Syringopeptin SP25A-mediated killing of gram-positive bacteria and the role of teichoic acid D-alanylation

FEMS Microbiology Letters

Volumn 268, Issue 1, 2007, Pages 106-111

  Bensaci, Mekki F ^a   Takemoto, Jon Y ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

Bacillus subtilis; Cyclic lipodepsipeptide; D alanylation; SP25A; Syringopeptin; Teichoic acids

Indexed keywords

ANTIINFECTIVE AGENT; CYCLOPEPTIDE; SYRINGOPEPTIN; TEICHOIC ACID; UNCLASSIFIED DRUG;

ALKALINITY; ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ALANINE; AMINO ACID SEQUENCE; BACTERIAL TOXINS; GRAM-POSITIVE BACTERIA; HUMANS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; TEICHOIC ACIDS;

BACILLUS SUBTILIS; FUNGI; NEGIBACTERIA; POSIBACTERIA; PSEUDOMONAS SYRINGAE;

EID: 33846681240     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2006.00591.x     Document Type: Article

References (32)

1. Adetuyi FC, Isogai A, Di Giorgio D, Ballio A & Takemoto JY (1995) Saprophytic Pseudomonas syringae strain M1 of wheat produces cyclic lipodepsipeptides. FEMS Microbiol Lett 131: 63-67.
2. Ballio A, Barra D, Bossa F et al. (1991) Syringopeptins, new phytotoxic lipodepspeptides of Pseudomonas syringae pv. syringae. FEBS Lett 291: 109-112.
3. Bender CL, Alarcon-Chaidez F & Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63: 266-292.
4. Bidwai AP, Zhang L, Bachmann RC & Takemoto JY (1987) Mechanism of action of Pseudomonas syringae phytotoxin, syringomycin. Stimulation of red beet plasma membrane ATPase activity. Plant Physiol 83: 39-43.
5. Boyd DA, Cvitkovitch DG, Bleiweis AS, Kiriukhin MY, Debabov DV, Neuhaus FC & Hamilton IR (2000) Defects in D-alanyllipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J Bacteriol 182: 6055-6065.
6. Carpaneto A, Dalla Serra M, Menestrina G, Fogliano V & Gambale F (2002) The phytotoxic lipodepsipeptide syringopeptin 25A from Pseudomonas syringae pv syringae forms ion channels in sugar beet vacuoles. J Membr Biol 188: 237-248.
7. Dalla Serra M, Bernhart I, Nordera P, Di Giorgio D, Ballio A & Menestrina G (1999) Conductive properties and gating of channels formed by syringopeptin 25A, a bioactive lipodepsipeptide from Pseudomonas syringae pv. syringae, in planar lipid membranes. Mol Plant Microbe Interact 12: 401-409.
8. DeVay JE, Lukezic FL, Sinden SL, English H & Coplin DL (1968) A biocide produced by pathogenic isolates of Pseudomonas syringae and its possible role in the bacterial canker disease of peach trees. Phytopathology 58: 95-101.
9. Fogliano V, Ballio A, Gallo M, Woo S, Scala F & Lorito M (2002) Pseudomonas lipodepsipeptides and fungal cell wall-degrading enzymes act synergistically in biological control. Mol Plant Microbe Interact 15: 323-333.
10. Grgurina I, Mariotti F, Fogliano V et al. (2002) A new syringopeptin produced by bean strains of Pseudomonas syringae pv. syringae. Biochim Biophys Acta 1597: 81-89.
11. Grgurina I, Bensaci M, Pocsfalvi G, Mannina L, Cruciani O, Fiore A, Fogliano V, Sorensen KN & Takemoto JY (2005) Novel cyclic lipodepsipeptide from Pseudomonas syringae pv. lachrymans strain 508 and syringopeptin antimicrobial activities. Antimicrob Agents Chemother 49: 5037-5045.
12. Haas R, Koch HU & Fischer W (1984) Alanyl turnover from lipoteichoic acid to teichoic acid in Staphylococcus aureus. FEMS Microbiol Lett 21: 27-31.
13. Hutchison ML & Gross DC (1997) Lipopeptide phytotoxins produced by Pseudomonas syringae pv. syringae: comparison of the biosurfactant and ion channel-forming activities of syringopeptin and syringomycin. Mol Plant Microbe Interact 10: 347-354.
