The potential of the endolysin Lysdb from Lactobacillus delbrueckii phage for combating Staphylococcus aureus during cheese manufacture from raw milk

Applied Microbiology and Biotechnology

Volumn 100, Issue 8, 2016, Pages 3545-3554

  Guo, Tingting ^a   Xin, YongPing ^a   Zhang, Chenchen ^a   Ouyang, Xudong ^a   Kong, Jian ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Antibacterial; Endolysin; Lactobacillus casei; Staphylococcus aureus

Indexed keywords

FERMENTATION; MANUFACTURE;

ANTIBACTERIAL; BACTERIAL NUMBERS; ENDOLYSIN; FERMENTATION PROCESS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; STAPHYLOCOCCUS AUREUS; TURBIDITY REDUCTION;

BACTERIA;

ANTIBIOTIC AGENT; ENDOLYSIN LYSDB; LYSOZYME; PEPTIDOGLYCAN; UNCLASSIFIED DRUG; ENDOLYSIN; PROTEINASE; VIRAL PROTEIN;

ANIMAL PRODUCT; ANTIMICROBIAL ACTIVITY; BACTERIUM; ENZYME ACTIVITY; FERMENTATION; FOOD POISONING; FOOD PRODUCTION; GENETIC ENGINEERING; PATHOGEN;

AMINO ACID SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOINFORMATICS; CELL WALL; CHEESE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOLYSIS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; MILK; MOLECULAR CLONING; NONHUMAN; STAPHYLOCOCCUS AUREUS; TURBIDITY; ANALYSIS; ANIMAL; BACTERIOPHAGE; BOVINE; DRUG EFFECTS; ENZYMOLOGY; FERMENTATION; FOOD CONTAMINATION; FOOD HANDLING; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PREVENTION AND CONTROL; VIROLOGY;

BACTERIA (MICROORGANISMS); CHALAROPSIS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIOPHAGES; CATTLE; CHEESE; ENDOPEPTIDASES; FERMENTATION; FOOD CONTAMINATION; FOOD HANDLING; LACTOBACILLUS DELBRUECKII; MILK; STAPHYLOCOCCUS AUREUS; VIRAL PROTEINS;

EID: 84948954099     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7185-x     Document Type: Article

References (44)

