The yin and yang of phenazine physiology

Microbial Phenazines: Biosynthesis, Agriculture and Health

Volumn , Issue , 2013, Pages 43-69

  Grahl, Nora ^a   Kern, Suzanne E ^b   Newman, Dianne K ^b   Hogan, Deborah A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84908327950     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-40573-0_3     Document Type: Chapter

References (160)

1. Allen L, Dockrell DH, Pattery T et al (2005) Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J Immunol 174(6):3643-3649
2. Alves MJ, Rabinovitch M (1983) Destruction of intracellular Trypanosoma cruzi after treatment of infected macrophages with cationic electron carriers. Infect Immun 39(1):435-438
3. Amin R, Dupuis A, Aaron SD et al (2010) The effect of chronic infection with Aspergillus fumigatus on lung function and hospitalization in patients with cystic fibrosis. Chest 137(1): 171-176
4. Aoki S, Ito-Kuwa S (1982) Respiration of Candida albicans in relation to its morphogenesis. Plant Cell Physiol 23(4):721-726
5. Armstrong AV, Stewart-Tull DE (1971) The site of the activity of extracellular products of Pseudomonas aeruginosa in the electron-transport chain in mammalian cell respiration. J Med Microbiol 4(2):263-270
6. Armstrong AV, Stewart-Tull DE, Roberts JS (1971) Characterisation of the Pseudomonas aeruginosa factor that inhibits mouse-liver mitochondrial respiration. J Med Microbiol 4(2): 249-262
7. Audenaert K, Pattery T, Cornelis P et al (2002) Induction of systemic resistance to Botyris cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyocholin, and pyocyanin. Mol Plant Microbe Interact 15:1147-1156
8. Avital A, Uwyyed K, Picard E et al (1995) Sensitivity and specificity of oropharyngeal suction versus bronchoalveolar lavage in identifying respiratory tract pathogens in children with chronic pulmonary infection. Pediatr Pulmonol 20(1):40-43
9. Banin E, Lozinski A, Brady KM et al (2008) The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc Natl Acad Sci USA 105(43):16761-16766
10. Baron SS, Rowe JJ (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20(6): 814-820
11. Baron SS, Terranova G, Rowe JJ (1989) Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol 18:223-230
12. Barron ES, Hoffman LA (1930) The catalytic effect of dyes on the oxygen consumption of living cells. J Gen Physiol 13(4):483-494
13. Bauernfeind A, Hörl G, Jungwirth R et al (1987) Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15(4):270-277
14. Bhargava V, Tomashefski JF Jr, Stern RC et al (1989) The pathology of fungal infection and colonization in patients with cystic fibrosis. Hum Pathol 20(10):977-986
15. Bolwerk A, Lagopodi AL, Wijfjes AH et al (2003) Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f. sp. radicis-lycopersici. Mol Plant Microbe Interact 16(11):983-993
16. Brisbane PG, Janik L, Tate M et al (1987) Revised structure for the phenazine antibiotic from Pseudomonas fluorescens 2-79 (NRRL B-15132). Antimicrob Agents Chemother 31(12): 1967-1971
17. Bull CT, Weller DM, Thomashow LS (1991) Relationship between root colonization and suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strain 2-79. Phytopathology 81:954-959
18. Burns JL, Van Dalfsen JM, Shawar RM et al (1999) Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis. J Infect Dis 179(5):1190-1196
19. Byng GS, Eustice DC, Jensen RA (1963) Biosynthesis of phenazine pigments in mutant and wildtype cultures of Pseudomonas aeruginosa. J Bacteriol 138:846-852
20. Cezairliyan B, Vinayavekhin N, Grenfell-Lee D et al (2013) Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog 9(1):e1003101
21. Chang HR, Pechere JC (1989) In-vitro toxoplasmacidal activity of cationic electron carriers. J Antimicrob Chemother 23(2):229-235
22. Chin-A-Woeng, TF, Bloemberg GV, van der Bij AJ et al (1998) Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol Plant Microbe Interact 11(11):1069-1077
23. Chin-A-Woeng TF, Bloemberg GV, Mulders IH, Dekkers LC, Lugtenberg BJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 13: 1340-1345
24. Chotirmall SH, O'Donoghue E, Bennett K et al (2010) Sputum Candida albicans presages FEV(1) decline and hospital-treated exacerbations in cystic fibrosis. Chest 138(5):1186-1195
