Role for ferredoxin: NAD(P)H oxidoreductase (FprA) in sulfate assimilation and siderophore biosynthesis in pseudomonads

Journal of Bacteriology

Volumn 195, Issue 17, 2013, Pages 3876-3887

  Lewis, Thomas A ^a   Glassing, Angela ^a   Harper, Justin ^a   Franklin, Michael J ^b  

^a MONTANA STATE UNIVERSITY BILLINGS   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; PYRIDINE 2,6 (THIOCARBOXYLATE); SIDEROPHORE; SULFATE; SULFITE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; AUXOTROPHIC MUTANT; BACTERIAL GENE; BACTERIAL STRAIN; BIOSYNTHESIS; CHLOROPLAST; CONTROLLED STUDY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PUTIDA; REDUCTION; TRANSCRIPTION INITIATION; TRANSPOSON; WILD TYPE;

DNA TRANSPOSABLE ELEMENTS; FERREDOXINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; NADH, NADPH OXIDOREDUCTASES; PSEUDOMONAS PUTIDA; PYRIDINES; SIDEROPHORES; SULFATES;

EID: 84883502997     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00528-13     Document Type: Article

References (61)

1. Lee C-H, Lewis TA, Paszczynski A, Crawford RL. 1999. Identification of an extracellular catalyst of carbon tetrachloride dehalogenation from Pseudomonas stutzeri strain KC as pyridine-2,6-bis(thiocarboxylate). Biochem. Biophys. Res. Commun. 261:562-566. (Erratum, 265:770.)
2. Ockels W, Römer Budzikiewicz AH. 1978. An Fe(III) complex of pyridine- 2,6-di-(monothiocarboxylic acid): a novel bacterial metabolic product. Tetrahedron Lett. 36:3341-342.
3. Cortese M, Paszczynski A, Lewis TA, Sebat J, Crawford RL. 2002. Metal chelating properties of pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities of the formed complexes. Biometals 15:103-120.
4. Leach L, Lewis TA. 2007. The role of the siderophore pyridine-2,6-bis (thiocarboxylic acid) (PDTC) in zinc utilization by Pseudomonas putida DSM 3601. Biometals 20:717-726.
5. Lewis TA, Paszczynski A, Gordon-Wylie S, Jeedigunta S, Lee C-H, Crawford RL. 2001. Carbon tetrachloride dechlorination by the bacterial transition metal chelator pyridine-2,6-bis(thiocarboxylic acid). Environ. Sci. Technol. 35:552-559.
6. Stolworthy JC, Paszczynski A, Korus RA, Crawford RL. 2001. Metal binding by pyridine-2,6-bis(monothiocarboxylic acid), a biochelator produced by Pseudomonas stutzeri and Pseudomonas putida. Biodegradation 12:411-418.
7. Criddle CS, DeWitt JT, Grbic-Galic D, McCarty PL. 1990. Transformation of carbon tetrachloride by Pseudomonas sp. strain KC under denitrification conditions. Appl. Environ. Microbiol. 56:3240-3246.
8. Sepulveda-Torres LC, Huang A, Kim H, Criddle CS. 2002. Analysis of regulatory elements and genes required for carbon tetrachloride degradation in Pseudomonas stutzeri strain KC. J. Mol. Microbiol. Biotechnol. 4:151-161.
9. Leach L, Lewis TA. 2006. Identification and characterization of Pseudomonas membrane transporters necessary for utilization of the siderophore pyridine-2,6-bis(thiocarboxylic acid) (PDTC). Microbiology 152:3157-3166.
10. Morales SE, Lewis TA. 2006. Transcriptional regulation of the pdt gene cluster of Pseudomonas stutzeri KC involves an AraC/XylS family transcriptional activator (PdtC) and the cognate siderophore pyridine-2,6-bis(thiocarboxylic acid) (PDTC). Appl. Environ. Microbiol. 72:6994-7002.
11. Crosa JH, Walsh CT. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol. Mol. Biol. Rev. 66:223-249.
12. Cornelis P, Matthijs S. 2002. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ. Microbiol. 4:787-798.
13. Stintzi A, Evans K, Meyer J-M, Poole K. 1998. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol. Lett. 166:341-345.
14. Juhas M, Wiehlmann L, Huber B, Jordan D, Lauber J, Salunkhe P, Limpert AS, von Götz F, Steinmetz I, Eberl L, Tümmler B. 2004. Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831-841.
15. Lewenza S, Sokol P. 2001. Regulation of ornibactin biosynthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J. Bacteriol. 183:2212-2218.
