Functional characterization of a new holin-like antibacterial protein coding gene tmp1 from goat skin surface metagenome

Applied Microbiology and Biotechnology

Volumn 89, Issue 4, 2011, Pages 1061-1073

  Rajesh, Thangamani ^a   Anthony, Thangamani ^a,b   Saranya, Subramani ^a,c   Pushpam, Paul Lavanya ^a   Gunasekaran, Paramasamy ^a  

^a MADURAI KAMARAJ UNIVERSITY   (India)

^b HH Rajah's Government College   (India)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Antibacterial activity; Hemolytic activity; Holin like protein; Metagenome; Site directed mutagenesis; Transmembrane domain

Indexed keywords

ANTI-BACTERIAL ACTIVITY; HEMOLYTIC ACTIVITY; HOLIN-LIKE PROTEIN; METAGENOMES; SITE-DIRECTED MUTAGENESIS; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; AMINO ACIDS; BACTERIOLOGY; BACTERIOPHAGES; ESCHERICHIA COLI; GENES; MUTAGENESIS; PROTEINS;

BACTERIA;

BACTERIAL PROTEIN; TMP1 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID; ANTIMICROBIAL ACTIVITY; COLIFORM BACTERIUM; GENE EXPRESSION; GENOME; GOAT; HYDROPHOBICITY; PROTEIN; SKIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIOLYSIS; BACTERIOPHAGE LAMBDA; CONTROLLED STUDY; DRUG SPECIFICITY; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENOTYPE; GOAT; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEMOLYSIS; HYDROPHOBICITY; METAGENOME; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RANDOMIZED CONTROLLED TRIAL; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SKIN SURFACE; ZYMOGRAPHY;

ANIMALS; BACTERIOPHAGE LAMBDA; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; GOATS; GRAM-POSITIVE BACTERIA; METAGENOME; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SKIN; VIRAL PROTEINS;

CAPRA HIRCUS; ENTEROBACTERIA PHAGE LAMBDA; ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA;

EID: 79952533678     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-010-2907-6     Document Type: Article

References (51)

