Abstract
Pseudomonas putida is widely distributed in nature and is capable of degrading various organic compounds due to its high metabolic versatility. The survival capacity of P. putida stems from its frequent exposure to various endogenous and exogenous oxidative stresses. Oxidative stress is an unavoidable consequence of interactions with various reactive oxygen species (ROS)-inducing agents existing in various niches. ROS could facilitate the evolution of bacteria by mutating genomes. Aerobic bacteria maintain defense mechanisms against oxidative stress throughout their evolution. To overcome the detrimental effects of oxidative stress, P. putida has developed defensive cellular systems involving induction of stress-sensing proteins and detoxification enzymes as well as regulation of oxidative stress response networks. Genetic responses to oxidative stress in P. putida differ markedly from those observed in Escherichia coli and Salmonella spp. Two major redox-sensing transcriptional regulators, SoxR and OxyR, are present and functional in the genome of P. putida. However, the novel regulators FinR and HexR control many genes belonging to the E. coli SoxR regulon. Oxidative stress can be generated by exposure to antibiotics, and iron homeostasis in P. putida is crucial for bacterial cell survival during treatment with antibiotics. This review highlights and summarizes current knowledge of oxidative stress in P. putida, as a model soil bacterium, together with recent studies from molecular genetics perspectives.
Similar content being viewed by others
References
Aliverti A, Pandini V, Pennati A, de Rosa M, Zanetti G (2008) Structural and functional diversity of ferredoxin-NADP+ reductases. Arch Biochem Biophys 474:283–291
An BC, Lee SS, Lee EM, Lee JT, Wi SG, Jung HS, Park W, Lee SY, Chung BY (2011a) Functional switching of a novel prokaryotic 2-Cys peroxiredoxin (PpPrx) under oxidative stress. Cell Stress Chaperones 16:317–328
An BC, Lee SS, Lee JT, Hong SH, Wi SG, Chung BY (2011b) Engineering of 2-Cys peroxiredoxin for enhanced stress-tolerance. Mol Cells 32:257–264
Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287:15544–15556
Antelmann H, Helmann JD (2011) Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14:1049–1063
Arcondéguy T, Jack R, Merrick M (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105
Banh A, Chavez V, Doi J, Nguyen A, Hernandez S, Ha V, Jimenez P, Espinoza F, Johnson HA (2013) Manganese (Mn) oxidation increases intracellular Mn in Pseudomonas putida GB-1. PLoS One 8:e77835
Bar-Even A, Noor E, Lewis NE, Milo R (2010) Design and analysis of synthetic carbon fixation pathways. Proc Natl Acad Sci USA 107:8889–8894
Benndorf D, Thiersch M, Loffhagen N, Kunath C, Harms H (2006) Pseudomonas putida KT2440 responds specifically to chlorophenoxy herbicides and their initial metabolites. Proteomics 6:3319–3329
Briggs GS, Mahdi AA, Wen Q, Lloyd RG (2005) DNA binding by the substrate specificity (wedge) domain of RecG helicase suggests a role in processivity. J Biol Chem 280:13921–13927
Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
Cao B, Loh KC (2008) Catabolic pathways and cellular responses of Pseudomonas putida P8 during growth on benzoate with a proteomics approach. Biotechnol Bioeng 101:1297–1312
Carlsson J, Carpenter VS (1980) The recA + gene product is more important than catalase and superoxide dismutase in protecting Escherichia coli against hydrogen peroxide toxicity. J Bacteriol 142:319–321
Chang WS, Li X, Halverson LJ (2009) Influence of water limitation on endogenous oxidative stress and cell death within unsaturated Pseudomonas putida biofilms. Environ Microbiol 11:1482–1492
Chauvatcharin N, Atichartpongkul S, Utamapongchai S, Whangsuk W, Vattanaviboon P, Mongkolsuk S (2005) Genetic and physiological analysis of the major OxyR-regulated katA from Xanthomonas campestris pv. phaseoli. Microbiology 151:597–605
Chavarría M, Kleijn RJ, Sauer U, Pflüger-Grau K, de Lorenzo V (2012) Regulatory tasks of the phosphoenolpyruvate–phosphotransferase system of Pseudomonas putida in central carbon metabolism. MBio 3:e00028-12
