A thermophilic phage endolysin fusion to a Clostridium perfringens-specific cell wall binding domain creates an anti-clostridium antimicrobial with improved thermostability

Viruses

Volumn 7, Issue 6, 2015, Pages 3019-3034

  Swift, Steven M ^a   Seal, Bruce S ^b,d   Garrish, Johnna K ^b   Oakley, Brian B ^b,e   Hiett, Kelli ^b   Yeh, Hung Yueh ^b   Woolsey, Rebekah ^c   Schegg, Kathleen M ^c   Line, John Eric ^b   Donovan, David M ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b RUSSELL RESEARCH CENTER   (United States)

^c UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^d OREGON STATE UNIVERSITY   (United States)

^e WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

Alternative antimicrobial; Bacteriophage; Endolysin; Feed additive; Food safety; Peptidoglycan hydrolase; Thermostabile; Thermostable

Indexed keywords

ANTIINFECTIVE AGENT; ENDOLYSIN; FOOD ADDITIVE; HYBRID PROTEIN; HYDROLASE; N ACETYLMURAMOYLALANINE AMIDASE; PEPTIDOGLYCAN; SODIUM CHLORIDE; SYNTHETIC DNA; UNCLASSIFIED DRUG; VIRUS ENZYME; ENZYME ACTIVATOR; PROTEIN BINDING; PROTEINASE;

AFFINITY CHROMATOGRAPHY; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIOLYSIS; BACTERIOPHAGE; CLONING VECTOR; CLOSTRIDIUM PERFRINGENS INFECTION; CODON; CONTROLLED STUDY; ENZYME PURIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; FOOD SAFETY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; POULTRY; PROTEIN EXPRESSION; ANIMAL; CELL WALL; CHEMISTRY; CHICKEN; CLOSTRIDIUM PERFRINGENS; DRUG EFFECTS; ENZYMOLOGY; FOOD INDUSTRY; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; PROCEDURES; PROTEIN STABILITY; TEMPERATURE;

ANIMALIA; BACTERIA (MICROORGANISMS); CLOSTRIDIUM; CLOSTRIDIUM PERFRINGENS; GALLUS GALLUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOLYSIS; BACTERIOPHAGES; CELL WALL; CHICKENS; CLOSTRIDIUM PERFRINGENS; ENDOPEPTIDASES; ENZYME ACTIVATORS; ENZYME STABILITY; ESCHERICHIA COLI; FOOD INDUSTRY; FOOD SAFETY; GENE EXPRESSION; HUMANS; HYDROGEN-ION CONCENTRATION; PROTEIN BINDING; PROTEIN STABILITY; RECOMBINANT FUSION PROTEINS; SODIUM CHLORIDE; TEMPERATURE;

EID: 84934978204     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7062758     Document Type: Article

References (56)

