Isolation and structural identification of the trihydroxamate siderophore vicibactin and its degradative products from Rhizobium leguminosarum ATCC 14479 bv. trifolii

BioMetals

Volumn 26, Issue 2, 2013, Pages 271-283

  Wright, William ^a   Little, James ^b   Liu, Fang ^b   Chakraborty, Ranjan ^a  

^a EAST TENNESSEE STATE UNIVERSITY   (United States)

^b EASTMAN CHEMICAL COMPANY   (United States)

Author keywords

ATCC 14479; Iron; Rhizobium leguminosarum; Siderophore; Trifolii; Vicibactin

Indexed keywords

DEUTERIUM; SIDEROPHORE; UNCLASSIFIED DRUG; VICIBACTIN;

ARTICLE; BACTERIAL STRAIN; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; CULTURE MEDIUM; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PLANT MICROORGANISM INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; RED CLOVER; RHIZOBIUM LEGUMINOSARUM; STRUCTURE ANALYSIS; THIN LAYER CHROMATOGRAPHY;

IRON; PEPTIDES, CYCLIC; PLANT ROOTS; RHIZOBIUM LEGUMINOSARUM; SIDEROPHORES; SOIL MICROBIOLOGY; SYMBIOSIS; TRIFOLIUM;

BACTERIA (MICROORGANISMS); RHIZOBIUM LEGUMINOSARUM; TRIFOLIUM; TRIFOLIUM PRATENSE;

EID: 84877873240     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-013-9609-3     Document Type: Article

References (54)

