A novel bacteriophage targeting Cronobacter sakazakii is a potential biocontrol agent in foods

Applied and Environmental Microbiology

Volumn 82, Issue 1, 2016, Pages 192-201

  Lee, Ju Hoon ^b   Bai, Jaewoo ^a   Shin, Hakdong ^a   Kim, Yeran ^a   Park, Bookyung ^a   Heu, Sunggi ^c   Ryu, Sangryeol ^a,d  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

^c National Institute of Animal Science   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; GENES; MASS SPECTROMETRY; POLYACRYLATES; TRANSCRIPTION;

ANTIBIOTIC RESISTANCE; BACTERIAL FLAGELLUM; CLINICAL ISOLATES; MATRIX-ASSISTED LASER DESORPTION-IONIZATION TIME-OF-FLIGHT MASS; MULTIPLICITY OF INFECTIONS; OPEN READING FRAME; PROTEOMIC ANALYSIS; STRUCTURAL PROTEINS;

BIOCONTROL;

BACTERIOPHAGE; BIOCONTROL AGENT; FOOD; GENOME; PATHOGEN; PROTEOMICS;

BACTERIA (MICROORGANISMS);

BIOLOGICAL CONTROL AGENT; VIRUS DNA;

ARTIFICIAL MILK; BACTERIOLYSIS; BIOLOGICAL CONTROL AGENT; CRONOBACTER SAKAZAKII; DNA BASE COMPOSITION; DNA SEQUENCE; FOOD CONTROL; GENETICS; HUMAN; INFANT; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MYOVIRIDAE; OPEN READING FRAME; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEOMICS; ULTRASTRUCTURE; VIROLOGY; VIRUS GENOME;

BACTERIOLYSIS; BASE COMPOSITION; BIOLOGICAL CONTROL AGENTS; CRONOBACTER SAKAZAKII; DNA, VIRAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FOOD MICROBIOLOGY; GENOME, VIRAL; HUMANS; INFANT; INFANT FORMULA; MOLECULAR SEQUENCE DATA; MYOVIRIDAE; OPEN READING FRAMES; PROTEOMICS; SEQUENCE ANALYSIS, DNA;

EID: 84953869674     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01827-15     Document Type: Article

References (45)

