Listeria bacteriophage peptidoglycan hydrolases feature high thermoresistance and reveal increased activity after divalent metal cation substitution

Applied Microbiology and Biotechnology

Volumn 93, Issue 2, 2012, Pages 633-643

  Schmelcher, Mathias ^a,b   Waldherr, Florian ^a   Loessner, Martin J ^a  

^a ETH ZURICH   (Switzerland)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Bacteriophage; Food safety; Listeria; Lytic enzyme; Peptidoglycan hydrolase

Indexed keywords

AMIDASE; CATALYTIC FUNCTIONS; DIVALENT METAL CATIONS; DIVALENT METALS; ELEVATED TEMPERATURE; FUNCTIONAL STATE; GRAM-POSITIVE BACTERIUM; LISTERIA MONOCYTOGENES; LYTIC ENZYMES; NACL CONCENTRATION; OPTIMUM CONDITIONS; PEPTIDOGLYCANS; PH VALUE; PRODUCTION EQUIPMENTS; REFOLDING; THERMORESISTANCE;

BACTERIOPHAGES; CATALYSIS; FOOD SAFETY; HYDROLASES; MANGANESE; MANGANESE COMPOUNDS; PATHOGENS; POSITIVE IONS; SODIUM CHLORIDE; ZINC;

LISTERIA;

AMIDASE; BACTERIAL ENZYME; CALCIUM; COBALT; DIVALENT CATION; EDETIC ACID; HYDROLASE; MANGANESE; METAL ION; RECOMBINANT ENDOLYSIN; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; ZINC;

BACTERIOPHAGE; BACTERIUM; CHEMICAL BINDING; ENZYME ACTIVITY; EXPERIMENTAL STUDY; FOOD SAFETY; LYSIS; OPTIMIZATION; PH; TEMPERATURE EFFECT;

ARTICLE; BACTERIOPHAGE; CATALYSIS; ENZYME ACTIVITY; ENZYME STABILITY; FOOD SAFETY; HEAT TOLERANCE; LISTERIA MONOCYTOGENES; NONHUMAN; PH; SUBSTITUTION REACTION; TEMPERATURE;

BACTERIOPHAGES; CATIONS, DIVALENT; EDETIC ACID; ENZYME ACTIVATORS; ENZYME INHIBITORS; ENZYME STABILITY; HYDROGEN-ION CONCENTRATION; LISTERIA MONOCYTOGENES; METALS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; TEMPERATURE; VIRAL PROTEINS;

LISTERIA; LISTERIA MONOCYTOGENES; POSIBACTERIA;

EID: 84856294356     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3372-6     Document Type: Article

References (56)