25. Cornelis P, Matthijs S (2002) Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 4(12):787-798
26. Cox CD (1980) Iron reductases from Pseudomonas aeruginosa. J Bacteriol 141(1):199-204
27. Cox CD (1986) Role of pyocyanin in the acquisition of iron from transferrin. Infect Immun 52(1):263-270
28. Cugini C, Calfee MW, Farrow JM et al (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65(4):896-906
29. Cugini C, Morales DK, Hogan DA (2010) Candida albicans-produced farnesol stimulates Pseudomonas quinolone signal production in LasR-defective Pseudomonas aeruginosa strains. Microbiology 156(10):3096-3107
30. e Andrade-Neto VF, Goulart MOF, da Silva Filho JF et al (2004) Antimalarial activity of phenazines from lapachol, beta-lapachone and its derivatives against Plasmodium falciparum in vitro and Plasmodium berghei in vivo. Bioorg Med Chem Lett 14(5):1145-1149
31. de Macedo JL, Santos JB (2005) Bacterial and fungal colonization of burn wounds. Mem Inst Oswaldo Cruz 100(5):535-539
32. De Vleesschauwer D, Cornelis P, HöfteM(2006) Redox-active pyocyanin secreted by Pseudomonas aeruginosa7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol Plant Microbe Interact 19(12):1406-1419
33. Denning GM, Wollenweber LA, Railsback MA et al (1998a) Pseudomonas pyocyanin increases interleukin-8 expression by human airway epithelial cells. Infect Immun 66(12):5777-5784
34. Denning GM, Railsback MA, Rasmussen GT et al (1998b) Pseudomonas pyocyanine alters calcium signaling in human airway epithelial cells. Am J Physiol 274(6 Pt 1):L893-L900
35. Dietrich LE, Price-Whelan A, Petersen A et al (2006) The phenazine pyocyanin is a terminal signaling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61(5):1308-1321
36. Dietrich LEP, Price-Whelan A, Teal T et al (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203-1206
37. Dietrich LE, Okegbe C, Price-Whelan A et al (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195(7):1371-1380
38. Dong YH, Zhang XF, An SW et al (2008) A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa. Commun Integr Biol 1(1):88-96
39. Dwivedi D, Johri BN, Ineichen K et al (2009) Impact of antifungals producing rhizobacteria on the performance of Vigna radiata in the presence of arbuscular mycorrhizal fungi. Mycorrhiza 19(8):559-570
40. Emde R, Schink B (1990) Oxidation of glycerol, lactate, and propionate by Propionibacterium freudenreichii in a poised-potential amperometric culture system. Arch Microbiol 153(5):506-512
41. Emde R, Swain A, Schink B (1989) Anaerobic oxidation of glycerol by Escherichia coli in an amperometric poised-potential culture system. Appl Microbiol Biotechnol 32:170-175
42. Emmerich R, Löw O (1899) Bakteriolytische Enzyme als Ursache der erworbenen Immunität und die Heilung von Infectionskrankheiten durch dieselben. Z. Hygiene Infektionskrankheiten 31(1):1-65
43. Eschbach M, Schreiber K, Trunk K et al (2004) Long-term anaerobic survival of the opportunistic pathogen Pseudomonas aeruginosa via pyruvate fermentation. J Bacteriol 186(14):4596-4604
44. Fitzpatrick DA (2009) Lines of evidence for horizontal gene transfer of a phenazine producing operon into multiple bacterial species. J Mol Evol 68(2):171-185
45. French SW, Palmer DS, Sim WA (1973) Phenazine methosulfate uptake by rat liver mitochondria. Can J Biochem 51(3):235-240
46. Friedheim EA (1931) Pyocyanine, an accessory respiratory enzyme. J Exp Med 54(2):207-221
47. Friedheim EA (1934) The effect of pyocyanine on the respiration of some normal tissues and tumours. Biochem J 28(1):173-179
48. Gibson J, Sood A, Hogan DA (2009) Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl EnvironMicrobiol 75(2):504-513
49. Giddens SR, Houliston GJ, Mahanty HK (2003) The influence of antibiotic production and preemptive colonization on the population dynamics of Pantoea agglomerans (Erwinia herbicola) Eh1087 and Erwinia amylovora in planta. Environ Microbiol 5(10):1016-1021
50. Glasser NR, Kern SE, Newman DK. Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by promoting fermentation and ATP synthesis. Submitted