1. Agu CA, Klein R, Schwab S, König-Schuster M, Kodajova P, Ausserlechner M, Binishofer B, Bläsi U, Salmons B, Günzburg WH, Hohenadl C (2006) The cytotoxic activity of the bacteriophage lambda-holin protein reduces tumour growth rates in mammary cancer cell xenograft models. J Gene Med 8:229-241 (Pubitemid 43250703)
2. Agu CA, Klein R, Lengler J, Schilcher F, Gregor W, Peterbauer T, Bläsi U, Salmons B, Günzburg WH, Hohenadl C (2007) Bacteriophage-encoded toxins: the lambda-holin protein causes caspase-independent non-apoptotic cell death of eukaryotic cells. Cell Microbiol 9:1753-1765 (Pubitemid 46958801)
3. Altschul SF, Gish W, Miller W, Myers EM, Lipmann DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
4. Anthony T, Rajesh T, Kayalvizhi N, Gunasekaran P (2009) Influence of medium components and fermentation conditions on the production of bacteriocin(s) by Bacillus licheniformis AnBa9. Bioresour Technol 100:872-877
5. Anthony T, Stalin CG, Rajesh T, Gunasekaran P (2010) Functional analysis of a putative holin-like peptide coding gene in the genome of Bacillus licheniformis AnBa9. Arch Microbiol 192:51-56
6. Berkmen M, Benedik MJ, Bläsi U (1997) The Serratia marcescens NucE functions as a holin in Escherichia coli. J Bacteriol 179:6522-6524 (Pubitemid 27443941)
7. Borysowski J, Weber-Dabrowka B, Gorski A (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med 231:366-377
8. Chen HC, Brown JH, Morell JL, Huang CM (1988) Synthetic magainin analogues with improved antimicrobial activity. FEBS Lett 236:462-466
9. Chen Y, Guarnieri MT, Vasil AI, Vasil ML, Mant CT, Hodges RS (2007) Role of peptide hydrophobicity in the mechanism of action of alpha-helical antimicrobial peptides. Antimicrob Agents Chemother 51:1398-1406 (Pubitemid 46586822)
10. Courchesne NMD, Parisien A, Lan CQ (2009) Production and application of bacteriophage and bacteriophage-encoded lysins. Recent Pat Biotechnol 3:37-45
11. Courtois S, Cappellano MC, Ball M, Francou XF, Normand P, Helynck G, Mareinez A, Kolvek JS, Hopke J, Osburne SM, August RP, Nalin R, Guèrineau M, Jeannin P, Simonet P, Pernodet L (2003) Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 69:46-55
12. Croux C, Ronda C, Lopez P, Garcia J (1993) Interchange of functional domains switches enzyme specificity: construction of a chimeric pneumococcal-clostridial cell wall lytic enzyme. Mol Microbiol 9:1019-1025 (Pubitemid 23271779)
13. Cuervo J, Rodriquez B, Houghten R (1990) The magainins: sequence factors relevant to increased antimicrobial activity and decreased hemolytic activity. Pept Res 1:81-86
14. Damman JC, Eggers CH, Samuels DS, Oliver DB (2000) Characterization of Borrelia burgdorferi BlyA and BlyB proteins: a prophage-encoded holin-like system. J Bacteriol 182:6791-6797 (Pubitemid 32249263)
15. Delisle LA, Barcak GJ, Guo M (2006) Isolation and expression of the lysis genes of Actinomyces naeslundii phage Av-1. J Bacteriol 71:1110-1117 (Pubitemid 43271216)
16. Drider D, Fimland G, Hechard Y, McMullen LM, Prevost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564-582 (Pubitemid 43895038)
17. Friedrich CL, Moyles D, Beveridge TJ, Hancock ER (2000) Antibacterial action of structurally diverse cationic peptides on Gram-positive bacteria. Antimicrob Agents Chemother 44:2086-2092 (Pubitemid 30484431)
18. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR, Clardy J, Goodman RM, Handelsman J (2002) Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68:4301-4306 (Pubitemid 34988109)
19. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:245-249
20. Haro A, Vèlez M, Goormaghtigh E, Lago S, Vàzquez J, Andreu D, Gasset M (2003) Reconstitution of holin activity with a synthetic peptide containing the 1-32 sequence of EJh, the phage EJ-1 phage holin. J Biol Chem 278:3929-3936 (Pubitemid 36801124)
21. Helmerhorst EJ, Reijnders IM, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (1999) A critical evaluation of the lytic activity of cationic antimicrobial peptides against Candida albicans cells and human erythrocytes. FEBS Lett 449:105-110
22. Henrich B, Binishofer B, Bläsi U (1990) Primary structure and functional analysis of the lysis of Lactobacillus gasseri bacterio-phage φadh. J Bacteriol 177:723-732
23. Hofmann K, Stoffel W (1993) TMbase - a database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 347:166-171
24. Kang YJ, Frank JF (1990) Characteristics of biological aerosols in dairy and processing plants. J Dairy Sci 73:621-626
25. Kayalvizhi N, Anthony T, Gunasekaran P (2008) Characterization of the predominant bacteria associated with sheep and goat skin. J Am Leather Chem Assoc 103:182-187
