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PMID: 19778043 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Enzymatic tailoring of ornithine in the biosynthesis of the Rhizobium cyclic trihydroxamate siderophore vicibactin.

Journal of the American Chemical Society ·Vol. 131 ·No. 42 ·2009-10-28 ·Pages 15317-29

Heemstra JR, Walsh CT, Sattely ES

Abstract

To acquire iron, the N(2)-fixing, symbiotic bacterium Rhizobium sp. produce the cyclic trihydroxamate siderophore vicibactin, containing a 30-membered trilactone scaffold. Herein we report the overproduction and purification of the six proteins VbsACGOLS in the bacterial host Escherichia coli and the reconstitution of the biosynthesis of vicibactin from primary metabolites. The flavoprotein VbsO acts as a pathway-initiating l-ornithine N(5)-hydroxylase, followed by VbsA, which transfers (R)-3-hydroxybutyryl- from the CoA thioester to N(5)-hydroxyornithine to yield N(5)-((R)-3-hydroxybutyryl)-N(5)-hydroxy-l-ornithine. VbsL is a PLP-dependent epimerase acting at C(2) of the 10 atom monomer unit. VbsS, a nonribosomal peptide synthetase free-standing module, then activates N(5)-((R)-3-hydroxybutyryl)-N(5)-hydroxy-d-ornithine as the AMP anhydride on the way to cyclotrimerization to the vicibactin scaffold. The last step, tris-acetylation of the C(2) amino group of desacetyl-d-vicibactin to the mature siderophore vicibactin, is catalyzed distributively by VbsC, using three molecules of acetyl-CoA.