51. Gohain N, Thomashow LS, Mavrodi DV et al (2006) The purification, crystallization and preliminary structural characterization of FAD-dependent monooxygenase PhzS, a phenazinemodifying enzyme from Pseudomonas aeruginosa. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 62(10):989-992
52. Gu M, Imlay JA (2011) The SoxRS response of Escherichia coli is directly activated by redoxcycling drugs rather than by superoxide. Mol Microbiol 79(5):1136-1150
53. Gupta N, Haque A, Mukhopadhyay G et al (2005) Interactions between bacteria and Candida in the burn wound. Burns 31(3):375-378
54. Gurusiddaiah S, Weller DM, Sarkar A et al (1986) Characterization of an antibiotic produced by a strain of Pseudomonas fluorescens inhibitory to Gaeumannomyces graminis var. tritici and Pythium spp. Antimicrob Agents Chemother 29(3):488-495
55. Harmsen M, Yang L, Pamp SJ et al (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59(3):253-268
56. Harrison F, Paul J, Massey RC et al (2008) Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2(1):49-55
57. Harrop GA, Barron ES (1928) Studies on blood cell metabolism: I. The effect of methylene blue and other dyes upon the oxygen consumption of mammalian and avian erythrocytes. J Exp Med 48(2):207-223
58. Hassan HM, Fridovich I (1980) Mechanism of the antibiotic action pyocyanine. J Bacteriol 141(1):156-163
59. Hassett DJ, Charniga L, Bean K et al (1992) Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganesecofactored superoxide dismutase. Infect Immun 60(2):328-336
60. Hassett DJ, Schweizer HP, Ohman DE (1995) Pseudomonas aeruginosa sodA and sodB mutants defective in manganese-and iron-cofactored superoxide dismutase activity demonstrate the importance of the iron-cofactored form in aerobic metabolism. J Bacteriol 177(22):6330-6337
61. Hermann C, Hermann J, Munzel U et al (1999) Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses 42(11-12):619-627
62. Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70(2):921-928
63. Hoffman LR, D'Argenio DA, MacCoss MJ et al (2010) Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathog 6(1):e1000712
64. Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296(5576):2229-2232
65. Hogan DA, Sundstrom P (2009) The Ras/cAMP/PKA signaling pathway and virulence in Candida albicans. Future Microbiol 4(10):1263-1270
66. Hollstein U, Van Gemert Jr RJ (1971) Interaction of phenazines with polydeoxyribonucleotides. Biochemistry 10(3):497-504
67. Huang J, Xu Y, Zhang H et al (2009) Temperature-dependent expression of phzM and its regulatory genes lasI and ptsP in rhizosphere isolate Pseudomonas sp. strain M18. Appl Environ Microbiol 75(20):6568-6580
68. Hughes WT, Kim HK (1973) Mycoflora in cystic fibrosis: some ecologic aspects of Pseudomonas aeruginosa and Candida albicans. Mycopathol Mycol Appl 50(3):261-269
69. Hunter RC, Klepac-Ceraj V, Lorenzi MM et al (2012) Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am J Respir Cell Mol Biol 47:738-745
70. Hunter R et al (2013) Ferrous iron is a significant component of bioavailable iron in the cystic fibrosis airways. mBio 4(4):e00557-13
71. Jackowski JT, Szepfalusi Z, Wanner DA et al (1991) Effects of P. aeruginosa-derived bacterial products on tracheal ciliary function: role of O2 radicals. Am J Physiol 260(2 Pt 1):L61-67
72. Kahl BC, Duebbers A, Lubritz G et al (2003) Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J Clin Microbiol 41(9):4424-4427
73. Kanner D, Gerber NN, Bartha R (1978) Pattern of phenazine pigment production by a strain of Pseudomonas aeruginosa. J Bacteriol 134(2):690-692
74. Kanthakumar K, Taylor G, Tsang KW et al (1993) Mechanisms of action of Pseudomonas aeruginosa pyocyanin on human ciliary beat in vitro. Infect Immun 61(7):2848-2853
75. Kanthakumar K, Taylor G, Tsang K et al (1996) The effect of bacterial toxins on levels of intracellular adenosine nucleotides and human ciliary beat frequency. Pulm Pharmacol 9(4):223-230
76. Kasozi DM, Gromer S, Adler H et al (2011) The bacterial redox signaller pyocyanin as an antiplasmodial agent: comparisonswith its thioanalog methylene blue. Redox Rep 16(4):154-165