1. Smedley, J.G., 3rd; Fisher, D.J.; Sayeed, S.; Chakrabarti, G.; McClane, B.A. The enteric toxins of Clostridium perfringens. Rev. Physiol. Biochem. Pharmacol. 2004, 152, 183–204.
2. Sawires, Y.S.; Songer, J.G. Clostridium perfringens: Insight into virulence evolution and population structure. Anaerobe 2006, 12, 23–43.
3. Scallan, E.; Griffin, P.M.; Angulo, F.J.; Tauxe, R.V.; Hoekstra, R.M. Foodborne illness acquired in the United States—Unspecified agents. Emerg. Infect. Dis. 2011, 17, 16–22.
4. Huyghebaert, G.; Ducatelle, R.; van Immerseel, F. An update on alternatives to antimicrobial growth promoters for broilers. Vet. J. 2011, 187, 182–188.
5. Millet, S.; Maertens, L. The European ban on antibiotic growth promoters in animal feed: From challenges to opportunities. Vet. J. 2011, 187, 143–144.
6. Wise, M.G.; Siragusa, G.R. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J. Appl. Microbiol. 2007, 102, 1138–1149.
7. Oakley, B.B.; Morales, C.A.; Line, J.; Berrang, M.E.; Meinersmann, R.J.; Tillman, G.E.; Wise, M.G.; Siragusa, G.R.; Hiett, K.L.; Seal, B.S. The poultry-associated microbiome: Network analysis and farm-to-fork characterizations. PLoS ONE 2013, 8, e57190.
8. Seal, B.S.; Lillehoj, H.S.; Donovan, D.M.; Gay, C.G. Alternatives to antibiotics: A symposium on the challenges and solutions for animal production. Anim. Health Res. Rev. 2013, 14, 78–87.
9. Sulakvelidze, A. Phage therapy: An attractive option for dealing with antibiotic-resistant bacterial infections. Drug Discov. Today 2005, 10, 807–809.
10. Liu, J.; Dehbi, M.; Moeck, G.; Arhin, F.; Bauda, P.; Bergeron, D.; Callejo, M.; Ferretti, V.; Ha, N.; Kwan, T.; et al. Antimicrobial drug discovery through bacteriophage genomics. Nat. Biotechnol. 2004, 22, 185–191.
11. Pastagia, M.; Schuch, R.; Fischetti, V.A.; Huang, D.B. Lysins: The arrival of pathogen-directed anti-infectives. J. Med. Microbiol. 2013, 62, 1506–1516.
12. Schmelcher, M.; Donovan, D.M.; Loessner, M.J. Bacteriophage endolysins as novel antimicrobials. Future Microbiol. 2012, 7, 1–25.
13. Rodríguez-Rubio, L.; Martínez, B.; Donovan, D.M.; Rodríguez, A.; García, P. Bacteriophage virion-associated peptidoglycan hydrolases: Potential new enzybiotics. Crit. Rev. Microbiol. 2013, 39, 427–434.
14. Seal, B.S. Characterization of bacteriophages virulent for Clostridium perfringens and identification of phage lytic enzymes as alternatives to antibiotics for potential control of the bacterium. Poult. Sci. 2013, 92, 526–533.
15. Bren, L. Bacteria-eating virus approved as food additive. FDA Consum. 2007, 41, 20–22.
16. Lu, T.K.; Koeris, M.S. The next generation of bacteriophage therapy. Curr. Opin. Microbiol. 2011, 14, 524–531.
17. Maura, D.; Debarbieux, L. Bacteriophages as twenty-first century antibacterial tools for food and medicine. Appl. Microbiol. Biotechnol. 2011, 90, 851–859.
18. Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317–327.
19. Simmons, M.; Donovan, D.M.; Siragusa, G.R.; Seal, B.S. 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 N-terminal active domains. J. Agric. Food Chem. 2010, 58, 10330–10337.
20. Ye, T.; Zhang, X. Characterization of a lysin from deep-sea thermophilic bacteriophage GVE2. Appl. Microbiol. Biotechnol. 2008, 78, 635–641.
21. Jin, M.; Ye, T.; Zhang, X. Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures. Microbiology 2013, 159, 1597–1605.
22. Schäffer, A.A.; Aravind, L.; Madden, T.L.; Shavirin, S.; Spouge, J.L.; Wolf, Y.I.; Koonin, E.V.; Altschul, S.F. Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res. 2001, 29, 2994–3005.
23. Studier, F.W.; Moffatt, B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 1986, 189, 113–130.
24. Siragusa, G.R.; Danyluk, M.D.; Hiett, K.L.; Wise, M.G.; Craven, S.E. Molecular subtyping of poultry-associated type A Clostridium perfringens isolates by repetitive-element PCR. J. Clin. Microbiol. 2006, 44, 1065–1073.
25. Crowe, J.; Döbeli, H.; Gentz, R.; Hochuli, E.; Stüber, D.; Henco, K. 6xHis-Ni-NTA chromatography as a superior technique in recombinant protein expression/purification. Methods Mol. Biol. 1994, 31, 371–387.
26. Hames, B.D. One-dimensional polyacrylamide gel electrophoresis. In Gel Electrophoresis of Proteins: A Practical Approach, 2nd ed.; Hames, B.D., Rickwood, D., Eds.; Oxford University Press: New York, NY, USA, 1990; pp. 1–147.
27. Keller, A.; Nesvizhskii, A.I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383–5392.
28. Nesvizhskii, A.I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75, 4646–4658.
29. Kall, L.; Storey, J.D.; MacCoss, M.J.; Noble, W.S. Assigning significance to peptides identified by tandem mass spectrometry using decoy databases. J. Proteome Res. 2008, 7, 29–34.
30. Hobbs, B.C.; Smith, M.E.; Oakley, C.L.; Warrack, G.H.; Cruickshank, J.C. Clostridium welchii food poisoning. J. Hyg. 1953, 51, 75–101.
