Gene PA2449 is essential for glycine metabolism and pyocyanin biosynthesis in Pseudomonas aeruginosa PAO1

Journal of Bacteriology

Volumn 195, Issue 9, 2013, Pages 2087-2100

  Lundgren, Benjamin R ^a   Thornton, William ^a   Dornan, Mark H ^b   Villegas Peñaranda, Luis Roberto ^b   Boddy, Christopher N ^b   Nomura, Christopher T ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCINE; GLYCINE HYDROXYMETHYLTRANSFERASE; PA2449 PROTEIN; PHENAZINE; PYOCYANINE; SERINE DEHYDRATASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BIOLOGICAL CONTROL AGENT; CARBON SOURCE; CONTROLLED STUDY; GENE INACTIVATION; GENETIC TRANSCRIPTION; INTRACELLULAR SIGNALING; METABOLITE; MICROARRAY ANALYSIS; OPEN READING FRAME; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; GLYCINE; PSEUDOMONAS AERUGINOSA; PYOCYANINE; TRANSCRIPTION FACTORS;

PSEUDOMONAS AERUGINOSA;

EID: 84876197380     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02205-12     Document Type: Article

References (71)

1. Laursen JB, Nielsen J. 2004. Phenazine natural products: biosynthesis, synthetic analogues, and biological activity. Chem. Rev. 104:1663-1686.
2. Price-Whelan A, Dietrich LE, Newman DK. 2006. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2:71-78.
3. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK. 2011. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J. Bacteriol. 193:3606 -3617.
4. Cox CD. 1986. Role of pyocyanin in the acquisition of iron from transferrin. Infect. Immun. 52:263-270.
5. Price-Whelan A, Dietrich LE, Newman DK. 2007. Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J. Bacteriol. 189:6372- 6381.
6. Wang Y, Kern SE, Newman DK. 2010. Endogenous phenazine antibiot-ics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J. Bacteriol. 192:365-369.
7. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61: 1308-1321.
8. D'Aes J, Hua GK, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, Dietrich LE, Thomashow LS, Mavrodi DV, Hofte M. 2011. Biological control of Rhizoctonia root rot on bean by phenazine- and cyclic lipopeptide- producing Pseudomonas CMR12a. Phytopathology 101:996 -1004.
9. Mavrodi DV, Parejko JA, Mavrodi OV, Kwak YS, Weller DM, Blankenfeldt W, Thomashow LS. Recent insights into the diversity, frequency and ecological roles of phenazines in fluorescent Pseudomonas spp. Environ. Microbiol., in press.
10. Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309 -348.
11. Denning GM, Iyer SS, Reszka KJ, O'Malley Y, Rasmussen GT, Britigan BE. 2003. Phenazine-1-carboxylic acid, a secondary metabolite of Pseudomonas aeruginosa, alters expression of immunomodulatory proteins by human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L584 -L592.
12. Lau GW, Hassett DJ, Ran H, Kong F. 2004. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10:599-606.
13. Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D. 2004. Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect. Immun. 72:4275- 4278.
14. Wilson R, Pitt T, Taylor G, Watson D, MacDermot J, Sykes D, Roberts D, Cole P. 1987. Pyocyanin and 1-hydroxyphenazine produced by Pseudomonas aeruginosa inhibit the beating of human respiratory cilia in vitro. J. Clin. Invest. 79:221-229.
15. Wilson R, Sykes DA, Watson D, Rutman A, Taylor GW, Cole PJ. 1988. Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect. Immun. 56:2515-2517.
16. Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS. 2001. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J. Bacteriol. 183:6454-6465.
17. Mentel M, Ahuja EG, Mavrodi DV, Breinbauer R, Thomashow LS, Blankenfeldt W. 2009. Of two make one: the biosynthesis of phenazines. Chembiochem 10:2295-2304.
18. Mavrodi DV, Ksenzenko VN, Bonsall RF, Cook RJ, Boronin AM, Thomashow LS. 1998. A seven-gene locus for synthesis of phenazine-1- carboxylic acid by Pseudomonas fluorescens 2-79. J. Bacteriol. 180:2541- 2548.
19. Whiteley M, Lee KM, Greenberg EP. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 96:13904 -13909.
20. Chugani SA, Whiteley M, Lee KM, D'Argenio D, Manoil C, Greenberg EP. 2001. QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 98: 2752-2757.
