Expression and delivery of an endolysin to combat Clostridium perfringens

Applied Microbiology and Biotechnology

Volumn 98, Issue 6, 2014, Pages 2495-2505

  Gervasi, Teresa ^a,b   Horn, Nikki ^a   Wegmann, Udo ^a   Dugo, Giacomo ^b   Narbad, Arjan ^a   Mayer, Melinda J ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b UNIVERSITY OF MESSINA   (Italy)

Author keywords

Clostridium perfringens; Delivery; Endolysin; Lactobacillus johnsonii; Probiotic

Indexed keywords

CLOSTRIDIUM PERFRINGENS; DELIVERY; ENDOLYSIN; LACTOBACILLUS JOHNSONII; PROBIOTICS;

AMINO ACIDS; BIOCHEMISTRY; CLONING; ESCHERICHIA COLI; GENES; STRAIN; TELEMETERING;

CLOSTRIDIUM;

BACTERIAL PROTEIN; CP251 PROTEIN; ENDOLYSIN; N ACETYLMURAMOYLALANINE AMIDASE; NISIN; NISIN A; NISRK PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROBIOTIC AGENT; REGULATOR PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

BACTERIOPHAGE; BACTERIUM; BIOENGINEERING; DIGESTIVE SYSTEM; DISEASE CONTROL; DISEASE TREATMENT; ENZYME ACTIVITY; GENE EXPRESSION; PATHOGEN; PROBIOTICS; SECRETION;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL STRAIN; BACTERIOPHAGE; CLOSTRIDIUM PERFRINGENS; CONTROL STRATEGY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLYSIS; DRUG DELIVERY SYSTEM; DRUG SYNTHESIS; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENE PRODUCT; IN VITRO STUDY; LACTOBACILLUS JOHNSONII; LACTOCOCCUS LACTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PROMOTER REGION;

ANIMALIA; CLOSTRIDIUM PERFRINGENS; ESCHERICHIA COLI; LACTOBACILLUS JOHNSONII; LACTOCOCCUS LACTIS;

BACTERIOLYSIS; BACTERIOPHAGES; CLONING, MOLECULAR; CLOSTRIDIUM PERFRINGENS; ENDOPEPTIDASES; ESCHERICHIA COLI; GENE EXPRESSION; LACTOBACILLUS; LACTOCOCCUS LACTIS; VIRAL PROTEINS;

EID: 84896728759     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5128-y     Document Type: Article