14. Hyyrylainen H-L, Vitikainen M, Thwaite J, Wu H, Sarvas M, Harwood CR, Kontinen VP & Stephenson K (2000) D-alanine substitution of teichoic acids as a modulator of protein folding and stability at the cytoplasmic membrane/cell wall interface of Bacillus subtilis. J Biol Chem 275: 26696-26703.
15. Iacobellis NS, Lavermicocca P, Grgurina I, Simmaco M & Ballio A (1992) Phytotoxic properties of Pseudomonas syringae pv. syringae toxins. Physiol Mol Plant Pathol 40: 107-116.
16. Isogai A, Iguchi J, Nakayama J, Kusai A, Takemoto J & Suzuki A (1995) Structural analysis of new syringopeptins by tandem mass spectroscopy. Biosci Biotech Biochem 59: 1374-1376.
17. Jasir AF, Kasprzykowska R, Lindstrom V, Schalen C & Grubb A (2003) New antimicrobial cystatin c-based peptide active against gram-positive bacterial pathogens, including methicillin-resistant Staphylococcus aureus and multiresistant coagulase-negative staphylococci. Acta Pathol Microbiol et Immunol Scandinavica 111: 1004-1010.
18. Kristian SA, Datta V, Weidenmaier C, Kansal R, Fedtke I, Peschel A, Gallo RL & Nizet V (2005) D-alanylation of teichoic acids promotes group a streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187: 6719-6725.
19. Lavermicocca P, Iacobellis N, Simmaco M & Graniti A (1997) Biological properties and spectrum of activity of Pseudomonas syringae pv. syringae toxins. Physiol Mol Plant Pathol 50: 129-140.
20. Liu J & Nikaido H (1999) A mutant of Mycobacterium smegmatis defective in the biosynthesis of mycolic acids accumulates meromycolates. Proc Natl Acad Sci USA 96: 4011-4016.
21. MacArthur AE & Archibald AR (1984) Effect of culture pH on the D-alanine ester content of lipoteichoic acid in Staphylococcus aureus. J Bacteriol 160: 792-793.
22. NCCLS (1993) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard M7-A3, National Committee for Clinical Laboratory Standards, Wayne, PA.
23. NCCLS (2003) Susceptibility Testing of Mycobacteria, Norcardia, and other Aerobic Actinomycetes; Approved Standard, National Committee for Clinical Laboratory Standards, Wayne, PA.
24. Perego M, Glaser P, Minutello A, Strauch MA, Leopold K & Fischer W (1995) Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J Biol Chem 270: 15598-15606.
25. Perry JD, Jones AL & Gould FK (1999) Glycopeptide tolerance in bacteria causing endocarditis. J Antimicrob Chemother 44: 121-124.
26. Peschel A & Sahl H-G (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4: 529-536.
27. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G & Gotz F (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
28. Peschel A, Vuong C, Otto M & Gotz F (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44: 2845-2847.
29. Sambrook J, Fritsch EF & Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Cold Spring Harbor, New York.
30. Scaloni AC, Camoni L, Di Giorgio D, Scortichini M, Cozzolino R & Ballio A (1997) A new syringopeptin produced by a Pseudomonas syringae pv. syringae strain isolated from diseased twigs of laurel. Physiol Mol Plant Pathol 51: 259-264.
31. Takemoto JY, Brand JG, Kaulin YA, Malev VV, Schagina LV & Blasko K (2003) The syringomycins: lipodepsipeptide pore formers from plant bacterium, Pseudomonas syringae. Pore forming peptides and protein toxins (Menestrina G, Serra MD & Lazarovici P, eds), pp. 260-271. Taylor & Francis, London.
32. Vassilev V, Lavermicocca P, Di Giorgio D & Iacobellis NS (1996) Production of syringomycins and syringopeptins by Pseudomonas syringae pv. atrofaciens. Plant Pathol 45: 316-322.