77. Kavitha K, Mathiyazhagan S, Sendhilvel V et al (2005) Broad spectrum action of phenazine against active and dormant structures of fungal pathogens and root knot nematode. Arch Phytopathol Plant Protect 38(1):69-76
78. Kerr J (1994a) Inhibition of fungal growth by Pseudomonas aeruginosa and Pseudomonas cepacia isolated from patients with cystic fibrosis. J Infect 28(3):305-310
79. Kerr JR (1994b) Suppression of fungal growth exhibited by Pseudomonas aeruginosa. J Clin Microbiol 32(2):525-527
80. Kerr JR (2000) Phenazine pigments: antibiotics and virulence factors. Infect Dis Rev 2(4): 184-194
81. Kerr JR, Taylor GW, Rutman A et al (1999) Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J Clin Pathol 52(5):385-387
82. Khare E, Arora NK (2011) Dual activity of pyocyanin from Pseudomonas aeruginosa-antibiotic against phytopathogen and signal molecule for biofilm development by rhizobia. Can J Microbiol 57(9):708-713
83. Knight M, Hartman PE, Hartman Z et al (1979) A new method of preparation of pyocyanin and demonstration of an unusual bacterial sensitivity. Anal Biochem 95(1):19-23
84. Kong F, Young L, Chen Y et al (2006) Pseudomonas aeruginosa pyocyanin inactivates lung epithelial vacuolar ATPase-dependent cystic fibrosis transmembrane conductance regulator expression and localization. Cell Microbiol 8(7):1121-1133
85. Korgaonkar A, Trivedi U, Rumbaugh K et al (2013) Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc Natl Acad Sci USA 110(3):1059-1064
86. Kreamer NNK, Wilks JC, Marlow JJ et al (2012) BqsR/BqsS constitute a two-component system that senses extracellular Fe(II) in Pseudomonas aeruginosa. J Bacteriol 194(5):1195-1204
87. Lau GW, Hassett DJ, Ran H et al (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10(12):599-606
88. Lauredo IT, Sabater JR, Ahmed A et al (1998) Mechanism of pyocyanin-and 1-hydroxyphenazine-induced lung neutrophilia in sheep airways. J Appl Physiol 85(6):2298-2304
89. Laursen JB, Nielsen J (2004) Phenazine natural products: biosynthesis, synthetic analogues, and biological activity. Chem Rev 104:1663-1685
90. Leclair LW, Hogan DA (2010) Mixed bacterial-fungal infections in the CF respiratory tract. Med Mycol 48(Suppl 1):S125-S132
91. Leeman M, Van Pelt JA, Den Ouden FM et al (1995) Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85:1021-1027
92. Leidal KG, Munson KL, Denning GM (2001) Small molecular weight secretory factors from Pseudomonas aeruginosa have opposite effects on IL-8 and RANTES expression by human airway epithelial cells. Am J Respir Cell Mol Biol 25(2):186-195
93. Liu GY, Nizet V (2009) Color me bad: microbial pigments as virulence factors. Trends Microbiol 17(9):406-413
94. Lo HJ, Köhler JR, DiDomenico B et al (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90(5):939-949
95. Maddula VSRK, Pierson EA, Pierson LS (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J Bacteriol 190(8):2759-2766
96. Mahajan-Miklos S, Tan MW, Rahme LG et al (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96(1):47-56
97. Makgatho ME et al (2000) Tetramethylpiperidine-substituted phenazines as novel antiplasmodial agents. Drug Dev Res 50(2):195-202
98. Marks MI (1990) Clinical significance of Staphylococcus aureus in cystic fibrosis. Infection 18(1):53-56
99. Mavrodi DV, Peever TL, Mavrodi OV et al (2010) Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 76:866-879
100. Mavrodi DV, Parejko JA, Mavrodi OV et al (2012) Recent insights into the diversity, frequency and ecological roles of phenazines in fluorescent Pseudomonas spp. EnvironMicrobiol 15(3):675-686
101. Mazzola M, Cook RJ, Thomashow LS et al (1992) Contribution of phenazine antibiotic synthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616-2624
102. McNamara PJ, Proctor RA (2006) Bacterial interactions and the microevolution of cytochrome bd: implications for pathogenesis. J Bacteriol 188(23):7997-7998
103. Mentel M, Ahuja EG, Mavrodi DV et al (2009) Of two make one: the biosynthesis of phenazines. ChemBioChem 10(14):2295-2304
104. Miller KM, Dearborn DG, Sorensen RU (1987) In vitro effect of synthetic pyocyanine on neutrophil superoxide production. Infect Immun 55(3):559-563
