Isolation, structure elucidation, and synergistic antibacterial activity of a novel two-component lantibiotic lichenicidin from bacillus licheniformis VK21

Biochemistry

Volumn 49, Issue 30, 2010, Pages 6462-6472

  Shenkarev, Zakhar O ^a   Finkina, Ekaterina I ^a   Nurmukhamedova, Elina K ^a   Balandin, Sergey V ^a   Mineev, Konstantin S ^a   Nadezhdin, Kirill D ^a   Yakimenko, Zoya A ^a   Tagaev, Andrey A ^a   Temirov, Yuri V ^a   Arseniev, Alexander S ^a   Ovchinnikova, Tatiana V ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; ANTI-BACTERIAL ACTIVITY; ANTIBIOTIC ACTIVITY; BACILLUS LICHENIFORMIS; GRAM-POSITIVE BACTERIUM; LANTIBIOTICS; METHANOL SOLUTION; MICROMOLAR CONCENTRATION; MOLECULAR INSIGHTS; N-AND C-TERMINAL DOMAINS; N-TERMINALS; NANOMOLAR CONCENTRATION; NMR SPECTROSCOPY; SPATIAL STRUCTURE; STRUCTURAL GENE; STRUCTURAL HOMOLOGY; STRUCTURE ELUCIDATION; THIOETHERS; TWO-COMPONENT;

AMINO ACIDS; BACTERIA; BACTERIOLOGY; FLEXIBLE DISPLAYS; GENE ENCODING; METHANOL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORGANIC ACIDS; PLANTS (BOTANY);

PEPTIDES;

AMINO ACID; HALODURACIN ALPHA; HALODURACIN BETA; LACTICIN A1; LACTICIN A2; LANTIBIOTIC; LICHENICIDIN ALPHA; LICHENICIDIN BETA; MERSACIDIN; NISIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS LICHENIFORMIS; BACTERIAL GENOME; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; COMPETITIVE INHIBITION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG ISOLATION; DRUG MECHANISM; DRUG POTENTIATION; DRUG STRUCTURE; GENE AMPLIFICATION; GENE CLUSTER; GENE SEQUENCE; GRAM POSITIVE BACTERIUM; HYDROPHOBICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ANTI-BACTERIAL AGENTS; BACILLUS; BACTERIOCINS; DRUG SYNERGISM; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION;

BACILLUS LICHENIFORMIS; POSIBACTERIA;

EID: 77955016145     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100871b     Document Type: Article

References (35)