References (58)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402 (Pubitemid 27359211)
2. Atterbury RJ, Van Bergen MA, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA (2007) Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol 73:4543-4549 (Pubitemid 47122599)
3. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L (2006) A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 4:754-759 (Pubitemid 43841860)
4. Catalao MJ, Gil F, Moniz-Pereira J, Sao-Jose C, Pimentel M (2012) Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev. doi:10.1111/1574-6976.12006
5. de Ruyter PG, Kuipers OP, de Vos WM (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62:3662-3667 (Pubitemid 26329592)
6. Dodd HM, Horn N, Hao Z, Gasson MJ (1992) A lactococcal expression system for engineered nisins. Appl Environ Microbiol 58:3683-3693
7. El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I (2009) Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Prot 72:733-740
8. Fenton M, Casey PG, Hill C, Gahan CG, Ross RP, McAuliffe O, O'Mahony J, Maher F, Coffey A (2010) The truncated phage lysin CHAP(k) eliminates Staphylococcus aureus in the nares of mice. Bioeng Bugs 1:404-407
9. Fernandez A, Horn N, Wegmann U, Nicoletti C, Gasson MJ, Narbad A (2009) Enhanced secretion of biologically activemurine interleukin-12 by Lactococcus lactis. Appl Environ Microbiol 75:869-871
10. Fischetti VA (2010) Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int J Med Microbiol 300:357-362
11. Garcia P, Martinez B, Rodriguez L, Rodriguez A (2010) Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. Int J Food Microbiol 141:151-155
12. Gervasi T, Lo Curto R, Narbad A, Mayer MJ (2013) Complete genome sequence of PhiCP51, a temperate bacteriophage of Clostridium perfringens. Arch Virol. doi:10.1007/s00705-013-1647-1
13. Gil de los Santos JR, Storch OB, Fernandes CG, Gil-Turnes C (2012) Evaluation in broilers of the probiotic properties of Pichia pastoris and a recombinant P. pastoris containing the Clostridium perfringens alpha toxin gene. Vet Microbiol 156:448-451
14. Grandgirard D, Loeffler JM, Fischetti VA, Leib SL (2008) Phage lytic enzyme Cpl-1 for antibacterial therapy in experimental pneumococcal meningitis. J Infect Dis 197:1519-1522 (Pubitemid 351706481)
15. Grant KA, Kenyon S, Nwafor I, Plowman J, Ohai C, Halford-Maw R, Peck MW, McLauchlin J (2008) The identification and characterization of Clostridium perfringens by real-time PCR, location of enterotoxin gene, and heat resistance. Foodborne Pathog Dis 5:629-639
16. Gupta R, Prasad Y (2011) P-27/HP endolysin as antibacterial agent for antibiotic resistant Staphylococcus aureus of human infections. Curr Microbiol 63:39-45
17. Hoopes JT, Stark CJ, Kim HA, Sussman DJ, Donovan DM, Nelson DC (2009) Use of a bacteriophage lysin, PlyC, as an enzyme disinfectant against Streptococcus equi. Appl Environ Microbiol 75:1388-1394
18. Horn N, Wegmann U, Narbad A, Gasson MJ (2005) Characterisation of a novel plasmid p9785S from Lactobacillus johnsonii FI9785. Plasmid 54:176-183 (Pubitemid 41191204)
19. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68 (Pubitemid 19125654)
20. Keyburn AL, Boyce JD, Vaz P, Bannam TL, Ford ME, Parker D, Di Rubbo A, Rood JI, Moore RJ (2008) NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog 4:e26
21. Kizerwetter-Swida M, Binek M (2009) Protective effect of potentially probiotic Lactobacillus strain on infection with pathogenic bacteria in chickens. Pol J Vet Sci 12:15-20
22. Kleerebezem M, Beerthuyzen MM, Vaughan EE, de Vos WM, Kuipers OP (1997) Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl Environ Microbiol 63:4581-4584 (Pubitemid 27485794)
23. Kretzer JW, Lehmann R, Schmelcher M, Banz M, Kim KP, Korn C, Loessner MJ (2007) Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol 73:1992-2000 (Pubitemid 46449084)
24. Kuipers OP, Beerthuyzen MM, de Ruyter PG, Luesink EJ, de Vos WM (1995) Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J Biol Chem 270:27299-27304
25. La Ragione RM, Narbad A, Gasson MJ, Woodward MJ (2004) In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Lett Appl Microbiol 38:197-205 (Pubitemid 38297054)
26. Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728-764
27. Lee KW, Lillehoj HS, Jeong W, Jeoung HY, An DJ (2011) Avian necrotic enteritis: experimental models, host immunity, pathogenesis, risk factors, and vaccine development. Poult Sci 90:1381-1390
28. Lindstrom M, Heikinheimo A, Lahti P, Korkeala H (2011) Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol 28:192-198
29. Liu D, Guo Y, Wang Z, Yuan J (2010) Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathol 39:17-24
30. Lu TK, Koeris MS (2011) The next generation of bacteriophage therapy. Curr Opin Microbiol 14:524-531
31. Maguin E, Prevost H, Ehrlich SD, Gruss A (1996) Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol 178:931-935 (Pubitemid 26036674)
32. Mandalari G, Nueno Palop C, Tuohy K, Gibson GR, Bennett RN, Waldron KW, Bisignano G, Narbad A, Faulds CB (2007) In vitro evaluation of the prebiotic activity of a pectic oligosaccharide-rich extract enzymatically derived from bergamot peel. Appl Microbiol Biotechnol 73:1173-1179 (Pubitemid 44974328)