105. Mitchell AP (1988) Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1(6):687-692
106. Morales DK, Jacobs NJ, Rajamani S et al (2010) Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78(6):1379-1392
107. Morales DK, Grahl N, Okegbe C et al (2013) Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines. mBIO 4(1):e00526-e00612
108. Moreau-Marquis S, O'Toole GA, Stanton BA (2009) Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am J Respir Cell Mol Biol 41(3):305-313
109. Moree WJ, Phelan VV, Wu CH et al (2012) Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc Natl Acad Sci USA 109(34):13811-13816
110. Muhlradt PF, Tsai H, Conradt P (1986) Effects of pyocyanine, a blue pigment from Pseudomonas aeruginosa, on separate steps of T cell activation: interleukin 2 (IL 2) production, IL 2 receptor formation, proliferation and induction of cytolytic activity. Eur J Immunol 16(4):434-440
111. Musk DJ, Banko DA, Hergenrother PJ (2005) Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chem Biol 12(7):789-796
112. Nabi ZF, Rabinovitch M (1984) Inhibition by superoxide dismutase and catalase of the damage of isolated Leishmania mexicana amazonensis by phenazine methosulfate. Mol Biochem Parasitol 10(3):297-303
113. Navarro J, Rainisio M, Harms HK et al (2001) Factors associated with poor pulmonary function: cross-sectional analysis of data from the ERCF. Eur Respir J 18(2):298-305
114. O'Malley YQ, Abdalla MY, McCormick ML et al (2003a) Subcellular localization of Pseudomonas pyocyanin cytotoxicity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 284(2):L420-L430
115. O'Malley YQ, Reszka KJ, Rasmussen GT et al (2003b) The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 285(5):L1077-L1086
116. Parejko JA, Mavrodi DV, Mavrodi OV et al (2012) Population structure and diversity of phenazine-1-carboxylic acid-producing fluorescent Pseudomonas spp. from dryland cereal fields of central Washington State (USA). Microb Ecol 64:226-241
117. Phillips DA, Fox TC, King MD et al (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136(1):2887-2894
118. Pieterse CMJ, Van Pelt JA, Van Wees SCM et al (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signalling and expression. Eur J Plant Pathol 107(1):51-61
119. Price-Whelan A (2009) Physiology and mechanisms of pyocyanin reduction in Pseudomonas aeruginosa. Ph.D. Thesis, California Institute of Technology, USA
120. Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nature Chem Biol 2(2):71-78
121. Price-Whelan A, Dietrich LEP, Newman DK (2007) Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J Bacteriol 189(17):6372-6381
122. Proctor RA, von Eiff C, Kahl BC et al (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4(4):295-305
123. Rabaey K, Boon N, Siciliano SD et al (2004) Biofuel cells select for microbial consortia that selfmediate electron transfer. Appl Environ Microbiol 70(9):5373-5382
124. Rabaey K, Boon N, Höfte M et al (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39(9):3401-3408
125. Rabinovitch M, Dedet JP, Ryter A et al (1982) Destruction of Leishmania mexicana amazonensis amastigotes within macrophages in culture by phenazine methosulfate and other electron carriers. J Exp Med 155(2):415-431
126. Rada B, Leto TL (2013) Pyocyanin effects on respiratory epithelium: relevance in Pseudomonas aeruginosa airway infections. Trends Microbiol (21)2:73-81
127. Rada B, Lekstrom K, Damian S et al (2008) The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells. J Immunol 181(7):4883-4893
128. Rada B, Gardina P, Myers TG et al (2011) Reactive oxygen species mediate inflammatory cytokine release and EGFR-dependent mucin secretion in airway epithelial cells exposed to Pseudomonas pyocyanin. Mucosal Immunol 4(2):158-171
129. Ramos I, Dietrich LEP, Price-Whelan A et al (2010) Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res Microbiol 61:187-191
130. Ran H, Hassett DJ, Lau GW (2003) Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci USA 100(24):14315-14320
131. Ratner D, Mueller C (2012) Immune responses in cystic fibrosis: are they intrinsically defective? Am J Respir Cell Mol Biol 46(6):715-722