1. Asaduzzaman, S. M. and Sonomoto, K. (2009) Lantibiotics: diverse activities and unique modes of action J. Biosci. Bioeng. 107, 475-487
2. Navaratna, M. A., Sahl, H. G., and Tagg, J. R. (1998) Two-component anti-Staphylococcus aureus lantibiotic activity produced by Staphylococcus aureus C55 Appl. Environ. Microbiol. 64, 4803-4808
3. Ryan, M. P., Jack, R. W., Josten, M., Sahl, H. G., Jung, G., Ross, R. P., and Hill, C. (1999) Extensive post-translational modification, including serine to D-alanine conversion, in the two-component lantibiotic, lacticin 3147 J. Biol. Chem. 274, 37544-37550
4. Holo, H., Jeknic, Z., Daeschel, M., Stevanovic, S., and Nes, I. V. (2001) Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics Microbiology 147, 643-651 (Pubitemid 32243725)
5. Yonezawa, H. and Kuramitsu, H. K. (2005) Genetic analysis of a unique bacteriocin, Smb, produced by Streptococcus mutants GS5 Antimicrob. Agents Chemother. 49, 541-548
6. Hyink, O., Balakrishnan, M., and Tagg, J. R. (2005) Streptococcus rattus strain BHT produces both a class I two-component lantibiotic and a class II bacteriocin FEMS Microbiol. Lett. 15, 235-241
7. McClerren, A. L., Cooper, L. E., Quan, C., Thomas, P. M., Kelleher, N. L., and van der Donk, W. A. (2006) Discovery and in vitro biosynthesis of haloduracin, a new two-component lantibiotic Proc. Natl. Acad. Sci. U.S.A. 103, 17243-17248
8. Martin, N. I., Sprules, T., Carpenter, M. R., Cotter, P. D., Hill, C., Ross, R. P., and Vederas, J. C. (2004) Structural characterization of lacticin 3147, a two-peptide lantibiotic with synergistic activity Biochemistry 43, 3049-3056
9. Cooper, L. E., McClerren, A. L., Chary, A., and van der Donk, W. A. (2008) Structure-activity relationship studies of the two-component lantibiotic haloduracin Chem. Biol. 15, 1035-1045
10. Begley, M., Cotter, P. D., Hill, C., and Ross, R. P. (2009) Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins Appl. Environ. Microbiol. 75, 5451-5460
11. Dischinger, J., Josten, M., Szekat, C., Sahl, H.-G., and Bierbaum, G. (2009) Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13 PLoS One 26, e6788
12. Sambrook, J. and Russel, D. W. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, New York.
13. Rey, M. W., Ramaiya, P., Nelson, B. A., Brody-Karpin, S. D., Zaretsky, E. J., Tang, M., Lopez de Leon, A., Xiang, H., Gusti, V., and Clausen, I. G. 2004, Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species Genome Biol. 5, R77
14. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319, 209-227
15. Ovchinnikova, T. V., Aleshina, G. M., Balandin, S. V., Krasnosdembskaya, A. D., Markelov, M. L., Frolova, E. I., Leonova, Y. F., Tagaev, A. A., Krasnodembsky, E. G., and Kokryakov, V. N. (2004) Purification and primary structure of two isoforms of arenicin, a novel antimicrobial peptide from marine polychaeta Arenicola marina FEBS Lett. 577, 209-214
16. Ovchinnikova, T. V., Shenkarev, Z. O., Nadezhdin, K. D., Balandin, S. V., Zhmak, M. N., Kudelina, I. A., Finkina, E. I., Kokryakov, V. N., and Arseniev, A. S. (2007) Recombinant expression, synthesis, purification, and solution structure of arenicin Biochem. Biophys. Res. Commun. 360, 156-162
17. Dewan, P. C., Anantharaman, A., Chauhan, V. S., and Sahal, D. (2009) Antimicrobial action of prototypic amphipathic cationic decapeptides and their branched dimers Biochemistry 48, 5642-5657
18. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., III, Skelton, N. J., and Rance, M. (2006) Protein NMR Spectroscopy: Principles and Practice, 2nd ed., Academic Press, New York.
19. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
20. Veith, B., Herzberg, C., Steckel, S., Feeshe, J., Maurer, K. H., Ehrenreich, P., Bäumer, S., Henne, A., Liesegang, H., Merkl, R., Ehrenreich, A., and Gottschalk, G. (2004) The complete genome sequebce of Bacillus licheniformis DSM13, an organism with great industrial potential J. Mol. Microbiol. Biotechnol. 7, 204-211
21. McAuliffe, O., Hill, C., and Ross, R. P. (2000) Each peptide of the two-component lantibiotic lacticin 3147 requires a separate modification enzyme for activity Microbiology 146, 2147-2154
22. Cotter, P. D., O'Connor, P. M., Draper, L. A., Lawton, E. M., Deegan, L. H., Hill, C., and Ross, R. P. (2005) Posttranslational conversion of L-serines to D-alanines is vital for optimal production and activity of the lantibiotic lacticin 3147 Proc. Natl. Acad. Sci. U.S.A. 102, 18584-18589
23. Willey, J. M. and van der Donk, W. A. (2007) Lantibiotics: peptides of diverse structure and function Annu. Rev. Microbiol. 61, 477-501
24. Kaletta, C., Entian, K.-D., Kellner, R., Jung, G., Reis, M., and Sahl, H.-G. (1989) Pep5, a new lantibiotic: structural gene isolation and prepeptide sequence Arch. Microbiol. 152, 16-19
25. Hsu, S. T., Breukink, E., Bierbaum, G., Sahl, H.-G., de Kruijff, B., Kaptein, R., van Nuland, N. A., and Bonvin, A. M. (2003) NMR study of mersacidin and lipid II interaction in dodecylphosphocholine micelles J. Biol. Chem. 278, 13110-13117
26. Hsu, S. T., Breukink, E., Tischenko, E., Lutters, M. A., de Kruijff, B., Kaptein, R., Bonvin, A. M., and van Nuland, N. A. (2004) The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics Nat. Struct. Mol. Biol. 11, 963-967
27. Morgan, S. M., O'Connor, P. M., Cotter, P. D., Ross, R. P., and Hill, C. (2005) Sequential actions of the two component peptides of the lantibiotic lacticin 3147 explain its antimicrobial activity at nanomolar concentrations Antimicrob. Agents Chemother. 49, 2606-2611
28. Oman, T. J. and van der Donk, W. A. (2009) Insights into the mode of action of the two-peptide lantibiotic haloduracin ACS Chem. Biol. 4, 865-874
29. Field, D., Collins, B., Cotter, P. D., Hill, C., and Ross, R. P. (2007) A system for the random mutagenesis of the two-peptide lantibiotic lacticin 3147: analysis of mutants producing reduced antibacterial activities J. Mol. Microbiol. Biotechnol. 13, 226-234
30. Bierbaum, G. and Sahl, H. G. (2009) Lantibiotics: mode of action, biosynthesis and bioengineering Curr. Pharm. Biotechnol. 10, 2-18
31. Brötz, H., Bierbaum, G., Reynolds, P. E., and Sahl, H. G. (1997) The lantibiotic mersacidin inhibits peptidoglycan biosynthesis at the level of transglycosylation Eur. J. Biochem. 246, 193-199
32. Brötz, H., Bierbaum, G., Leopold, K., Reynolds, P. E., and Sahl, H. G. (1998) The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II Antimicrob. Agents Chemother. 42, 154-160
33. Schneider, T. R., Kärcher, J., Pohl, E., Lubini, P., and Sheldrick, G. M. (2000) Ab initio structure determination of the lantibiotic mersacidin Acta Crystallogr., Sect. D 56, 705-713
34. Breukink, E. and de Kruijff, B. (2006) Lipid II as a target for antibiotics Nat. Rev. Drug Discovery 5, 321-332
35. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graphics 14, 51-55