1. Farmer JJ, III, Asbury MA, Hickman FW, Brenner DJ, the Enterobacteriaceae Study Group. 1980. Enterobacter sakazakii: a new species of "Enterobacteriaceae" isolated from clinical specimens. Int J Syst Bacteriol 30:569-584. http://dx.doi.org/10.1099/00207713-30-3-569.
2. Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, Fanning S, Stephan R, Joosten H. 2007. The taxonomy of Enterobacter sakazakii: proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov. Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies 1. BMC Evol Biol 7:64. http://dx.doi.org/10.1186/1471-2148-7-64.
3. Drudy D, Mullane NR, Quinn T, Wall PG, Fanning S. 2006. Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin Infect Dis 42:996-1002. http://dx.doi.org/10.1086/501019.
4. Nazarowec-White M, Farber JM. 1997. Enterobacter sakazakii: a review. Int J Food Microbiol 34:103-113. http://dx.doi.org/10.1016/S0168-1605(96)01172-5.
5. Tsai H, Liao C, Huang Y, Lee P, Ren HP. 2013. Cronobacter infections not from infant formula, Taiwan. Emerg Infect Dis 19:167-169. http://dx.doi.org/10.3201/eid1901.120774.
6. Lai KK. 2001. Enterobacter sakazakii infections among neonates, infants, children, and adults: case reports and a review of the literature. Medicine (Baltimore) 80:113-122. http://dx.doi.org/10.1097/00005792-200103000-00004.
7. Calendar R. 2006. The bacteriophages, 2nd ed. Oxford University Press, New York, NY.
8. Sulakvelidze A, Alavidze Z, Morris JG, Jr. 2001. Bacteriophage therapy. Antimicrob Agents Chemother 45:649-659. http://dx.doi.org/10.1128/AAC.45.3.649-659.2001.
9. Lee Y-D, Chang H-I, Park J-H. 2011. Complete genomic sequence of virulent Cronobacter sakazakii phage ESSI-2 isolated from swine feces. Arch Virol 156:721-724. http://dx.doi.org/10.1007/s00705-011-0934-y.
10. Lee Y-D, Park J-H, Chang H-I. 2011. Genomic sequence analysis of virulent Cronobacter sakazakii bacteriophage ES2. Arch Virol 156:2105-2108. http://dx.doi.org/10.1007/s00705-011-1096-7.
11. Lee Y-D, Kim J-Y, Park J-H, Chang H. 2012. Genomic analysis of bacteriophage ESP2949-1, which is virulent for Cronobacter sakazakii. Arch Virol 157:199-202. http://dx.doi.org/10.1007/s00705-011-1147-0.
12. Lee Y-D, Park J-H. 2012. Complete genome of temperate phage ENT39118 from Cronobacter sakazakii. J Virol 86:5400-5401. http://dx.doi.org/10.1128/JVI.00345-12.
13. Shin H, Lee J-H, Kim Y, Ryu S. 2012. Complete genome sequence of Cronobacter sakazakii bacteriophage CR3. J Virol 86:6367-6368. http://dx.doi.org/10.1128/JVI.00636-12.
14. Lee J-H, Choi Y, Shin H, Lee J, Ryu S. 2012. Complete genome sequence of Cronobacter sakazakii temperate bacteriophage phiES15. J Virol 86: 7713-7714. http://dx.doi.org/10.1128/JVI.01042-12.
15. Abbasifar R, Kropinski AM, Sabour PM, Ackermann H-W, Lingohr EJ, Griffiths MW. 2012. Complete genome sequence of Cronobacter sakazakii bacteriophage vB_CsaM_GAP161. J Virol 86:13806-13807. http://dx.doi.org/10.1128/JVI.02546-12.
16. Abbasifar R, Kropinski AM, Sabour PM, Ackermann H-W, Alanis Villa A, Abbasifar A, Griffiths MW. 2012. Genome sequence of Cronobacter sakazakii myovirus vB_CsaM_GAP31. J Virol 86:13830-13831. http://dx.doi.org/10.1128/JVI.02629-12.
17. Abbasifar R, Kropinski AM, Sabour PM, Ackermann H-W, Alanis Villa A, Abbasifar A, Griffiths MW. 2013. The genome of Cronobacter sakazakii bacteriophage vB_CsaP_GAP227 suggests a new genus within the Autographivirinae. Genome Announc 1(1):e00122-12. http://dx.doi.org/10.1128/genomeA.00122-12.
18. Endersen L, Guinane CM, Johnston C, Neve H, Coffey A, Ross RP, McAuliffe O, O'Mahony J. 2015. Genome analysis of Cronobacter phage vB_CsaP_Ss1 reveals an endolysin with potential for biocontrol of Gramnegative bacterial pathogens. J Gen Virol 96:463-477. http://dx.doi.org/10.1099/vir.0.068494-0.
19. Abbasifar R, Griffiths MW, Sabour PM, Ackermann HW, Vandersteegen K, Lavigne R, Noben JP, Alanis Villa A, Abbasifar A, Nash JH, Kropinski AM. 2014. Supersize me: Cronobacter sakazakii phage GAP32. Virology 460-461:138-146. http://dx.doi.org/10.1016/j.virol.2014.05.003.
20. Kim KP, Klumpp J, Loessner MJ. 2007. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int J Food Microbiol 115:195-203. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.029.
21. Zuber S, Boissin-Delaporte C, Michot L, Iversen C, Diep B, Brussow H, Breeuwer P. 2008. Decreasing Enterobacter sakazakii (Cronobacter spp.) food contamination level with bacteriophages: prospects and problems. Microbiol Biotechnol 1:532-543. http://dx.doi.org/10.1111/j.1751-7915.2008.00058.x.
22. Tóthová L, Celec P, Bábíčková J, Gajdošová J, Al-Alami H, Kamodyova N, Drahovská H, Liptáková A, Turňa J, Hodosy J. 2011. Phage therapy of Cronobacter-induced urinary tract infection in mice. Med Sci Monit 17:BR173-BR178.
