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PMID: 11591669 Published · ppublish English Comparative Study Journal Article

Cloning, sequencing, and characterization of the iturin A operon.

Journal of bacteriology ·Vol. 183 ·No. 21 ·2001-11-00 ·Pages 6265-73

Tsuge K, Akiyama T, Shoda M

Abstract

Bacillus subtilis RB14 is a producer of the antifungal lipopeptide iturin A. Using a transposon, we identified and cloned the iturin A synthetase operon of RB14, and the sequence of this operon was also determined. The iturin A operon spans a region that is more than 38 kb long and is composed of four open reading frames, ituD, ituA, ituB, and ituC. The ituD gene encodes a putative malonyl coenzyme A transacylase, whose disruption results in a specific deficiency in iturin A production. The second gene, ituA, encodes a 449-kDa protein that has three functional modules homologous to fatty acid synthetase, amino acid transferase, and peptide synthetase. The third gene, ituB, and the fourth gene, ituC, encode 609- and 297-kDa peptide synthetases that harbor four and two amino acid modules, respectively. Mycosubtilin, which is produced by B. subtilis ATCC 6633, has almost the same structure as iturin A, but the amino acids at positions 6 and 7 in the mycosubtilin sequence are D-Ser-->L-Asn, while in iturin A these amino acids are inverted (i.e., D-Asn-->L-Ser). Comparison of the amino acid sequences encoded by the iturin A operon and the mycosubtilin operon revealed that ituD, ituA, and ituB have high levels of homology to the counterpart genes fenF (79%), mycA (79%), and mycB (79%), respectively. Although the overall level of homology of the amino acid sequences encoded by ituC and mycC, the counterpart of ituC, is relatively low (64%), which indicates that there is a difference in the amino acid sequences of the two lipopeptides, the levels of homology between the putative serine adenylation domains and between the asparagine adenylation domains in the two synthetases are high (79 and 80%, respectively), implying that there is an intragenic domain change in the synthetases. The fact that the flanking sequence of the iturin A synthetase coding region was highly homologous to the flanking sequence that of xynD of B. subtilis 168 and the fact that the promoter of the iturin A operon which we identified was also conserved in an upstream sequence of xynD imply that horizontal transfer of this operon occurred. When the promoter was replaced by the repU promoter of the plasmid pUB110 replication protein, production of iturin A increased threefold.

