Characterization of a novel cell wall binding domain-containing Staphylococcus aureus endolysin LysSA97

Applied Microbiology and Biotechnology

Volumn 101, Issue 1, 2017, Pages 147-158

  Chang, Yoonjee ^a   Ryu, Sangryeol ^a,b  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Antibacterial; Cell wall binding domain; Endolysin; Staphylococcus aureus

Indexed keywords

AMINO ACIDS; BACTERIA; BIOINFORMATICS; CELLS; CLONING; CYTOLOGY; PROTEINS;

ANTIBACTERIAL; BIOINFORMATIC ANALYSIS; CELL WALL-BINDING DOMAIN; DOMAIN COMPOSITION; ENDOLYSIN; GREEN FLUORESCENT PROTEIN; STAPHYLOCOCCAL STRAINS; STAPHYLOCOCCUS AUREUS;

BINS;

AMIDASE; BACTERIAL ENZYME; BACTERIAL PROTEIN; BINDING PROTEIN; CYSTEINE; GREEN FLUORESCENT PROTEIN; HISTIDINE; HYBRID PROTEIN; N ACETYLMURAMOYLALANINE AMIDASE; PEPTIDASE; STAPHYLOCOCCAL ENDOLYSIN; UNCLASSIFIED DRUG; ENDOLYSIN; PROTEIN BINDING; PROTEINASE;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; CELLS AND CELL COMPONENTS; ENZYME; ENZYME ACTIVITY; GENE EXPRESSION; HOMOLOGY; PROTEIN; THERMOPHILIC BACTERIUM;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL STRAIN; BIOFILM; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; CLONING; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVE SITE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN DOMAIN; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PHAGE; BINDING SITE; BIOLOGY; CELL WALL; DNA SEQUENCE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; PHYSIOLOGY; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS PHAGE; VIROLOGY;

STAPHYLOCOCCUS AUREUS;

BINDING SITES; BIOFILMS; CELL WALL; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; ENDOPEPTIDASES; PROTEIN BINDING; PROTEIN DOMAINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES;

EID: 84982958297     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-016-7747-6     Document Type: Article

References (57)