1. Abergel RJ, Zawadzka AM, Hoette TM, Raymond KN (2009) Enzymatic Hydrolysis of trilactone siderophores: where chiral recognition occurs in enterobactin and bacillibactin iron transport. J Am Chem Soc 131:12682-12692
2. Albrecht-Gary AM, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. Met Ions Biol Syst 35:239-327
3. Arnow LE (1937) Colorimetric determination of the components of 3,4-dihydroxyphenylalaninetyrosine mixtures. J Biol Chem 118:531-537
4. Atkin CL, Neilands JB, Phaff HJ (1970) Rhodotorulic acid from species of Leucosporidium, Rhodosporidium, Rhodotorula, Sporidiobolus, and Sporobolomyces, and a new alanine-containing ferrichrome from Cryptococcus melibiosum. J Bacteriol 103:722-733
5. Bagg A, Neilands JB (1987) Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev 51:509-518
6. Battistoni F, Platero R, Duran R, Cervenansky C, Battistoni J, Arias A, Fabiano E (2002) Identification of an iron-regulated, hemin-binding outer membrane protein in Sinorhizobium meliloti. Appl Environ Microbiol 68:5877-5881
7. Braun V, Hantke K, Koster W (1998) Bacterial iron transport: mechanisms, genetics, and regulation. Metal Ions Biol Syst 35:67-145
8. Bristow AW, Nichols WF, Webb KS, Conway B (2002) Evaluation of protocols for reproducible electrospray in-source collisionally induced dissociation on various liquid chromatography/mass spectrometry instruments and the development of spectral libraries. Rapid Commun Mass Spectrom 16:2374-2386
9. Carson KC, Meyer JM, Dilworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11-21
10. Carter RA, Worsley PS, Sawers G, Challis GL, Dilworth MJ, Carson KC et al (2002) 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 44:1153-1166
11. Chao TC, Becker A, Buhrmester J, Puhler A, Weidner S (2004) The Sinorhizobium meliloti fur gene regulates, with dependence on Mn(II), transcription of the sitABCD operon, encoding a metal-type transporter. J Bacteriol 186:3609-3620
12. Chernushevich IV, Loboda AV, Thomson BA (2001) An introduction to quadrupole-time-of-flight mass spectrometry. J Mass Spectrom 36:849-865
13. Crosa JH (1989) Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53:517-530
14. Crosa JH (1997) Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol Mol Biol Rev 61:319-336
15. De Lorenzo V, Herrero M, Giovannini F, Neilands JB (1988) Fur (ferric uptake regulation) protein and CAP (catabolite-activator protein) modulate transcription of fur gene in Escherichia coli. Eur J Biochem 173:537-546
16. Dilworth MJ, Carson KC, Giles RGF, Byrne LT, Glenn AR (1998) Rhizobium leguminosarum bv. viciae produces a novel cyclic trihydroxamate siderophore, vicibactin. Microbiology 144:781-791
17. Emery T, Neilands JB (1961) Structure of the ferrichrome compounds. J Am Chem Soc 83:1626-1628
18. Eng-Wilmot DL, Rahman A, Mendenhall JV, Grayson SL, Van der Helm D (1984) Molecular structure of ferric neurosporin, a minor siderophore-like compound containing N.delta.-hydroxy-d-ornithine. J Am Chem Soc 106:1285-1290
19. Frost GE, Rosenberg H (1973) The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta 330:90-101
20. Gibson F, Magrath DI (1969) The isolation and characterization of a hydroxamic acid (aerobactin) formed by Aerobacter aerogenes 62-I. Biochim Biophys Acta 192:175-184
21. Harrington JM, Crumbliss AL (2009) The redox hypothesis in siderophore-mediated iron uptake. Biometals 22:679-699
22. Heemstra JR Jr, Walsh CT, Sattely ES (2009) Enzymatic tailoring of ornithine in the biosynthesis of the Rhizobium cyclic trihydroxamate siderophore vicibactin. J Am Chem Soc 131:15317-15329
23. Hemling M, Conboy J, Bean M, Mentzer M, Carr S (1994) Gas phase hydrogen/deuterium exchange in electrospray ionization mass spectrometry as a practical tool for structure elucidation. J Am Soc Mass Spectrom 5:434-442
24. Jadhav RS, Desai AJ (1996) Effect of nutritional and environmental conditions on siderophore production by Rhizobium GN1 (peanut isolate). Indian J Exp Biol 34:436-439
25. Jalal MAF, van der Helm D (1991) Isolation and spectroscopic identification of fungal siderophores. In: Winkelmann G (ed) CRC handbook of microbial iron chelates. CRC Press, Boca Raton, pp 235-269
26. Johnston AW (2004) Mechanisms and regulation of iron uptake in the Rhizobia. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 469-488
27. Lam W, Ramanathan R (2002) In electrospray ionization source hydrogen/deuterium exchange LC-MS and LC-MS/MS for characterization of metabolites. J Am Soc Mass Spectrom 13:345-353
28. Lankford CE, Walker JR, Reeves JB, Nabbut NH, Byers BR, Jones RJ (1966) Inoculum-dependent division lag of Bacillus cultures and its relation to an endogenous factor(s) ("schizokinen"). J Bacteriol 91:1070-1079
29. LeVier K, Guerinot ML (1996) The Bradyrhizobium japonicum fegA gene encodes an iron-regulated outer membrane protein with similarity to hydroxamate-type siderophore receptors. J Bacteriol 178:7265-7275
30. Little JL, Cleven CD, Brown SD (2011) Identification of "known unknowns" utilizing accurate mass data and chemical abstracts service databases. J Am Soc Mass Spectrom 22:348-359
31. Lynch D, O'Brien J, Welch T, Clarke P, Cuiv PO, Crosa JH, O'Connell M (2001) Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J Bacteriol 183:2576-2585
32. Manhart JR, Wong PP (1979) Nitrate reductase activities of Rhizobia and the correlation between nitrate reduction and nitrogen fixation. Can J Microbiol 25:1169-1174
33. Matzanke B, Anemüller S, Schünemann V, Trautwein AX, Hanke K (2004) FhuF, Part of a siderophore-reductase system. Biochemistry 43:1386-1392
34. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413-451
35. Mullis KB, Pollack JR, Neilands JB (1971) Structure of schizokinen, an iron-transport compound from Bacillus megaterium. Biochemistry 10:4894-4898
36. Noya F, Arias A, Fabiano E (1997) Heme compounds as iron sources for nonpathogenic Rhizobium bacteria. J Bacteriol 179:3076-3078
37. O'Brien IG, Gibson F (1970) The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim Biophys Acta 215:393-402
38. Patel HN, Chakraborty RN, Desai SB (1988) Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol Lett 56:131-134
39. Persmark M, Pittman P, Buyer JS, Schwyn B, Gill PR, Neilands JB (1993) Isolation and structure of rhizobactin 1021, a siderophore from the alfalfa symbiont Rhizobium meliloti 1021. J Am Chem Soc 115:3950-3956
40. Ramirez-Bahena MH, Garcia-Fraile P, Peix A, Valverde A, Rivas R, Igual JM et al (2008) Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (= NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol 58:2484-2490
41. Raymond KN, Dertz EA (2004) Biochemical and physical properties of siderophores. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 3-17
42. Rohrbach MR, Braun V, Köster W (1995) Ferrichrome transport in Escherichia coli K-12: altered substrate specificity of mutated periplasmic FhuD and interaction of FhuD with the integral membrane protein FhuB. J Bacteriol 177:7186-7193
43. Rudolph G, Hennecke H, Fischer HM (2006) Beyond the fur paradigm: iron-controlled gene expression in rhizobia. FEMS Microbiol Rev 30:631-648
44. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47-56
45. Smith MJ, Shoolery JN, Schwyn B, Holden I, Neilands JB (1985) Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. J Am Chem Soc 107:1739-1743
46. Stevens JB, Carter RA, Hussain H, Carson KC, Dilworth MJ, Johnston AW (1999) The fhu genes of Rhizobium leguminosarum, specifying siderophore uptake proteins: fhuDCB are adjacent to a pseudogene version of fhuA. Microbiology 145(Pt 3):593-601
47. Storey EP (2005) Characterization of a dihydroxamate-type siderophore produced by Rhizobium leguminosarum IARI 917: is it schizokinen? MS Thesis. East Tennessee State University, Johnson City
48. Storey EP, Boghozian R, Little JL, Lowman DW, Chakraborty R (2006) Characterization of 'schizokinen'; a dihydroxamate-type siderophore produced by Rhizobium leguminosarum IARI 917. Biometals 19:637-649
49. Todd JD, Wexler M, Sawers G, Yeoman KH, Poole PS, Johnston AW (2002) RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148:4059-4071
50. Todd JD, Sawers G, Johnston AW (2005) Proteomic analysis reveals the wide-ranging effects of the novel, iron-responsive regulator RirA in Rhizobium leguminosarum bv. viciae. Mol Genet Genomics 273:197-206
51. Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AW (2001) The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol 41:801-816
52. Wexler M, Todd JD, Kolade O, Bellini D, Hemmings AM, Sawers G, Johnston AW (2003) Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149:1357-1365
53. Wright WH (2010) Isolation and identification of the siderophore "vicibactin" produced by Rhizobium leguminosarum ATCC 14479. MS Thesis. East Tennessee State University, Johnson City
54. Yeoman KH, Wisniewski-Dye F, Timony C, Stevens JB, deLuca NG, Downie JA, Johnston AW (2000) Analysis of the Rhizobium leguminosarum siderophore-uptake gene fhuA: differential expression in free-living bacteria and nitrogen-fixing bacteroids and distribution of an fhuA pseudogene in different strains. Microbiology 146(Pt 4):829-837