33. Mayer MJ, Narbad A, Gasson MJ (2008) Molecular characterization of a Clostridium difficile bacteriophage and its cloned biologically active endolysin. J Bacteriol 190:6734-6740
34. Mayer MJ, Payne J, Gasson MJ, Narbad A (2010) Genomic sequence and characterization of the virulent bacteriophage Φ CTP1 from Clostridium tyrobutyricum and heterologous expression of its endolysin. Appl Environ Microbiol 76:5415-5422
35. Mayer MJ, Gasson MJ, Narbad A (2012) Genomic sequence of bacteriophage ATCC 8074-B1 and activity of its endolysin and engineered variants against Clostridium sporogenes. Appl Environ Microbiol 78:3685-3692
36. Meng X, Shi Y, Ji W, Zhang J, Wang H, Lu C, Sun J, Yan Y (2011) Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl Environ Microbiol 77:8272-8279
37. Miller RW, Skinner EJ, Sulakvelidze A, Mathis GF, Hofacre CL (2010) Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Dis 54:33-40
38. Miyamoto K, Li J, McClane BA (2012) Enterotoxigenic Clostridium perfringens: detection and identification. Microbes Environ 27:343-349
39. Morales CA, Oakley BB, Garrish JK, Siragusa GR, Ard MB, Seal BS (2012) Complete genome sequence of the podoviral bacteriophage PhiCP24R, which is virulent for Clostridium perfringens. Arch Virol 157:769-772
40. Nariya H, Miyata S, Tamai E, Sekiya H, Maki J, Okabe A (2011) Identification and characterization of a putative endolysin encoded by episomal phage phiSM101 of Clostridium perfringens. Appl Microbiol Biotechnol 90:1973-1979
41. Nicholas KB, H.B. N, Deerfield DW (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4:14.
42. O'Flaherty S, Ross RP, Coffey A (2009) Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol Rev 33:801-819
43. Oakley BB, Talundzic E, Morales CA, Hiett KL, Siragusa GR, Volozhantsev NV, Seal BS (2011) Comparative genomics of four closely related Clostridium perfringens bacteriophages reveals variable evolution among core genes with therapeutic potential. BMC Genomics 12:282
44. Petit L, Gibert M, Popoff MR (1999) Clostridium perfringens: toxinotype and genotype. Trends Microbiol 7:104-110 (Pubitemid 29271996)
45. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States - major pathogens. Emerg Infect Dis 17:7-15
46. Schmelcher M, Donovan DM, Loessner MJ (2012) Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7:1147-1171
47. Schmitz JE, Ossiprandi MC, Rumah KR, Fischetti VA (2011) Lytic enzyme discovery through multigenomic sequence analysis in Clostridium perfringens. Appl Microbiol Biotechnol 89:1783-1795
48. Simmons M, Donovan DM, Siragusa GR, Seal BS (2010) Recombinant expression of two bacteriophage proteins that lyse Clostridium perfringens and share identical sequences in the C-terminal cell wall binding domain of the molecules but are dissimilar in their Nterminal active domains. J Agric Food Chem 58:10330-10337
49. Stentz R, Bongaerts RJ, Gunning AP, Gasson M, Shearman C (2010) Controlled release of protein from viable Lactococcus lactis cells. Appl Environ Microbiol 76:3026-3031
50. Timbermont L, Lanckriet A, Dewulf J, Nollet N, Schwarzer K, Haesebrouck F, Ducatelle R, Van Immerseel F (2010) Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils. Avian Pathol 39:117-121
51. Turner MS, Waldherr F, Loessner MJ, Giffard PM (2007) Antimicrobial activity of lysostaphin and a Listeria monocytogenes bacteriophage endolysin produced and secreted by lactic acid bacteria. Syst Appl Microbiol 30:58-67 (Pubitemid 44969474)
52. Van Immerseel F, Rood JI, Moore RJ, Titball RW (2009) Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol 17:32-36
53. Volozhantsev NV, Oakley BB, Morales CA, Verevkin VV, Bannov VA, Krasilnikova VM, Popova AV, Zhilenkov EL, Garrish JK, Schegg KM, Woolsey R, Quilici DR, Line JE, Hiett KL, Siragusa GR, Svetoch EA, Seal BS (2012) Molecular characterization of podoviral bacteriophages virulent for Clostridium perfringens and their comparison with members of the Picovirinae. PLoS One 7:e38283
54. Volozhantsev NV, Verevkin VV, Bannov VA, Krasilnikova VM, Myakinina VP, Zhilenkov EL, Svetoch EA, Stern NJ, Oakley BB, Seal BS (2011) The genome sequence and proteome of bacteriophage PhiCPV1 virulent for Clostridium perfringens. Virus Res 155:433-439
55. Wegmann U, Klein JR, Drumm I, Kuipers OP, Henrich B (1999) Introduction of peptidase genes from Lactobacillus delbrueckii subsp. lactis into Lactococcus lactis and controlled expression. Appl Environ Microbiol 65:4729-4733
56. Yoong P, Schuch R, Nelson D, Fischetti VA (2006) PlyPH, a bacteriolytic enzyme with a broad pH range of activity and lytic action against Bacillus anthracis. J Bacteriol 188:2711-2714
57. Zhang G, Mathis GF, Hofacre CL, Yaghmaee P, Holley RA, Duranc TD (2010) Effect of a radiant energy-treated lysozyme antimicrobial blend on the control of clostridial necrotic enteritis in broiler chickens. Avian Dis 54:1298-1300
58. Zimmer M, Vukov N, Scherer S, Loessner MJ (2002) The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol 68:5311-5317 (Pubitemid 35265662)