21. Schuster M, Greenberg EP. 2006. A network of networks: quorumsensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:73- 81.
22. Pearson JP, Passador L, Iglewski BH, Greenberg EP. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 92:1490 -1494.
23. Pearson JP, Gray KM, Passador L, Tucker KD, Eberhard A, Iglewski BH, Greenberg EP. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. U. S. A. 91:197-201.
24. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH. 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 96:11229 -11234.
25. Bains M, Fernandez L, Hancock RE. 2012. Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78:6762- 6768.
26. Long J, Zaborina O, Holbrook C, Zaborin A, Alverdy J. 2008. Depletion of intestinal phosphate after operative injury activates the virulence of Pseudomonas aeruginosa causing lethal gut-derived sepsis. Surgery 144: 189-197.
27. Frank LH, Demoss RD. 1959. On the biosynthesis of pyocyanine. J. Bacteriol. 77:776 -782.
28. Oglesby AG, Farrow JM, III, Lee JH, Tomaras AP, Greenberg EP, Pesci EC, Vasil ML. 2008. The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J. Biol. Chem. 283:15558 -15567.
29. Essar DW, Eberly L, Hadero A, Crawford IP. 1990. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172:884 -900.
30. Macdonald JC. 1963. Biosynthesis of pyocyanine. Can. J. Microbiol. 9:809-819.
31. Heurlier K, Denervaud V, Haenni M, Guy L, Krishnapillai V, Haas D. 2005. Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J. Bacteriol. 187:4875- 4883.
32. Miller JH. 1972. Experiments in molecular genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 100:14339 -14344.
34. Choi KH, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
35. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR. 2006. Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 1:3111-3120.
36. Zhang X, Bremer H. 1995. Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J. Biol. Chem. 270:11181-11189.
37. Trutko SM, Garagulya AD, Kiprianova EA, Akimenko VK. 1989. The physiological role of phenazine pigments synthesized by the bacteria Pseudomonas aureofaciens. Biochemistry (Mosc) 54:1092-1098.
38. Henderson JW, Ricker RD, Bidlingmeyer BA, Woodward C. 2000. Rapid, accurate, sensitive, and reproducible HPLC analysis of amino acids. AAA technical note P5 publication no. 5980-1193. Agilent Technologies, Santa Clara, CA.
39. MacEachran DP, Ye S, Bomberger JM, Hogan DA, Swiatecka-Urban A, Stanton BA, O'Toole GA. 2007. The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 75:3902-3912.
40. Morett E, Segovia L. 1993. The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J. Bacteriol. 175:6067- 6074.
41. Song J, Jensen RA. 1996. PhhR, a divergently transcribed activator of the phenylalanine hydroxylase gene cluster of Pseudomonas aeruginosa. Mol. Microbiol. 22:497-507.
42. Palmer GC, Palmer KL, Jorth PA, Whiteley M. 2010. Characterization of the Pseudomonas aeruginosa transcriptional response to phenylalanine and tyrosine. J. Bacteriol. 192:2722-2728.
43. Palmer KL, Aye LM, Whiteley M. 2007. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J. Bacteriol. 189:8079-8087.
44. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
45. Cataldi TR, Bianco G, Abate S. 2009. Accurate mass analysis of N-acylhomoserine- lactones and cognate lactone-opened compounds in bacterial isolates of Pseudomonas aeruginosa PAO1 by LC-ESI-LTQ-FTICRMS. J. Mass Spectrom. 44:182-192.
46. McKnight SL, Iglewski BH, Pesci EC. 2000. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 182:2702-2708.
47. Mashburn LM, Jett AM, Akins DR, Whiteley M. 2005. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187:554 -566.
48. Deziel E, Lepine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG. 2004. Analysis of Pseudomonas aeruginosa 4-hydroxy-2- alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc. Natl. Acad. Sci. U. S. A. 101:1339 -1344.
49. Farrow JM, Pesci EC. 2007. Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal. J. Bacteriol. 189:3425- 3433.
50. Gray VL, O'Reilly M, Muller CT, Watkins ID, Lloyd D. 2006. Low tyrosine content of growth media yields aflagellate Salmonella enterica serovar Typhimurium. Microbiology 152:23-28.