26. Kiyota T, Lee S, Sugihara G (1996) Design and synthesis of amphiphilic α-helical model peptides with systematically varied hydrophobic- hydrophilic balance and their interaction with lipid- and bio-membranes. Biochemistry 35:13196-13204 (Pubitemid 26349472)
27. Kondejewski LH, Lee DL, Niaraki MJ, Farmer SW, Hancock REW, Hodges RS (2002) Optimization of microbial specificity in cyclic peptides by modulation of hydrophobicity within a defined structural framework. J Biol Chem 277:67-74 (Pubitemid 34952029)
28. Koo SP, Bayer AS, Sahl HG, Proctor RA, Yeaman MR (1996) Staphylocidal action of thrombin-induced platelet microbicidal protein is not solely dependent on transmembrane potential. Infect Immun 64:1070-1074 (Pubitemid 26065593)
29. Kordel M, Benz R, Sahl HG (1988) Mode of action of the staphylococcin like peptide Pep 5: voltage-dependent depolarization of bacterial and artificial membranes. J Bacteriol 170:84-88 (Pubitemid 18028525)
30. Kourie JI, Shorthouse AA (2008) Properties of cytotoxic peptide formed ion channels. Am J Physiol Cell Physiol 278:1063-1087
31. Kwon MY, Hong SY, Lee KH (1998) Structure-activity analysis of brevinin 1E amide, an antimicrobial peptide from Rana esculenta. Biochim Biophys Acta 1387:239-248
32. Loessner MJ, Gaeng S, Scherer S (1999) Evidence for a holin-like protein gene fully embedded out of frame in the endolysin gene of Staphylococcus aureus bacteriophage 187. J Bacteriol 181:4452-4460 (Pubitemid 29357922)
33. Madden HR (1994) Microbial hazards in animal products. Proc Nutr Soc UK 53:309-316
34. Oren Z, Shai Y (1997) Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry 18:1826-1835 (Pubitemid 27086279)
35. Oren Z, Hong J, Shai Y (1997) A repertoire of novel antibacterial diasteriometric peptides with selective cytolytic activity. J Biol Chem 272:14643-14649 (Pubitemid 27251727)
36. Park T, Struck DK, Deaton JF, Young R (2006) Topological dynamics of holins in programmed bacterial lysis. Proc Natl Acad Sci 103:19713-19718 (Pubitemid 46037497)
37. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, New York
38. Sao-Jose C, Parreira R, Vieira G, Santos MA (2000) The N-terminal region of the Oenococcus oeni bacteriophage fOg44 lysin behaves as a bona fide signal peptide in Escherichia coli and as a cis-inhibitory element, preventing lytic activity on oenococcal cells. J Bacteriol 182:5823-5831
39. Schloss DS, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6:229.1-229.4
40. Seow KT, Meurer G, Gerlitz M, Wendt-Pienkowski E, Hutchinson CR, Davies J (1997) A study of iterative type II polyketide synthases, using bacterial genes cloned from soil DNA: a means to access and use genes from uncultured microorganisms. J Bacteriol 179:7360-7368 (Pubitemid 27509973)
41. Shai Y, Bach D, Yanovsky A (1996) Diastereomers of cytolysins, a novel class of potent antibacterial peptides. J Biol Chem 271:7305-7308 (Pubitemid 26106994)
42. Uchiyama T, Watanabe K (2006) Improved inverse PCR scheme for metagenome walking. BioTechniques 41:183-188 (Pubitemid 46542602)
43. Wang IN, Smith DL, Young R (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799-825
44. Wieprecht T, Dathe M, Beyermann M, Krause E, Maloy WL, MacDonald DL, Bienert M (1997) Peptide hydrophobicity controls the activity and selectivity of magainin 2 amide in interaction with membranes. Biochem 36:6124-6132 (Pubitemid 27257879)
45. Wu M, Hancock REW (1999) Interaction of the cyclic antimicrobial cationic peptide actenecin with the outer and cytoplasmic membrane. J Biol Chem 274:29-35 (Pubitemid 29035025)
46. Xu M, Struck DK, Deaton J, Wang N, Young R (2004) A signal arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci USA 101:6415-6420 (Pubitemid 38585988)
47. Yeates C, Gillings MR, Davison AD, Altavilla N, Veal DA (1998) Methods for microbial DNA extraction from soil for PCR amplification. Biol Proced Online 1:40-47
48. Yokogawa KS, Nishimura KS, Ikeda Y, Yoshimura Y (1974) Mutanolysin, bacteriolytic agent for cariogenic Streptococci: partial purification and properties. Antimicrob Agents Chemother 6:156-165
49. Young R (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56:430-481
50. Zairi A, Tangy F, Bouassida K, Hani K (2009) Dermaseptins and magainins: antimicrobial peptides from frogs' skin - new sources for a promising spermicides microbicides - a mini review. J Biomed Biotechnol 2009(452567):8. doi:10.1155/2009/452567
51. Ziedaite G, Daugelavicius R, Bamford HKJ, Bamford HD (2005) The holin protein of bacteriophage PRD1 forms a pore for small molecule endolysin translocation. J Bacteriol 187:5397-5405 (Pubitemid 41022959)