1. Altschul SF, Madden TL, Schaffer 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. doi:10.1093/nar/25.17.3389
2. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME (2011) Staphylococcus aureus biofilms properties, regulation and roles in human disease. Virulence 2:445–459. doi:10.4161/viru.2.5.17724
3. Arciola CR, Montanaro L, Baldassarri L, Borsetti E, Cavedagna D, Donati E (1999) Slime production by staphylococci isolated from prosthesis-associated infections. New Microbiol 22:337–341. doi:10.1007/978-1-4471-3454-1_55
4. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190:300–310. doi:10.1128/JB.01000-07
5. Becker SC, Foster-Frey J, Stodola AJ, Anacker D, Donovan DM (2009) Differentially conserved staphylococcal SH3b_5 cell wall binding domains confer increased staphylolytic and streptolytic activity to a streptococcal prophage endolysin domain. Gene 443:32–41. doi:10.1016/j.gene.2009.04.023
6. Chang Y, Lee JH, Shin H, Heu S, Ryu S (2013) Characterization and complete genome sequence analysis of Staphylococcus aureus bacteriophage SA12. Virus Genes 47:389–393. doi:10.1007/s11262-013-0938-7
7. Chang Y, Shin H, Lee JH, Park C, Paik S, Ryu S (2015) Isolation and genome characterization of the virulent Staphylococcus aureus bacteriophage SA97. Viruses 7:5225–5242. doi:10.3390/v7102870
8. Cone LA, Sontz EM, Wilson JW, Mitruka SN (2005) Staphylococcus capitis endocarditis due to a transvenous endocardial pacemaker infection: case report and review of Staphylococcus capitis endocarditis. Int J Infect Dis 9:335–339. doi:10.1016/j.ijid.2004.08.004
9. Cuong Vuong MO (2002) Staphylococcus epidermidis infections. Microbes Infec 4:481–489. doi:10.1016/S1286-4579(02)01563-0
10. Daniel B, Saleem M, Naseer G, Fida A (2014) Significance of Staphylococcus haemolyticus in hospital acquired infections. J Pioneer Med Sci 4:119–125
11. Eugster MR, Haug MC, Huwiler SG, Loessner MJ (2011) The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid. Mol Microbiol 81:1419–1432. doi:10.1111/j.1365-2958.2011.07774.x
12. Fein JE, Rogers HJ (1976) Autolytic enzyme-deficient mutants of Bacillus subtilis 168. J Bacteriol 127:1427–1442
13. k eliminates and prevents staphylococcal biofilms. Int J Microbiol 2013:625341. doi:10.1155/2013/625341
14. Fernandes S, Proenca D, Cantante C, Silva FA, Leandro C, Lourenco S, Milheirico C, de Lencastre H, Cavaco-Silva P, Pimentel M, Sao-Jose C (2012) Novel chimerical endolysins with broad antimicrobial activity against methicillin-resistant Staphylococcus aureus. Microb Drug Resist 18:333–343. doi:10.1089/mdr.2012.0025
15. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230. doi:10.1093/nar/gkt1223
16. Fischetti VA (2008) Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol 11:393–400. doi:10.1016/j.mib.2008.09.012
17. Fox LK, Zadoks RN, Gaskins CT (2005) Biofilm production by Staphylococcus aureus associated with intramammary infection. Vet Microbiol 107:295–299. doi:10.1016/j.vetmic.2005.02.005
18. 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. doi:10.1128/aem.66.7.2951-2958.2000
19. Grundling A, Schneewind O (2006) Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J Bacteriol 188:2463–2472. doi:10.1128/JB.188.7.2463-2472.2006
20. Gu J, Lu R, Liu X, Han W, Lei L, Gao Y, Zhao H, Li Y, Diao Y (2011a) LysGH15B, the SH3b domain of staphylococcal phage endolysin LysGH15, retains high affinity to staphylococci. Curr Microbiol 63:538–542. doi:10.1007/s00284-011-0018-y
21. Gu J, Xu W, Lei L, Huang J, Feng X, Sun C, Du C, Zuo J, Li Y, Du T, Li L, Han W (2011b) LysGH15, a novel bacteriophage lysin, protects a murine bacteremia model efficiently against lethal methicillin-resistant Staphylococcus aureus infection. J Clin Microbiol 49:111–117. doi:10.1128/JCM.01144-10
22. Hadzija O (1974) A simple method for the quantitative determination of muramic acid. Anal Biochem 60:512–517. doi:10.1016/0003-2697(74)90261-9
23. Hazenberg MP, de Visser H (1992) Assay for N-acetylmuramyl-L-alanine amidase in serum by determination of muramic acid released from the peptidoglycan of Brevibacterium divaricatum. Eur J Clin Chem Clin Biochem 30:141–144
24. Hendrickx AP, van Schaik W, Willems RJ (2013) The cell wall architecture of Enterococcus faecium: from resistance to pathogenesis. Future Microbiol 8:993–1010. doi:10.2217/Fmb.13.66
25. Hovelius B, Mardh PA (1984) Staphylococcus saprophyticus as a common cause of urinary-tract infections. Rev Infect Dis 6:328–337. doi:10.1093/clinids/6.3.328
26. Jin JW, Zhang L, Zha XL, Li HL, Qu D (2005) Effect of glucose on biofilm and the gene ica expression in Staphylococcus epidermidis with different biofilm-forming capability. Acta Microbiol Sin 45:431–436
27. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. doi:10.1093/bioinformatics/btu031
28. Kamisango K, Saiki I, Tanio Y, Okumura H, Araki Y, Sekikawa I, Azuma I, Yamamura Y (1982) Structures and biological-activities of peptidoglycans of Listeria monocytogenes and Propionibacterium acnes. J Biochem 92:23–33
29. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306. doi:10.1093/bib/bbn017
30. Kuroda A, Sekiguchi J (1990) Cloning, sequencing and genetic mapping of a Bacillus subtilis cell wall hydrolase gene. J Gen Microbiol 136:2209–2216. doi:10.1099/00221287-136-11-2209
31. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404
32. Leive L (1968) Studies on the permeability change produced in coliform bacteria by ethylenediaminetetraacetate. J Biol Chem 243:2373–2380
33. Loeffler JM, Nelson D, Fischetti VA (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294:2170–2172. doi:10.1126/science.1066869
34. Loessner MJ (2005) Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol 8:480–487. doi:10.1016/j.mib.2005.06.002
35. 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. doi:10.1046/j.1365-2958.2002.02889.x
36. Melchior MB, Vaarkamp H, Fink-Gremmels J (2006) Biofilms: a role in recurrent mastitis infections? Vet J 171:398–407. doi:10.1016/j.tvjl.2005.01.006
37. Moreira JMR, Gomes LC, Araujo JDP, Miranda JM, Simoes M, Melo LF, Mergulhao FJ (2013) The effect of glucose concentration and shaking conditions on Escherichia coli biofilm formation in microtiter plates. Chem Eng Sci 94:192–199. doi:10.1016/j.ces.2013.02.045
38. Obeso JM, Martinez B, Rodriguez A, Garcia P (2008) Lytic activity of the recombinant staphylococcal bacteriophage phiH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128:212–218. doi:10.1016/j.ijfoodmicro.2008.08.010
39. Oliveira H, Azeredo J, Lavigne R, Kluskens LD (2012) Bacteriophage endolysins as a response to emerging foodborne pathogens. Trends Food Sci Tech 28:103–115. doi:10.1016/j.tifs.2012.06.016
40. Oliveira H, Melo LD, Santos SB, Nobrega FL, Ferreira EC, Cerca N, Azeredo J, Kluskens LD (2013) Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol 87:4558–4570. doi:10.1128/JVI.03277-12
41. Park KH, Kurokawa K, Zheng L, Jung DJ, Tateishi K, Jin JO, Ha NC, Kang HJ, Matsushita M, Kwak JY, Takahashi K, Lee BL (2010) Human serum mannose-binding lectin senses wall teichoic acid Glycopolymer of Staphylococcus aureus, which is restricted in infancy. J Biol Chem 285:27167–27175. doi:10.1074/jbc.M110.141309
42. Park J, Yun J, Lim JA, Kang DH, Ryu S (2012) Characterization of an endolysin, LysBPS13, from a Bacillus cereus bacteriophage. FEMS Microbiol Lett 332:76–83. doi:10.1111/j.1574-6968.2012.02578.x
43. Regulski K, Courtin P, Kulakauskas S, Chapot-Chartier MP (2013) A novel type of peptidoglycan-binding domain highly specific for amidated D-asp cross-bridge, identified in Lactobacillus casei bacteriophage endolysins. J Biol Chem 288:20416–20426. doi:10.1074/jbc.M112.446344
44. Salazar JK, Wu ZC, Yang WX, Freitag NE, Tortorello ML, Wang H, Zhang W (2013) Roles of a novel Crp/Fnr family transcription factor Lmo0753 in soil survival, biofilm production and surface attachment to fresh produce of Listeria monocytogenes. PLoS One 8:e75736. doi:10.1371/journal.pone.0075736
45. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477
46. Schmelcher M, Shen Y, Nelson DC, Eugster MR, Eichenseher F, Hanke DC, Loessner MJ, Dong S, Pritchard DG, Lee JC, Becker SC, Foster-Frey J, Donovan DM (2015) Evolutionarily distinct bacteriophage endolysins featuring conserved peptidoglycan cleavage sites protect mice from MRSA infection. J Antimicrob Chemoth 70:1453–1465. doi:10.1093/jac/dku552
47. Shen Y, Koller T, Kreikemeyer B, Nelson DC (2013) Rapid degradation of Streptococcus pyogenes biofilms by PlyC, a bacteriophage-encoded endolysin. J Antimicrob Chemother 68:1818–1824. doi:10.1093/jac/dkt104
48. Simoes LC, Simoes M, Vieira MJ (2007) Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol 73:6192–6200. doi:10.1128/Aem.00837-07
49. Son JS, Lee SJ, Jun SY, Yoon SJ, Kang SH, Paik HR, Kang JO, Choi YJ (2010) Antibacterial and biofilm removal activity of a podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl Microbiol Biotechnol 86:1439–1449. doi:10.1007/s00253-009-2386-9
50. Son B, Yun J, Lim JA, Shin H, Heu S, Ryu S (2012) Characterization of LysB4, an endolysin from the Bacillus cereus-infecting bacteriophage B4. BMC Microb 12:33. doi:10.1186/1471-2180-12-33
51. Szweda P, Schielmann M, Kotlowski R, Gorczyca G, Zalewska M, Milewski S (2012) Peptidoglycan hydrolases-potential weapons against Staphylococcus aureus. Appl Microbiol Biotechnol 96:1157–1174. doi:10.1007/s00253-012-4484-3
52. Theodoros Kelesidis ST (2010) Staphylococcus intermedius is not only a zoonotic pathogen, but may also cause skin abscesses in humans after exposure to saliva. Int J Infect Dis 14:e838–e841. doi:10.1016/j.ijid.2010.02.2249
53. Voineagu L, Braga V, Botnarciuc M, Barbu A, Tataru M (2012) Emergence of Staphylococcus hominis strains in general infections. ARS Medica Tomitana 18:80–82. doi:10.2478/v10307-012-0016-8
54. tm1Lau mice with dermatitis. Microbiol Immunol 46:629–632
55. Wu JA, Kusuma C, Mond JJ, Kokai-Kun JF (2003) Lysostaphin disrupts Staphylococcus aureus and Staphylococcus epidermidis biofilms on artificial surfaces. Antimicrob Agents Chemother 47:3407–3414. doi:10.1128/aac.47.11.3407-3414.2003
56. Yang H, Zhang Y, Huang Y, Yu J, Wei H (2014a) Degradation of methicillin-resistant Staphylococcus aureus biofilms using a chimeric lysin. Biofouling 30:667–674. doi:10.1080/08927014.2014.905927
57. Yang H, Zhang Y, Yu J, Huang Y, Zhang XE, Wei H (2014b) Novel chimeric lysin with high-level antimicrobial activity against methicillin-resistant Staphylococcus aureus in vitro and in vivo. Antimicrob Agents Chemother 58:536–542. doi:10.1128/AAC.01793-13