51. Kikuchi G, Motokawa Y, Yoshida T, Hiraga K. 2008. Glycine cleavage system: reaction mechanism, physiological significance, and hyperglycinemia. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 84:246 -263.
52. Castric PA. 1977. Glycine metabolism by Pseudomonas aeruginosa: hydrogen cyanide biosynthesis. J. Bacteriol. 130:826-831.
53. Pessi G, Haas D. 2000. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum- sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182:6940-6949.
54. Pessi G, Haas D. 2001. Dual control of hydrogen cyanide biosynthesis by the global activator GacA in Pseudomonas aeruginosa PAO1. FEMS Microbiol. Lett. 200:73-78.
55. Steele MI, Lorenz D, Hatter K, Park A, Sokatch JR. 1992. Characterization of the mmsAB operon of Pseudomonas aeruginosa PAO encoding methylmalonate-semialdehyde dehydrogenase and 3-hydroxyisobutyrate dehydrogenase. J. Biol. Chem. 267:13585-13592.
56. Köhler T, van Delden C, Curty LK, Hamzehpour MM, Pechere JC. 2001. Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. J. Bacteriol. 183:5213- 5222.
57. Olivares J, Alvarez-Ortega C, Linares JF, Rojo F, Köhler T, Martinez JL. 2012. Overproduction of the multidrug efflux pump MexEF-OprN does not impair Pseudomonas aeruginosa fitness in competition tests, but produces specific changes in bacterial regulatory networks. Environ. Microbiol. 14:1968 -1981.
58. Lamarche MG, Deziel E. 2011. MexEF-OprN efflux pump exports the Pseudomonas quinolone signal (PQS) precursor HHQ (4-hydroxy-2- heptylquinoline). PLoS One 6:e24310. doi:10.1371/journal.pone.0024310.
59. Köhler T, Michea-Hamzehpour M, Henze U, Gotoh N, Curty LK, Pechere JC. 1997. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol. Microbiol. 23:345-354.
60. Wong HC, Lessie TG. 1979. Hydroxy amino acid metabolism in Pseudomonas cepacia: role of L-serine deaminase in dissimilation of serine, glycine, and threonine. J. Bacteriol. 140:240 -245.
61. Jacob GS, Garbow JR, Schaefer J, Kishore GM. 1987. Solid-state NMR studies of regulation of N-(phosphonomethyl)glycine and glycine metabolism in Pseudomonas sp. strain PG2982. J. Biol. Chem. 262:1552-1557.
62. Kishore GM, Jacob GS. 1987. Degradation of glyphosate by Pseudomonas sp. PG2982 via a sarcosine intermediate. J. Biol. Chem. 262:12164 -12168.
63. Diab F, Bernard T, Bazire A, Haras D, Blanco C, Jebbar M. 2006. Succinate-mediated catabolite repression control on the production of glycine betaine catabolic enzymes in Pseudomonas aeruginosa PAO1 under low and elevated salinities. Microbiology 152:1395-1406.
64. Wargo MJ, Szwergold BS, Hogan DA. 2008. Identification of two gene clusters and a transcriptional regulator required for Pseudomonas aeruginosa glycine betaine catabolism. J. Bacteriol. 190:2690 -2699.
65. Schuster M, Lostroh CP, Ogi T, Greenberg EP. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorumcontrolled genes: a transcriptome analysis. J. Bacteriol. 185:2066 -2079.
66. Maseda H, Uwate M, Nakae T. 2010. Transcriptional regulation of the mexEF-oprN multidrug efflux pump operon by MexT and an unidentified repressor in nfxC-type mutant of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 311:36-43.
67. Fargier E, Mac Aogain M, Mooij MJ, Woods DF, Morrissey JP, Dobson AD, Adams C, O'Gara F. 2012. MexT functions as a redox-responsive regulator modulating disulfide stress resistance in Pseudomonas aeruginosa. J. Bacteriol. 194:3502-3511.
68. Westfall LW, Carty NL, Layland N, Kuan P, Colmer-Hamood JA, Hamood AN. 2006. mvaT mutation modifies the expression of the Pseudomonas aeruginosa multidrug efflux operon mexEF-oprN. FEMS Microbiol. Lett. 255:247-254.
69. Thompson LS, Webb JS, Rice SA, Kjelleberg S. 2003. The alternative sigma factor RpoN regulates the quorum sensing gene rhlI in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 220:187-195.
70. Köhler T, Harayama S, Ramos JL, Timmis KN. 1989. Involvement of Pseudomonas putida RpoN sigma factor in regulation of various metabolic functions. J. Bacteriol. 171:4326-4333.
71. Li W, Lu CD. 2007. Regulation of carbon and nitrogen utilization by CbrAB and NtrBC two-component systems in Pseudomonas aeruginosa. J. Bacteriol. 189:5413-5420.