132. Recinos DA, Sekedat MD, Hernandez A et al (2012) Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci USA 109(47):19420-19425
133. Rella A, Yang MW, Gruber J et al (2012) Pseudomonas aeruginosa inhibits the growth of Cryptococcus species. Mycopathologia 173(5-6):451-461
134. Sadik CD, Kim ND, Luster AD (2011) Neutrophils cascading their way to inflammation. Trends Immunol 32(10):452-460
135. Schoental R (1941) The nature of the antibacterial agents present in Pseudomonas pyocyanea cultures. Brit J Exp Pathol 1941(22):137-147
136. Schwarzer C, Fischer H, Kim EJ et al (2008) Oxidative stress caused by pyocyanin impairs CFTR Cl-transport in human bronchial epithelial cells. Free Radic Biol Med 45(12):1653-1662
137. Shipton PJ (1975) Take-all decline during cereal monoculture. In: Biology and control of soil borne plant pathogens international symposium (3d), pp 137-144
138. Singh PK, Parsek MR, Greenberg EP et al (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417(6888):552-555
139. Slininger PJ, Jackson MA (1992) Nutritional factors regulating growth and accumulation of phenazine 1-carboxylic acid by Pseudomonas fluorescens 2-79. Appl Microbiol Biotechnol 37:388-392
140. Slininger PJ, Shea-Wilbur MA (1995) Liquid-culture pH, temperature, and carbon (not nitrogen) source regulate phenazine productivity of the take-all biocontrol agent Pseudomonas fluorescens 2-79. Appl Microbiol Biotechnol 43(5):794-800
141. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6(3):199-210
142. Stewart-Tull DE, Armstrong A (1971) The effect of 1-hydroxyphenazine and pyocyanine from Pseudomonas aeruginosa on mammalian cell respiration. J Med Microbiol 5:67-73
143. Sullivan NL, Tzeranis DS, Wang Y et al (2011) Quantifying the dynamics of bacterial secondary metabolites by spectral multiphoton microscopy. ACS Chem Biol 6(9):893-899
144. Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170(8):3499-3508
145. Thomashow LS, Weller DM, Bonsall RF et al (1990) Production of the antibiotic phenazine-1-carboxylic acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Appl Environ Microbiol 56(4):908-912
146. Toohey JI, Nelson CD, Krotkov G (1965) Toxicity of phenazine carboxylic acids to some bacteria, algae, higher plants, and animals. Can J Bot 43(9):1151-1155
147. Usher LR, Lawson RA, Geary I et al (2002) Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J Immunol 168(4):1861-1868
148. Vagelas IK, Pembroke B, Gowen SR et al (2007) The control of root-knot nematodes (Meloidogyne spp.) by Pseudomonas oryzihabitans and its immunological detection on tomato roots. Nematology 9(3):363-370
149. van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453-483
150. van Rij ET, Wesselink M, Chin-A-Woeng TFC et al (2004) Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol Plant Microbe Interact 17:557-566
151. Venkataraman A, Rosenbaum MA, Perkins SD et al (2011) Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ Sci 4:4550-4559
152. Voggu L, Schlag S, Biswas R et al (2006) Microevolution of cytochrome bd oxidase in staphylococci and its implication in resistance to respiratory toxins released by Pseudomonas. J Bacteriol 188(23):8079-8086
153. Wang Y, Newman DK (2008) Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol 42(7):2380-2386
154. WangY, Kern SE, NewmanDK(2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192(1):365-369
155. Wang Y, Wilks JC, Danhorn T et al (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193:3606-3617
156. Weller DM, Cook RJ (1983) Suppression of take-all of wheat by seed treatments with fluorescent pseudomonads. Phytopathology 73:463-469
157. Wilson R, Sykes DA, Watson D et al (1988) Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory ephithelium. Infect Immun 56(9):2515-2517
158. Worlitzsch D, Tarran R, Ulrich M et al (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109(3):317-325
159. Wurtzel O, Yoder-Himes DR, Han K et al (2012) The single-nucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLoS Pathog 8(9):e1002945
160. Young G (1947) Pigment production and antibiotic activity in cultures of Pseudomonas aeruginosa. J Bacteriol 54(2):109-117