1. Atrih A, Bacher G, Allmaier G, Williamson MP, Foster SJ (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 181:3956–3966
2. Callewaert L, Walmagh M, Michiels CW, Lavigne R (2011) Food applications of bacterial cell wall hydrolases. Curr Opin Biotechnol 22:164–171
3. Castellano P, Aristoy MC, Sentandreu MA, Vignolo G, Toldrá F (2015) Lactobacillus sakei CRL1862 improves safety and protein hydrolysis in meat systems. J Appl Microbiol 113:1407–1416
4. Catalão MJ, Gil F, Moniz-Pereira J, São-José C, Pimentel M (2012) Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev 37:554–571
5. De Buyser ML, Dufour B, Maire M, Lafarge V (2001) Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 67:1–17
6. Delbes C, Alomar J, Chougui N, Martin JF, Montel MC (2006) Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows raw milk. J Food Prot 69:2161–2167
7. Endersen L, O’Mahony J, Hill C, Ross RP, McAuliffe O, Coffey A (2014) Phage therapy in the food industry. Annu Rev Food Sci T 5:327–349
8. Enouf V, Langella P, Commissaire J, Cohen J, Corthier G (2001) Bovine rotavirus nonstructural protein 4 produced by Lactococcus lactis is antigenic and immunogenic. Appl Environ Microbiol 67:1423–1428
9. Fischetti VA (2008) Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol 11:393–400
10. Fischetti VA (2010) Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int J Med Microbiol 300:357–362
11. Fleurot I, Aigle M, Fleurot R, Darrigo C, Hennekinne JA, Gruss A, Borezée-Durant E, Delacroix-Buchet A (2014) Following pathogen development and gene expression in a food ecosystem: the case of a Staphylococcus aureus isolated in cheese. Appl Environ Microbiol 80:5106–5115
12. Gaeng S, Scherer S, Neve H, Loessner MJ (2000) Gene cloning and expression and secretion of Listeria monocytogens bacteriophage-lytic enzymes in Lactococcus lactis. Appl Environ Microbiol 66:2951–2958
13. Gervasi T, Horn N, Wegmann U, Dugo G, Narbad A, Mayer MJ (2014a) Expression and delivery of an endolysin to combat Clostridium perfringens. Appl Microbiol Biotechnol 98:2495–2505
14. Gervasi T, Lo Gurto R, Minniti E, Narbad A, Mayer MJ (2014b) Application of Lactobacillus johnsonii expressing phage endolysin for control of Clostridium perfringens. Lett Appl Microbiol 59:355–361
15. Gücükoğlu A, Kevenk O, Uyanik T, Cadirci Ő, Terzi G, Alisarli M (2012) Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. J Food Sci 77:620–623
16. Guo T, Kong J, Zhang L, Zhang C, Hu S (2012) Fine tuning of the lactate and diacetyl production through promoter engineering in Lactococcus lactis. PLoS One 7(4):e36296
17. Hazebrouck S, Pothelune L, Azevedo V, Corthier G, Wal JM, Langella P (2007) Efficient production and secretion of bovine beta-lactoglobulin by Lactobacillus casei. Microb Cell Factories 6:12
18. Hugenholtz J (2008) The lactic acid bacterium as a cell factory for food ingredient production. Int Dairy J 18:466–475
19. Jorgensen HJ, Mork T, Hogasen HR, Rovik LM (2005) Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol 99:158–167
20. Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764
21. 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
22. Morello E, Bermúdez-Humarán LG, Llull D, Solé V, Miraglio N, Langella P, Poquet I (2008) Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 14:48–58
23. Obeso JM, Martínez B, Rodríguez A, García P (2008) Lytic activity of the recombinant staphylococcal bacteriophage φH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128:212–218
24. O’Flaherty S, Coffey A, Meaney W, Fitzgerald GF, Ross RP (2005) The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J Bacteriol 187:7161–7164
25. Oliveira H, Melo LD, Santos SB, Nóbrega FL, Ferreira EC, Cerca N, Azeredo J, Kluskens LD (2013) Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol 87:4558–4570
26. Park J, Yun J, Lim J-A, Kang D-H, Ryu S (2012) Characterization of an endolysin, LysBPS13, from a Bacillus cereus bacteriophage. FEMS Microbiol Lett 332:76–83
27. Pérez-Dorado I, Campillo NE, Monterroso B, Hesek D, Lee M, Páez JA, García JL, Mobashery S, Menéndez M, Hermoso JA (2007) Elucidation of the molecular recognition of bacteria cell wall by modular pneumococcal phage endolysin CPL-1. J Biol Chem 282:24990–24999
28. Rau A, Hogg T, Marquardt R, Hilgenfeld R (2000) A new lysozyme fold. Crystal structure of the muramidase from Streptomyces coelicolor at 1.65 Å resolution. J Biol Chem 276:31994–31999
29. 2 and protection of Lactobacillus bulgaricus from oxidative stress in milk. Appl Environ Microbiol 72:5143–5149
30. Rodríguez-Rubio L, Martínez B, Rodríguez A, Donovan DM, García P (2012) Enhanced staphylolytic activity of the staphlococcus aureus bacteriophage vB_SauS-phiIPLA88 HydH5 virion-associated peptidoglygan hydrolase: fusions, deletions, and synergy with LysH5. Appl Environ Microbiol 78:2241–2248
31. Rodríguez-Rubio L, Gutiérrez D, Donovan DM, Martínez B, Rodríguez A, García P (2015) Phage lytic proteins: biotechnological applications beyond clinical antimicrobials. Crit Rev Biotechnol 0:1–11
32. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, vol 1–3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
33. Settanni L, Moschetti G (2010) Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol 27:691–697
34. Thompson K, Collins MA (1996) Improvement in electroporation efficiency for Lactobacillus plantarum by the inclusion of high concentrations of glycine in the growth medium. J Micro Methods 26:73–79
35. Tilkens B, King AM, Glass KA, Sinderlar JJ (2015) Validating the inhibition of Staphylococcus aureus in shelf-stable, ready-to-eat snack sausages with varying combinations of pH and water activity. J Food Prot 78:1215–1220
36. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, Robert C, Oztas S, Mangenot S, Couloux A, Loux V, Dervyn R, Bossy R, Bolotin A, Batto J-M, Walunas T, Gibrat J-F, Bessières P, Weissenbach J, Ehrlich SD, Maguin E (2006) The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci U S A 103:9274–9279
37. Walcher G, Gonano M, Kümmel J, Barker GC, Lebl K, Bereuter O, Ehling-Schulz M, Wagner M, Stessl B (2014) Staphylocuccus aureus reservoirs during traditional Austrian raw milk cheese production. J Dairy Res 81:462–470
38. Wang S, Kong J, Zhang X (2008) Identification and characterization of the two-component cell lysis cassette encoded by temperate bacteriophage φPYB5 of Lactobacillus fermentum. J Appl Microbiol 105:1939–1944
39. Wang S, Kong J, Gao C, Guo T, Liu X (2010) Isolation and characterization of a novel virulent phage (phiLdb) of Lactobacillus delbrueckii. Int J Food Microbiol 137:22–27
40. White R, Chiba S, Pang T, Dewey JS, Savva CG, Holzenburg A, Pogliano K, Young R (2011) Holin triggering in real time. Proc Natl Acad Sci U S A 108:798–803
41. Xu Y, Kong J (2013) Construction and potential application of controlled autolytic systems for Lactobacillus casei in cheese manufacture. J Food Prot 76:1187–1193
42. Yoong P, Schuch R, Nelson D, Fischetti VA (2004) Identification of a broadly active phage lytic enzyme with lethal activity against antibiotic-resistant Enterococcus faecalis and Enterococcus faecium. J Bacteriol 186:4808–4812
43. Young R (2013) Phage lysis: do we have the hole story yet? Curr Opin Microbiol 16:790–797
44. Zhang H, Bao H, Billington C, Hudson JA, Wang R (2012) Isolation and lytic activity of the Listeria bacteriophage endolysin LysZ5 against Listeria monocytogenes in soya milk. Food Microbiol 31:133–136