1. Becker SC, Foster-Frey J, Donovan DM (2008) The phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol Lett 287:185-191
2. Bernhardt TG, Wang IN, Struck DK, Young R (2002) Breaking free: "protein antibiotics" and phage lysis. Res Microbiol 153:493-501 (Pubitemid 35248113)
3. Briers Y, Lavigne R, Plessers P, Hertveldt K, Hanssens I, Engelborghs Y, Volckaert G (2006) Stability analysis of the bacteriophage phiKMV lysin gp36C and its putative role during infection. Cell Mol Life Sci 63:1899-1905
4. Briers Y, Miroshnikov K, Chertkov O, Nekrasov A, Mesyanzhinov V, Volckaert G, Lavigne R (2008) The structural peptidoglycan hydrolase gp181 of bacteriophage phiKZ. Biochem Biophys Res Commun 374:747-751
5. Cheng Q, Fischetti VA (2006) Mutagenesis of a bacteriophage lytic enzyme PlyGBS significantly increases its antibacterial activity against group B streptococci. Appl Microbiol Biotechnol 74:1284-1291 (Pubitemid 46674066)
6. 2+ atom into the S1 subsite of aminopeptidase A: a key element for substrate specificity. Biochem J 416:37-46
7. Danielsen EM, Noren O, Sjostrom H, Ingram J, Kenny AJ (1980) Proteins of the kidney microvillar membrane. Aspartate aminopeptidase: purification by immunoadsorbent chromatography and properties of the detergent- and proteinase-solubilized forms. Biochem J 189:591-603
8. Donovan DM, Lardeo M, Foster-Frey J (2006) Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiol Lett 265:133-139 (Pubitemid 44715454)
9. Dorscht J, Klumpp J, Bielmann R, Schmelcher M, Born Y, Zimmer M, Calendar R, Loessner MJ (2009) Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site. J Bacteriol 191:7206-7215
10. Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476-511 (Pubitemid 21895164)
11. Fiedler F, Ruhland G (1987) Structure of Listeria monocytogenes cell walls. Bull Inst Pasteur 85:287-300
12. Fiedler F, Seger J, Schrettenbrunner A, Seeliger HPR (1984) The biochemistry of murein and cell wall teichoic acids in the genus Listeria. Syst Appl Microbiol 5:360-376 (Pubitemid 15187179)
13. Fischetti VA (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13:491-496 (Pubitemid 41317527)
14. Fischetti VA (2010) Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int J Med Microbiol 300:357-362
15. Fukushima T, Yao Y, Kitajima T, Yamamoto H, Sekiguchi J (2007) Characterization of new L, D-endopeptidase gene product CwlK (previous YcdD) that hydrolyzes peptidoglycan in Bacillus subtilis. Mol Genet Genomics 278:371-383 (Pubitemid 47437681)
16. Gaeng S, Scherer S, Neve H, Loessner MJ (2000) Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl Environ Microbiol 66:2951-2958 (Pubitemid 30497604)
17. 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
18. Good NE, Winget GD, Winter W, Connolly TN, Izawa S, Singh RM (1966) Hydrogen ion buffers for biological research. Biochemistry 5:467-477
19. Guenther S, Loessner MJ (2011) Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 1:94-100
20. Hagens S, Loessner MJ (2007) Application of bacteriophages for detection and control of foodborne pathogens. Appl Microbiol Biotechnol 76:513-519 (Pubitemid 47283108)
21. Hermoso JA, Garcia JL, Garcia P (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol 10:461-472 (Pubitemid 350064581)
22. Korndoerfer IP, Danzer J, Schmelcher M, Zimmer M, Skerra A, Loessner MJ (2006) The crystal structure of the bacteriophage PSA endolysin reveals a unique fold responsible for specific recognition of Listeria cell walls. J Mol Biol 364:678-689 (Pubitemid 44755313)
23. Korndoerfer IP, Kanitz A, Danzer J, Zimmer M, Loessner MJ, Skerra A (2008) Structural analysis of the L-alanoyl-D-glutamate endopeptidase domain of Listeria bacteriophage endolysin Ply500 reveals a new member of the LAS peptidase family. Acta Crystallogr D Biol Crystallogr 64:644-650 (Pubitemid 351872065)
24. Kretzer JW, Lehmann R, Schmelcher M, Banz M, Kim KP, Korn C, Loessner MJ (2007) High affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol 73:1992-2000 (Pubitemid 46449084)
25. Kyomuhendo P, Myrnes B, Nilsen IW (2007) A cold-active salmon goose-type lysozyme with high heat tolerance. Cell Mol Life Sci 64:2841-2847 (Pubitemid 351152266)
26. Lavigne R, Briers Y, Hertveldt K, Robben J, Volckaert G (2004) Identification and characterization of a highly thermostable bacteriophage lysozyme. Cell Mol Life Sci 61:2753-2759 (Pubitemid 40022438)
27. Loeffler JM, Nelson D, Fischetti VA (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294:2170-2172 (Pubitemid 33150674)