MeSH Terms
Biocatalysis Models, Molecular Molecular Structure Multigene Family Ornithine/chemistry,metabolism Peptides, Cyclic/biosynthesis,chemistry Rhizobium/chemistry,enzymology,genetics
Chemicals
Peptides, Cyclic vicibactin Ornithine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Heemstra John R
Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Walsh Christopher T
Sattely Elizabeth S
References (47)
47 references, click to expand
  1. The vbs genes that direct synthesis of the siderophore vicibactin in Rhizobium leguminosarum: their expression in other genera requires ECF sigma factor RpoI.
    Mol Microbiol. 2002 Jun;44(5):1153-66 PMID: 12028377
  2. Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145.
    J Am Chem Soc. 2004 Dec 22;126(50):16282-3 PMID: 15600304
  3. A new family of ATP-dependent oligomerization-macrocyclization biocatalysts.
    Nat Chem Biol. 2007 Oct;3(10):652-6 PMID: 17704771
  4. Biosynthesis of the iron-molybdenum cofactor of nitrogenase.
    Annu Rev Microbiol. 2008;62:93-111 PMID: 18429691
  5. The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence.
    Infect Immun. 2005 Sep;73(9):5493-503 PMID: 16113265
  6. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases.
    Chem Biol. 1999 Aug;6(8):493-505 PMID: 10421756
  7. Delta-amino group hydroxylation of L-ornithine during coelichelin biosynthesis.
    Org Biomol Chem. 2008 May 21;6(10):1843-8 PMID: 18452021
  8. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria.
    Microbiol Mol Biol Rev. 2002 Jun;66(2):223-49 PMID: 12040125
  9. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains.
    Chem Biol. 2000 Mar;7(3):211-24 PMID: 10712928
  10. Detection, isolation, and characterization of siderophores.
    Methods Enzymol. 1994;235:329-44 PMID: 8057905
  11. Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations.
    Annu Rev Biochem. 2004;73:383-415 PMID: 15189147
  12. A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases.
    Chembiochem. 2005 Apr;6(4):601-11 PMID: 15719346
  13. Kinetics of aminoacyl-tRNA synthetases catalyzed ATP-PPi exchange.
    Methods Enzymol. 1974;29:620-7 PMID: 4368856
  14. MbtH-like protein-mediated cross-talk between non-ribosomal peptide antibiotic and siderophore biosynthetic pathways in Streptomyces coelicolor M145.
    Microbiology (Reading). 2007 May;153(Pt 5):1405-1412 PMID: 17464054
  15. Assembly-line enzymology for polyketide and nonribosomal Peptide antibiotics: logic, machinery, and mechanisms.
    Chem Rev. 2006 Aug;106(8):3468-96 PMID: 16895337
  16. Reconstitution and characterization of the Escherichia coli enterobactin synthetase from EntB, EntE, and EntF.
    Biochemistry. 1998 Feb 24;37(8):2648-59 PMID: 9485415
  17. Siderophore-based iron acquisition and pathogen control.
    Microbiol Mol Biol Rev. 2007 Sep;71(3):413-51 PMID: 17804665
  18. Siderophore and organic acid production in root nodule bacteria.
    Arch Microbiol. 1992;157(3):264-71 PMID: 1387306
  19. Recent advances in siderophore biosynthesis.
    Curr Opin Chem Biol. 2009 Apr;13(2):205-15 PMID: 19369113
  20. Isolation and properties of N epsilon-hydroxylysine:acetyl coenzyme A N epsilon-transacetylase from Escherichia coli pABN11.
    Biochemistry. 1986 May 6;25(9):2485-9 PMID: 3521734
  21. Utilization of microbial iron assimilation processes for the development of new antibiotics and inspiration for the design of new anticancer agents.
    Biometals. 2009 Feb;22(1):61-75 PMID: 19130268
  22. Role of ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding L-ornithine N(5)-oxygenase.
    Infect Immun. 1999 Sep;67(9):4443-55 PMID: 10456885
  23. Mining microbial genomes for new natural products and biosynthetic pathways.
    Microbiology (Reading). 2008 Jun;154(Pt 6):1555-1569 PMID: 18524911
  24. Pyoverdine siderophores: from biogenesis to biosignificance.
    Trends Microbiol. 2007 Jan;15(1):22-30 PMID: 17118662
  25. Ammonia assimilation by rhizobium cultures and bacteroids.
    J Gen Microbiol. 1975 Jan;86(1):39-48 PMID: 234505
  26. Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts.
    J Biotechnol. 2006 Aug 5;124(4):670-89 PMID: 16712999
  27. Isolation, characterization, and properties of fusarinine, a delta-hydroxamic acid derivative of ornithine.
    Biochemistry. 1965 Jul;4(7):1410-7 PMID: 5856641
  28. Peptide siderophores.
    J Pept Sci. 1998 May;4(3):147-81 PMID: 9643626
  29. The siderophore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding l-ornithine N 5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC).
    Mol Microbiol. 2003 Jul;49(2):359-75 PMID: 12828635
  30. The role of PHB metabolism in the symbiosis of rhizobia with legumes.
    Appl Microbiol Biotechnol. 2006 Jul;71(4):377-86 PMID: 16703322
  31. Molecular basis of plant growth promotion and biocontrol by rhizobacteria.
    Curr Opin Plant Biol. 2001 Aug;4(4):343-50 PMID: 11418345
  32. A latent oxazoline electrophile for N-O-C bond formation in pseudomonine biosynthesis.
    J Am Chem Soc. 2008 Sep 17;130(37):12282-4 PMID: 18710233
  33. Yersiniabactin synthetase: a four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis.
    Chem Biol. 2002 Mar;9(3):333-44 PMID: 11927258
  34. Biosynthesis of sideramines in fungi. Fusigen synthetase from extracts of Fusarium cubense.
    FEBS Lett. 1973 Nov 1;36(3):323-5 PMID: 4357812
  35. Structure elucidation and biosynthesis of fuscachelins, peptide siderophores from the moderate thermophile Thermobifida fusca.
    Proc Natl Acad Sci U S A. 2008 Oct 7;105(40):15311-6 PMID: 18832174
  36. Identification of a gene cluster that directs putrebactin biosynthesis in Shewanella species: PubC catalyzes cyclodimerization of N-hydroxy-N-succinylputrescine.
    J Am Chem Soc. 2008 Aug 13;130(32):10458-9 PMID: 18630910
  37. Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection.
    PLoS Pathog. 2007 Sep 28;3(9):1195-207 PMID: 17845073
  38. Construction and biochemical characterization of recombinant cytoplasmic forms of the IucD protein (lysine:N6-hydroxylase) encoded by the pColV-K30 aerobactin gene cluster.
    J Bacteriol. 1993 Feb;175(3):589-96 PMID: 8423134
  39. Expression, purification, and characterization of HMWP2, a 229 kDa, six domain protein subunit of Yersiniabactin synthetase.
    Biochemistry. 2000 Apr 25;39(16):4729-39 PMID: 10769129
  40. Hydroxamic acids in nature.
    Science. 1967 Jun 16;156(3781):1443-7 PMID: 4304945
  41. Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis.
    Chem Rev. 1997 Nov 10;97(7):2651-2674 PMID: 11851476
  42. Epimerization of an L-cysteinyl to a D-cysteinyl residue during thiazoline ring formation in siderophore chain elongation by pyochelin synthetase from Pseudomonas aeruginosa.
    Biochemistry. 2003 Sep 9;42(35):10514-27 PMID: 12950179
  43. Siderophores in fungal physiology and virulence.
    Annu Rev Phytopathol. 2008;46:149-87 PMID: 18680426
  44. A genetic locus required for iron acquisition in Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2006 Feb 14;103(7):2069-74 PMID: 16461464
  45. Purification and properties of ornithine racemase from Clostridium sticklandii.
    J Bacteriol. 2000 Apr;182(7):2052-4 PMID: 10715017
  46. Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12.
    J Bacteriol. 1986 Feb;165(2):570-8 PMID: 2935523
  47. The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons.
    Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3834-9 PMID: 16505379
Article Info
Journal
Journal of the American Chemical Society
Abbr.
J Am Chem Soc
ISSN
1520-5126
Published
2009-10-28
Pages
15317-29
Language
English
Region
United States
NLM ID
7503056
PMCID
PMC2783850
Subset
IM
Grants
NIGMS NIH HHS · F32 GM083464 · United States
NIAID NIH HHS · R01 AI042738 · United States
NIGMS NIH HHS · F32 GM083464-01 · United States
NIAID NIH HHS · R01 AI042738-09 · United States
NIGMS NIH HHS · F32GM083464 · United States
NIAID NIH HHS · AI042738 · United States
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