16. Farmer KL, Thomas MS. 2004. Isolation and characterization of Burkholderia cenocepacia mutants deficient in pyochelin production: pyochelin biosynthesis is sensitive to sulfur availability. J. Bacteriol. 186:270-277.
17. Matthijs S, Tehrani KA, Laus G, Jackson RW, Cooper RM, Cornelis P. 2007. Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-pythium activity. Environ. Microbiol. 9:425-434.
18. Lewis TA, Cortese M, Sebat J, Green T, Lee C-H, Crawford RL. 2000. A Pseudomonas stutzeri gene cluster encoding the biosynthesis of the CCl4-dechlorination agent pyridine-2,6-bis(thiocarboxylic acid). Environ. Microbiol. 2:407-416.
19. Begley TP, Xi J, Kinsland C, Taylor SM, McLafferty FW. 1999. The enzymology of sulfur activation during thiamin and biotin biosynthesis. Curr. Opin. Chem. Biol. 3:623-629.
20. Leimkühler S, Rajagopalan KV. 2001. A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J. Biol. Chem. 276:22024-22031.
21. Taylor SM, Kelleher NL, Kinsland C, Chiu H-J, Costello CA, Backstrom AD, McLafferty FW, Begley TP. 1998. Thiamin biosynthesis in Escherichia coli: identification of ThiS thiocarboxylate as the immediate sulfur donor in the thiazole formation. J. Biol. Chem. 273:16555-16560.
22. Hildebrand U, Taraz K, Budzikiewicz H. 1986. 6-(Hydroxythio)carbonylpyridine- 2-carboxylic acid and pyridine-2-carboxylic-6-monothiocarboxylic acid as intermediates in the biosynthesis of pyridine-2,6-di(monothiocarboxylic acid) from pyridine-2,6-dicarboxylic acid. Z. Naturforsch. 41c:691-694.
23. Budzikiewicz H. 2003. Heteroaromatic monothiocarboxylic acids from Pseudomonas spp. Biodegradation 14:65-72.
24. Lewis TA, Leach L, Morales SE, Austin PR, Hartwell HJ, Kaplan B, Forker C, Meyer J-M. 2004. Physiological and molecular genetic evaluation of the dechlorination agent, pyridine-2,6-bis(monothiocarboxylic acid) (PDTC) as a secondary siderophore of Pseudomonas. Environ. Microbiol. 6:159-169.
25. Maniatis T, Sambrook J, Fritsch EF. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Kredich NM. 1987. Biosynthesis of cysteine, p 419-428. In Neidhardt NC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, DC.
27. Nelson KE, Weinei C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VAP, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen J, Timmis K, Düsterhöft A, Tümmler B, Fraser CM. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4:799-808.
28. Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
29. DeLorenzo V, Herrero M, Jakubzik U, Timmis K. 1990. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J. Bacteriol. 172:6568-6572.
30. O'Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R. 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310:91-109.
31. Bailey J, Manoil CJ. 2002. Genome-wide internal tagging of bacterial exported proteins. Nat. Biotechnol. 20:839-842.
32. Choi K-H, Schweizer HP. 2006. Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat. Protoc. 1:153-161.
33. Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL. 1996. Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35:1-13.
34. Quadroni M, James P, Dainese-Hatt P, Kertesz MA. 1999. Proteome mapping, mass spectrometric sequencing and reverse transcription-PCR for characterization of the sulfate starvation-induced response in Pseudomonas aeruginosa PAO1. Eur. J. Biochem. 266:986-996.
35. Endoh T, Habe H, Yoshida T, Nojiri H, Omori T. 2003. A CysBregulated and sigma 54-dependent regulator, SfnR, is essential for dimethyl sulfone metabolism of Pseudomonas putida strain DS1. Microbiol. 149:991-1000.
36. Hummerjohann J, Kuttel E, Quadroni M, Ragaller J, Leisinger T, Kertesz MA. 1998. Regulation of the sulfate starvation response in Pseudomonas aeruginosa: role of cysteine biosynthetic intermediates. Microbiol. 144:1375-1386.
37. Matthijs S. 2002. The in-vitro antagonism of Pseudomonas fluorescens ATCC17400 against Pythium debaryanum: the role of trehalose in the interaction between both microorganims, and the identificaiton of the siderophores pyoverdine and quinolobactin as the antagonistic compounds. Ph.D. thesis. Vrije Universiteit Brussels, Brussels, Belgium.