28. Loeffler JM, Djurkovic S, Fischetti VA (2003) Phage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia. Infect Immun 71:6199-6204 (Pubitemid 37337675)
29. Loessner MJ (2005) Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol 8:480-487 (Pubitemid 41021911)
30. Loessner MJ, Schneider A, Scherer S (1995a) A new procedure for efficient recovery of DNA, RNA, and proteins from Listeria cells by rapid lysis with a recombinant bacteriophage endolysin. Appl Environ Microbiol 61:1150-1152
31. Loessner MJ, Wendlinger G, Scherer S (1995b) Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol Microbiol 16:1231-1241
32. Loessner MJ, Schneider A, Scherer S (1996) Modified Listeria bacteriophage lysin genes (ply) allow efficient overexpression and one-step purification of biochemically active fusion proteins. Appl Environ Microbiol 62:3057-3060
33. Loessner MJ, Kramer K, Ebel F, Scherer S (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44:335-349 (Pubitemid 34429740)
34. Low LY, Yang C, Perego M, Osterman A, Liddington RC (2005) Structure and lytic activity of a Bacillus anthracis prophage endolysin. J Biol Chem 280:35433-35439 (Pubitemid 41532733)
35. McCafferty DG, Lessard IA, Walsh CT (1997) Mutational analysis of potential zinc-binding residues in the active site of the enterococcal D-Ala-D-Ala dipeptidase VanX. Biochemistry 36:10498-10505 (Pubitemid 27374142)
36. Mikoulinskaia GV, Odinokova IV, Zimin AA, Lysanskaya VY, Feofanov SA, Stepnaya OA (2009) Identification and characterization of the metal ion-dependent L-alanoyl-D-glutamate peptidase encoded by bacteriophage T5. FEBS J 276:7329-7342
37. Morita M, Tanji Y, Mizoguchi K, Soejima A, Orito Y, Unno H (2001) Antibacterial activity of Bacillus amyloliquefaciens phage endolysin without holin conjugation. J Biosci Bioeng 91:469-473 (Pubitemid 32565181)
38. Murzin AG (1996) Structural classification of proteins: new superfamilies. Curr Opin Struct Biol 6:386-394 (Pubitemid 26197440)
39. Nelson D, Loomis L, Fischetti VA (2001) Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc Natl Acad Sci USA 98:4107-4112 (Pubitemid 32249906)
40. Pritchard DG, Dong S, Baker JR, Engler JA (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 150:2079-2087 (Pubitemid 39117622)
41. Sambrook J, Maniatis J, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
42. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407-477
43. Schmelcher M, Shabarova T, Eugster MR, Eichenseher F, Tchang VS, Banz M, Loessner MJ (2010) Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl Environ Microbiol 76:5745-5756
44. Schmelcher M, Tchang VS, Loessner MJ (2011) Domain shuffling and module engineering of Listeria phage endolysins for enhanced lytic activity and binding affinity. Microb Biotechnol. doi: 10.1111/j.1751-7915.2011.00263.x
45. 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. doi:
46. Shida T, Hattori H, Ise F, Sekiguchi J (2001) Mutational analysis of catalytic sites of the cell wall lytic N-acetylmuramoyl-L-alanine amidases CwlC and CwlV. J Biol Chem 276:28140-28146
47. Sugahara K, Yokoi KJ, Nakamura Y, Nishino T, Yamakawa A, Taketo A, Kodaira KI (2007) Mutational and biochemical analyses of the endolysin Lys(gaY) encoded by the Lactobacillus gasseri JCM 1131(T) phage phigaY. Gene 404:41-52 (Pubitemid 47562642)
48. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680 (Pubitemid 24354800)
49. Turner MS, Waldherr F, Loessner MJ, Giffard PM (2006) 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)
50. Vanderzant C, Splittstoesser DF (1992) Compendium of methods for the microbiological examination of foods, 3rd edn. APHA, Washington
51. Vasala A, Valkkila M, Caldentey J, Alatossava T (1995) Genetic and biochemical characterization of the Lactobacillus delbrueckii subsp. lactis bacteriophage LL-H lysin. Appl Environ Microbiol 61:4004-4011
52. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, Goebel W, Gonzalez-Zorn B, Wehland J, Kreft J (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584-640 (Pubitemid 32642752)
53. Wendlinger G, Loessner MJ, Scherer S (1996) Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself. Microbiology 142:985-992 (Pubitemid 26139373)
54. 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 (Pubitemid 38891043)
55. 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
56. Young I, Wang I, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120-128 (Pubitemid 30155487)