23. Kim M, Ryu S. 2011. Characterization of a T5-like coliphage SPC35 and differential development of resistance to SPC35 in Salmonella Typhimurium and Escherichia coli. Appl Environ Microbiol 77:2042-2050. http://dx.doi.org/10.1128/AEM.02504-10.
24. Fauquet C, Mayo MA, Maniloff J, Desselberger U, Ball LA (ed). 2005. Virus taxonomy: eighth report of the International Committee on the Taxonomy of Viruses, 1st ed. Elsevier Academic Press, San Diego, CA.
25. Kim K, Kim K-P, Choi J, Lim J-A, Lee J, Hwang S, Ryu S. 2010. Outer membrane proteinsA(OmpA) andX(OmpX) are essential for basolateral invasion of Cronobacter sakazakii. Appl Environ Microbiol 76:5188-5198. http://dx.doi.org/10.1128/AEM.02498-09.
26. 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. http://dx.doi.org/10.1073/pnas.120163297.
27. Wilcox SA, Toder R, Foster JW. 1996. Rapid isolation of recombinant lambda phageDNAfor use in fluorescence in situ hybridization. Chromosome Res 4:397-398. http://dx.doi.org/10.1007/BF02257276.
28. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673-679. http://dx.doi.org/10.1093/bioinformatics/btm009.
30. Besemer J, Lomsadze A, Borodovsky M. 2001. GeneMarkS: a selftraining method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607-2618.
31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic Local Alignment Search Tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
32. Zdobnov EM, Apweiler R. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848. http://dx.doi.org/10.1093/bioinformatics/17.9.847.
33. Carver T, Berriman M, Tivey A, Patel C, Böhme U, Barrell BG, Parkhill J, Rajandream M-A. 2008. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24: 2672-2676. http://dx.doi.org/10.1093/bioinformatics/btn529.
34. Hartmann I, Carranza P, Lehner A, Stephan R, Eberl L, Riedel K. 2010. Genes involved in Cronobacter sakazakii biofilm formation. Appl Environ Microbiol 76:2251-2261. http://dx.doi.org/10.1128/AEM.00930-09.
35. Evans TJ, Trauner A, Komitopoulou E, Salmond GP. 2010. Exploitation of a new flagellatropic phage of Erwinia for positive selection of bacterial mutants attenuated in plant virulence: towards phage therapy. J Appl Microbiol 108:676-685. http://dx.doi.org/10.1111/j.1365-2672.2009.04462.x.
36. Lee JH, Shin H, Kim H, Ryu S. 2011. Complete genome sequence of Salmonella bacteriophage SPN3US. J Virol 85:13470-13471. http://dx.doi.org/10.1128/JVI.06344-11.
37. Dömötör D, Becságh P, Rákhely G, Schneider G, Kovács T. 2012. Complete genomic sequence of Erwinia amylovora phage PhiEaH2. J Virol 86:10899. http://dx.doi.org/10.1128/JVI.01870-12.
38. Conway JF, Duda RL, Cheng N, Hendrix RW, Steven AC. 1995. Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system. J Mol Biol 253:86-99. http://dx.doi.org/10.1006/jmbi.1995.0538.
39. Hagens S, Loessner MJ. 2007. Application of bacteriophages for detection and control of foodborne pathogens. Appl Microbiol Biotechnol 76:513-519. http://dx.doi.org/10.1007/s00253-007-1031-8.
40. Thomas JA, Rolando MR, Carroll CA, Shen PS, Belnap DM, Weintraub ST, Serwer P, Hardies SC. 2008. Characterization of Pseudomonas chlororaphis myovirus 201varphi2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 376:330-338. http://dx.doi.org/10.1016/j.virol.2008.04.004.
41. Mesyanzhinov VV, Robben J, Grymonprez B, Kostyuchenko VA, Bourkaltseva MV, Sykilinda NN, Krylov VN, Volckaert G. 2002. The genome of bacteriophage phiKZ of Pseudomonas aeruginosa. J Mol Biol 317:1-19. http://dx.doi.org/10.1006/jmbi.2001.5396.
42. Monson R, Foulds I, Foweraker J, Welch M, Salmond GP. 2011. The Pseudomonas aeruginosa generalized transducing phage phiPA3 is a new member of the phiKZ-like group of 'jumbo' phages, and infects model laboratory strains and clinical isolates from cystic fibrosis patients. Microbiology 157:859-867. http://dx.doi.org/10.1099/mic.0.044701-0.
43. Zaychikov E, Martin E, Denissova L, Kozlov M, Markovtsov V, Kashlev M, Heumann H, Nikiforov V, Goldfarb A, Mustaev A. 1996. Mapping of catalytic residues in the RNA polymerase active center. Science 273: 107-109. http://dx.doi.org/10.1126/science.273.5271.107.
44. Kucerova E, Clifton SW, Xia XQ, Long F, Porwollik S, Fulton L, Fronick C, Minx P, Kyung K, Warren W, Fulton R, Feng D, Wollam A, Shah N, Bhonagiri V, Nash WE, Hallsworth-Pepin K, Wilson RK, McClelland M, Forsythe SJ. 2010. Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS One 5:e9556. http://dx.doi.org/10.1371/journal.pone.0009556.
45. Kim K, Jang SS, Kim SK, Park JH, Heu S, Ryu S. 2008. Prevalence and genetic diversity of Enterobacter sakazakii in ingredients of infant foods. Int J Food Microbiol 122:196-203. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.11.072.