi: 10.1371/journal.pone.0033155 (2012).
66. Moller, H. J., Heinegard, D. & Poulsen, J. H. Combined alcian blue and silver staining of subnanogram quantities of proteoglycans and glycosaminoglycans in sodium dodecyl sulfate-polyacrylamide gels. Analytical biochemistry 209, 169-175, doi: 10.1006/abio.1993.1098 (1993).
67. Zamze, S. et al. Recognition of bacterial capsular polysaccharides and lipopolysaccharides by the macrophage mannose receptor. The Journal of biological chemistry 277, 41613-41623, doi: 10.1074/jbc.M207057200 (2002).
68. Maneval, W. E. Staining bacteria and yeasts with acid dyes. Stain Technology 16, 13-19 (1941).