38. + reductase) gene in Pseudomonas putida KT2440. Biochem. Biophys. Res. Commun. 339:1246-1254.
39. Yeom S, Yeom J, Park W. 2010. Molecular characterization of FinR, a novel redox-sensing transcriptional regulator in Pseudomonas putida KT2440. Microbiology 156:1487-1496.
40. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, Brinkman FS. 2011. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39:596-600.
41. Taiz L, Zeiger E. 2010. Plant physiology. Sinauer Associates, Sunderland, MA.
42. Sepulveda-Torres LdC, Rajendran N, Dybas MJ, Criddle CS. 1999. Generation and initial characterization of Pseudomonas stutzeri KC mutants with impaired ability to degrade carbon tetrachloride. Arch. Microbiol. 171:424-429.
43. Tralau T, Vuillemier S, Thibault C, Campbell BJ, Hart CA, Kertesz MA. 2007. Transcriptomic analysis of the sulfate starvation response of Pseudomonas aeruginosa. J. Bacteriol. 189:6743-6750.
44. Michel L, Gonzales N, Jagdeep Nguyen-Ngoc ST, Reimmann C. 2005. PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol. Microbiol. 58:495-509.
45. Neumann S, Wynen A, Truper HG, Dahl C. 2000. Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway. Mol. Biol. Rep. 27:27-33.
46. Rückert C, Koch DJ, Rey DA, Albersmeier A, Mormann S, Pühler A, Kalinowski J. 2005. Functional genomics and expression analysis of the Corynebacterium glutamicum fpr2-cysIXHDNYZ gene cluster involved in assimilatory sulphate reduction. BMC Genomics 6:1-18. doi:10.1186/1471-2164-6-121.
47. Bick JA, Dennis JJ, Zylstra GJ, Nowack J, Leustek T. 2000. Identification of a new class of 5=-adenylylsulfate (APS) reductases from sulfateassimilating bacteria. J. Bacteriol. 182:135-142.
48. + reductase and not ferredoxin Is the redox partner of heme oxygenase under iron-starvation conditions. Biochem 46:12198-12211.
49. Marchler-Bauer A, Lu S, Anderson JB, Chisaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Jurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang N, Zheng C, Bryant SH. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39:225-229.
50. + reductases in Pseudomonas putida. J. Biochem. 145:481-491.
51. Yeom J, Jeon CO, Madsen EL, Park W. 2009. Ferredoxin-NADP reductase from Pseudomonas putida functions as a ferric reductase. J. Bacteriol. 191:1472-1479.
52. Ohtsu I, Wiriyathanawudhiwong N, Nakatani T, Takagi H. 2010. The L-cysteine/L-cystine shuttle system provides reducing equivalents to the periplasm in Escherichia coli. J. Biol. Chem. 285:17479-17487.
53. Park S, Imlay J. 2003. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 185:1942-1950.
54. Williams PA, Murray K. 1974. Metabolism of benzoate and the methylbenzoates by Pseudomonas putida (arvilla) mt-2: evidence for the existence of a TOL plasmid. J. Bacteriol. 120:416-423.
55. Jacobs MA, Alwood A, Thaipisuttikul I, spencer, D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenther D, Bovee D, Olson MV, Manoil CJ. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 100:14339-14344.
56. Schweizer HP. 1993. Small broad-host-range gentamicin resistance gene cassettes for site-specific insertion and deletion mutagenesis. Biotechniques 15:831-833.
57. Blatny JM, Brautaset T, Winther-Larsen HC, Haugan K, Valla S. 1997. Construction and use of a versatile set of broad-host-range cloning and expression vectors based on the RK2 replicon. Appl. Environ. Microbiol. 63:370-379.
58. Miller V, Mekalanos J. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
59. Newman JR, Fuqua C. 1999. Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli ara BAD promoter and the araC regulator. Gene 227:197-203.
60. Hoang TT, Karkhoff-Schweizer R, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
61. Franklin MF, Chitnis CE, Gacesa P, Sonesson A, White DC, Ohman DE. 1994. Pseudomonas aeruginosa AlgG is a polymer level alginate C5- mannuronan epimerase. J. Bacteriol. 176:1821-1830.