MeSH Terms
Amino Acid Sequence Anti-Bacterial Agents/biosynthesis Bacillus subtilis/genetics Base Sequence Cloning, Molecular Lipoproteins/genetics Molecular Sequence Data Mutation Operon Peptides Peptides, Cyclic/genetics,physiology Phenotype Phylogeny Promoter Regions, Genetic Sequence Homology, Nucleic Acid
Chemicals
Anti-Bacterial Agents Lipoproteins Peptides Peptides, Cyclic iturin D mycosubtiline iturin A
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tsuge K
Chemical Resources Laboratory, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8503, Japan.
Akiyama T
Shoda M
References (39)
39 references, click to expand
  1. Complete physical map of the Bacillus subtilis 168 chromosome constructed by a gene-directed mutagenesis method.
    J Mol Biol. 1991 Aug 5;220(3):631-48 PMID: 1908013
  2. Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis.
    Chem Rev. 1997 Nov 10;97(7):2651-2674 PMID: 11851476
  3. Structure of iturine A, a peptidolipid antibiotic from Bacillus subtilis.
    Biochemistry. 1978 Sep 19;17(19):3992-6 PMID: 101232
  4. New genes in the 170 degrees region of the Bacillus subtilis genome encode DNA gyrase subunits, a thioredoxin, a xylanase and an amino acid transporter.
    Microbiology. 1996 Nov;142 ( Pt 11):3097-101 PMID: 8969507
  5. A putative lichenysin A synthetase operon in Bacillus licheniformis: initial characterization.
    Biochim Biophys Acta. 1998 Aug 20;1399(2-3):141-53 PMID: 9765590
  6. The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates.
    J Biol Chem. 1996 Jun 28;271(26):15428-35 PMID: 8663196
  7. Bacterial control of plant diseases.
    J Biosci Bioeng. 2000;89(6):515-21 PMID: 16232790
  8. Functional and transcriptional analyses of a fengycin synthetase gene, fenC, from Bacillus subtilis.
    J Bacteriol. 1999 Aug;181(16):5060-7 PMID: 10438779
  9. Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains.
    Science. 1995 Jul 7;269(5220):69-72 PMID: 7604280
  10. The tyrocidine biosynthesis operon of Bacillus brevis: complete nucleotide sequence and biochemical characterization of functional internal adenylation domains.
    J Bacteriol. 1997 Nov;179(21):6843-50 PMID: 9352938
  11. Engineered biosynthesis of peptide antibiotics.
    Biochem Pharmacol. 1996 Jul 26;52(2):177-86 PMID: 8694841
  12. The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase.
    Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13294-9 PMID: 10557314
  13. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome.
    Nucleic Acids Res. 1989 Jun 12;17(11):4410 PMID: 2500645
  14. Plipastatins: new inhibitors of phospholipase A2, produced by Bacillus cereus BMG302-fF67. I. Taxonomy, production, isolation and preliminary characterization.
    J Antibiot (Tokyo). 1986 Jun;39(6):737-44 PMID: 3089997
  15. Isolation of a gene essential for biosynthesis of the lipopeptide antibiotics plipastatin B1 and surfactin in Bacillus subtilis YB8.
    Arch Microbiol. 1996 Apr;165(4):243-51 PMID: 8639027
  16. Fengycin--a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3.
    J Antibiot (Tokyo). 1986 Jul;39(7):888-901 PMID: 3093430
  17. Sequence completion, identification and definition of the fengycin operon in Bacillus subtilis 168.
    Microbiology. 1997 Nov;143 ( Pt 11):3443-50 PMID: 9387222
  18. Effect of in vitro DNA rearrangement in the NH2-terminal region of the penicillinase gene from Bacillus licheniformis on the mode of expression in Bacillus subtilis.
    J Gen Microbiol. 1985 Jul;131(7):1753-63 PMID: 3930658
  19. Design and application of multimodular peptide synthetases.
    Curr Opin Biotechnol. 1999 Aug;10(4):341-8 PMID: 10449311
  20. Molecular and biochemical characterization of the protein template controlling biosynthesis of the lipopeptide lichenysin.
    J Bacteriol. 1999 Jan;181(1):133-40 PMID: 9864322
  21. The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
    Nature. 1997 Nov 20;390(6657):249-56 PMID: 9384377
  22. Recent trends in the biochemistry of surfactin.
    Appl Microbiol Biotechnol. 1999 May;51(5):553-63 PMID: 10390813
  23. The level of the pUB110 replication initiator protein is autoregulated, which provides an additional control for plasmid copy number.
    Nucleic Acids Res. 1995 Jun 11;23(11):1894-900 PMID: 7596815
  24. Tn10-derived transposons active in Bacillus subtilis.
    J Bacteriol. 1990 Dec;172(12):6736-40 PMID: 2174858
  25. The nucleotide sequence of pUB110: some salient features in relation to replication and its regulation.
    Plasmid. 1986 Mar;15(2):93-103 PMID: 3010356
  26. Purification of a malonyltransferase from Streptomyces coelicolor A3(2) and analysis of its genetic determinant.
    J Bacteriol. 1995 Jul;177(14):3946-52 PMID: 7608065
  27. Cloning, nucleotide sequence, and expression of the Escherichia coli fabD gene, encoding malonyl coenzyme A-acyl carrier protein transacylase.
    J Bacteriol. 1992 May;174(9):2851-7 PMID: 1314802
  28. The genes degQ, pps, and lpa-8 (sfp) are responsible for conversion of Bacillus subtilis 168 to plipastatin production.
    Antimicrob Agents Chemother. 1999 Sep;43(9):2183-92 PMID: 10471562
  29. Targeted alteration of the substrate specificity of peptide synthetases by rational module swapping.
    Mol Gen Genet. 1998 Feb;257(3):308-18 PMID: 9520265
  30. Transposon mutagenesis and cloning of the genes encoding the enzymes of fengycin biosynthesis in Bacillus subtilis.
    Mol Gen Genet. 1995 Jul 28;248(2):121-5 PMID: 7651334
  31. Multifunctional Peptide Synthetases.
    Chem Rev. 1997 Nov 10;97(7):2675-2706 PMID: 11851477
  32. Biocontrol of Rhizoctonia solani Damping-Off of Tomato with Bacillus subtilis RB14.
    Appl Environ Microbiol. 1996 Nov;62(11):4081-5 PMID: 16535440
  33. Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties.
    Toxicology. 1994 Feb 28;87(1-3):151-74 PMID: 8160184
  34. A new enzyme superfamily - the phosphopantetheinyl transferases.
    Chem Biol. 1996 Nov;3(11):923-36 PMID: 8939709
  35. Bacillus subtilis acyl carrier protein is encoded in a cluster of lipid biosynthesis genes.
    J Bacteriol. 1996 Aug;178(16):4794-800 PMID: 8759840
  36. Specific inhibition of iturin biosynthesis by cerulenin.
    Can J Microbiol. 1990 Mar;36(3):164-8 PMID: 2111202
  37. A putative new peptide synthase operon in Bacillus subtilis: partial characterization.
    Microbiology. 1995 Mar;141 ( Pt 3):645-8 PMID: 7711903
  38. Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis.
    Mol Microbiol. 1993 May;8(5):821-31 PMID: 8355609
  39. Malonyl-coenzyme A:acyl carrier protein acyltransferase of Streptomyces glaucescens: a possible link between fatty acid and polyketide biosynthesis.
    Biochemistry. 1995 Jul 25;34(29):9389-402 PMID: 7626609
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2001-11-00
Pages
6265-73
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC100110
Subset
IM
Databases
GENBANK
AB050629
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