31. Rotilie, C.A.; Fass, R.J.; Prior, R.B.; Perkins, R.L. Microdilution technique for antimicrobial susceptibility testing of anaerobic bacteria. Antimicrob. Agents Chemother. 1975, 7, 311–315.
32. Andrews, J.M. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 2001, 48 (Suppl. 1), 5–16.
33. Donovan, D.M.; Dong, S.; Garrett, W.; Rousseau, G.M.; Moineau, S.; Pritchard, D.G. Peptidoglycan hydrolase fusions maintain their parental specificities. Appl. Environ. Microbiol. 2006, 72, 2988–2996.
34. Linden, S.B.; Zhang, H.; Heselpoth, R.D.; Shen, Y.; Schmelcher, M.; Eichenseher, F.; Nelson, D.C. Biochemical and biophysical characterization of PlyGRCS, a bacteriophage endolysin active against methicillin-resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 2015, 99, 741–752.
35. Becker, S.C.; Dong, S.; Baker, J.R.; Foster-Frey, J.; Pritchard, D.G.; Donovan, D.M. LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells. FEMS Microbiol. Lett. 2009, 294, 52–60.
36. Hermoso, J.A.; García, J.L.; García, P. Taking aim on bacterial pathogens: From phage therapy to enzybiotics. Curr. Opin. Microbiol. 2007, 10, 461–472.
37. Low, L.Y.; Yang, C.; Perego, M.; Osterman, A.; Liddington, R.C. Structure and lytic activity of a Bacillus anthracis prophage endolysin. J. Biol. Chem. 2005, 280, 35433–35439.
38. Bousquet-Antonelli, C.; Deragon, J.M. A comprehensive analysis of the La-motif protein superfamily. RNA 2009, 15, 750–764.
39. Tillman, G.E.; Simmons, M.; Garrish, J.K.; Seal, B.S. Expression of a Clostridium perfringens genome-encoded putative N-acetylmuramoyl-L-alanine amidase as a potential antimicrobial to control the bacterium. Arch. Microbiol. 2013, 195, 675–681.
40. Zhang, G.; Darius, S.; Smith, S.R.; Ritchie, S.J. In vitro inhibitory effect of hen egg white lysozyme on Clostridium perfringens type A associated with broiler necrotic enteritis and its alpha-toxin production. Lett. Appl. Microbiol. 2006, 42, 138–143.
41. Schmelcher, M.; Powell, A.M.; Becker, S.C.; Camp, M.J.; Donovan, D.M. Chimeric phage lysins act synergistically with lysostaphin to kill mastitis-causing Staphylococcus aureus in murine mammary glands. Appl. Environ. Microbiol. 2012, 78, 2297–2305.
42. Waxman, D.J.; Stromingerr, J.L. Penicillin-binding proteins and the mechanism of action of beta-lactam antibiotics. Annu. Rev. Biochem. 1983, 52, 825–869.
43. Watkins, K.L.; Shryock, T.R.; Dearth, R.N.; Saif, Y.M. In-vitro antimicrobial susceptibility of Clostridium perfringens from commercial turkey and broiler chicken origin. Vet. Microbiol. 1997, 54, 195–200.
44. Slavic, D.; Boerlin, P.; Fabri, M.; Klotins, K.C.; Zoethout, J.K.; Weir, P.E.; Bateman, D. Antimicrobial susceptibility of Clostridium perfringens isolates of bovine, chicken, porcine, and turkey origin from Ontario. Can. J. Vet. Res. 2011, 75, 89–97.
45. Liu, D.; Guo, Y.; Wang, Z.; Yuan, J. Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathol. 2010, 39, 17–24.
46. Gervasi, T.; Horn, N.; Wegmann, U.; Dugo, G.; Narbad, A.; Mayer, M.J. Expression and delivery of an endolysin to combat Clostridium perfringens. Appl. Microbiol. Biotechnol. 2014, 98, 2495–2505.
47. Schmitz, J.E.; Ossiprandi, M.C.; Rumah, K.R.; Fischetti, V.A. Lytic enzyme discovery through multigenomic sequence analysis in Clostridium perfringens. Appl. Microbiol. Biotechnol. 2011, 89, 1783–1795.
48. Zimmer, M.; Vukov, N.; Scherer, S.; Loessner, M.J. The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl. Environ. Microbiol. 2002, 68, 5311–5317.
49. Kokas, E.; Phillips, J.L., Jr.; Brunson, W.D., Jr. The secretory activity of the duodenum in chickens. Comp. Biochem. Physiol. 1967, 22, 81–90.
50. Lu, J.; Idris, U.; Harmon, B.; Hofacre, C.; Maurer, J.J.; Lee, M.D. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl. Environ. Microbiol. 2003, 69, 6816–6824.
51. Rolls, B.A. Inorganic ions in the intestinal and caecal contents of germ-free and conventional chickens. Lab. Anim. 1977, 11, 99–104.
52. Zettlmeissl, G.; Rudolph, R.; Jaenicke, R. Reconstitution of lactic dehydrogenase. Noncovalent aggregation vs. reactivation. 1. Physical properties and kinetics of aggregation. Biochemistry 1979, 18, 5567–5571.
53. Nohara, D.; Mizutani, A.; Sakai, T. Kinetic study on thermal denaturation of hen egg-white lysozyme involving precipitation. J. Biosci. Bioeng. 1999, 87, 199–205.
54. Heselpoth, R.D.; Nelson, D.C. A new screening method for the directed evolution of thermostable bacteriolytic enzymes. J. Vis. Exp. 2012.
55. Normal Rectal Temperature Ranges Reference Guides Merck Vet Manual. Available online: http://www.merckvetmanual.com/mvm/appendixes/reference:guides/normal_rectal_temperature_ ranges.html (accessed on 25 May 2015).
56. Robertshaw, D. Temperature Regulation and Thermal Environment. In Dukes’ Physiology of Domestic Animals, 12th ed.; Reece, W.O., Ed.; Comstock Publishing Associates: Ithaca, NY, USA, 2004.