Chavarría M, Nikel PI, Pérez-Pantoja D, de Lorenzo V (2013) The Entner–Doudoroff pathway empowers Pseudomonas putida KT2440 with a high tolerance to oxidative stress. Environ Microbiol 15:1772–1785
Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192–208
Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 525:161–169
Choi HJ, Yoo JS, Jeong YK, Joo WH (2013) Involvement of antioxidant defense system in solvent tolerance of Pseudomonas putida BCNU 106. J Basic Microbiol. doi:10.1002/jobm.201300176
Conway T (1992) The Entner–Doudoroff pathway: history, physiology and molecular biology. FEMS Microbiol Rev 9:1–27
De Smet MJ, Kingma J, Witholt B (1978) The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of Escherichia coli. Biochim Biophys Acta 506:64–80
Del Castillo T, Ramos JL, Rodríguez-Herva JJ, Fuhrer T, Sauer U, Duque E (2007) Convergent peripheral pathways catalyze initial glucose catabolism in Pseudomonas putida: genomic and flux analysis. J Bacteriol 189:5142–5152
Del Castillo T, Duque E, Ramos JL (2008) A set of activators and repressors control peripheral glucose pathways in Pseudomonas putida to yield a common central intermediate. J Bacteriol 190:2331–2339
Deng X, Weerapana E, Ulanovskaya O, Sun F, Liang H, Ji Q, Ye Y, Fu Y, Zhou L, Li J, Zhang H, Wang C, Alvarez S, Hicks LM, Lan L, Wu M, Cravatt BF, He C (2013) Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe 13:358–370
Deng X, Liang H, Ulanovskaya OA, Ji Q, Zhou T, Sun F, Lu Z, Hutchison AL, Lan L, Wu M, Cravatt BF, He C (2014) Steady-state hydrogen peroxide induces glycolysis in Staphylococcus aureus and Pseudomonas aeruginosa. J Bacteriol. doi:10.1128/JB.01538-14
Díaz E, Ferrández A, Prieto MA, García JL (2001) Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65:523–569
Dietrich LE, Teal TK, Price-Whelan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206
Ding H, Demple B (2000) Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc Natl Acad Sci U S A 97:5146–5150
Domínguez-Cuevas P, González-Pastor JE, Marqués S, Ramos JL, de Lorenzo V (2006) Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 281:11981–11991
Dos Santos VA, Heim S, Moore ER, Strätz M, Timmis KN (2004) Insights into the genomic basis of niche specificity of Pseudomonas putida KT2440. Environ Microbiol 6:1264–1286
Dubbs JM, Mongkolsuk S (2012) Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol 194:5495–5503
Dwyer DJ, Kohanski MA, Collins JJ (2009) Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 12:482–489
Ehira S, Ogino H, Teramoto H, Inui M, Yukawa H (2009) Regulation of quinone oxidoreductase by the redox-sensing transcriptional regulator QorR in Corynebacterium glutamicum. J Biol Chem 284:16736–16742
Ehira S, Teramoto H, Inui M, Yukawa H (2010) A novel redox-sensing transcriptional regulator CyeR controls expression of an Old Yellow Enzyme family protein in Corynebacterium glutamicum. Microbiology 156:1335–1341
Farr SB, Kogoma T (1991) Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 55:561–585
Fernández M, Niqui-Arroyo JL, Conde S, Ramos JL, Duque E (2012) Enhanced tolerance to naphthalene and enhanced rhizoremediation performance for Pseudomonas putida KT2440 via the NAH7 catabolic plasmid. Appl Environ Microbiol 78:5104–5110
Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R (2013) Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc Natl Acad Sci U S A 110:10039–10044
Follonier S, Escapa IF, Fonseca PM, Henes B, Panke S, Zinn M, Prieto MA (2013) New insights on the reorganization of gene transcription in Pseudomonas putida KT2440 at elevated pressure. Microb Cell Factories 12:30
Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112
Fuhrer T, Fischer E, Sauer U (2005) Experimental identification and quantification of glucose metabolism in seven bacterial species. J Bacteriol 187:1581–1590
Fukumori F, Kishii M (2001) Molecular cloning and transcriptional analysis of the alkyl hydroperoxide reductase genes from Pseudomonas putida KT2442. J Gen Appl Microbiol 47:269–277
Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243
Giró M, Carrillo N, Krapp AR (2006) Glucose-6-phosphate dehydrogenase and ferredoxin-NADP(H) reductase contribute to damage repair during the soxRS response of Escherichia coli. Microbiology 152:1119–1128
Godoy P, Molina-Henares AJ, de la Torre J, Duque E, Ramos JL (2010) Characterization of the RND family of multidrug efflux pumps: in silico to in vivo confirmation of four functionally distinct subgroups. Microb Biotechnol 3:691–700
Gonzalez CF, Ackerley DF, Lynch SV, Matin A (2005) ChrR, a soluble quinone reductase of Pseudomonas putida that defends against H2O2. J Biol Chem 280:22590–22595
Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966
Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B (1990) Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci U S A 87:6181–6185
Gyaneshwar P, Paliy O, McAuliffe J, Popham DL, Jordan MI, Kustu S (2005) Sulfur and nitrogen limitation in Escherichia coli K-12: specific homeostatic responses. J Bacteriol 187:1074–1090
Hager PW, Calfee MW, Phibbs PV (2000) The Pseudomonas aeruginosa devB/SOL homolog, pgl, is a member of the hex regulon and encodes 6-phosphogluconolactonase. J Bacteriol 182:3934–3941
Heim S, Ferrer M, Heuer H, Regenhardt D, Nimtz M, Timmis KN (2003) Proteome reference map of Pseudomonas putida strain KT2440 for genome expression profiling: distinct responses of KT2440 and Pseudomonas aeruginosa strain PAO1 to iron deprivation and a new form of superoxide dismutase. Environ Microbiol 5:1257–1269
Helmann JD, Wu MF, Gaballa A, Kobel PA, Morshedi MM, Fawcett P, Paddon C (2003) The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J Bacteriol 185:243–253
Hervás AB, Canosa I, Santero E (2008) Transcriptome analysis of Pseudomonas putida in response to nitrogen availability. J Bacteriol 190:416–420
Hidalgo E, Demple B (1997) Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor. EMBO J 16:1056–1065
Hidalgo E, Ding H, Demple B (1997) Redox signal transduction: mutations shifting [2Fe–2S] centers of the SoxR sensor-regulator to the oxidized form. Cell 88:121–129
Hishinuma S, Yuki M, Fujimura M, Fukumori F (2006) OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida. Environ Microbiol 8:2115–2124
Hishinuma S, Ohtsu I, Fujimura M, Fukumori F (2008) OxyR is involved in the expression of thioredoxin reductase TrxB in Pseudomonas putida. FEMS Microbiol Lett 289:138–145
Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418
Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776
Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454
Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309
Ivanova A, Miller C, Glinsky G, Eisenstark A (1994) Role of rpoS (katF) in oxyR-independent regulation of hydroperoxidase I in Escherichia coli. Mol Microbiol 12:571–578
Jamet A, Kiss E, Batut J, Puppo A, Hérouart D (2005) The katA catalase gene is regulated by OxyR in both free-living and symbiotic Sinorhizobium meliloti. J Bacteriol 187:376–381
Ju KS, Parales RE (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74:250–272
Kaito C, Morishita D, Matsumoto Y, Kurokawa K, Sekimizu K (2006) Novel DNA binding protein SarZ contributes to virulence in Staphylococcus aureus. Mol Microbiol 62:1601–1617
Katsuwon J, Anderson AJ (1989) Response of plant-colonizing pseudomonads to hydrogen peroxide. Appl Environ Microbiol 55:2985–2989
Katsuwon J, Anderson AJ (1990) Catalase and superoxide dismutase of root-colonizing saprophytic fluorescent pseudomonads. Appl Environ Microbiol 56:3576–3582
Kim FJ, Kim HP, Hah YC, Roe JH (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur J Biochem 241:178–785
Kim EJ, Chung HJ, Suh B, Hah YC, Roe JH (1998) Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Müller. Mol Microbiol 27:187–195
Kim YC, Miller CD, Anderson AJ (1999) Transcriptional regulation by iron of genes encoding iron- and manganese-superoxide dismutases from Pseudomonas putida. Gene 239:129–135
Kim YC, Miller CD, Anderson AJ (2000) Superoxide dismutase activity in Pseudomonas putida affects utilization of sugars and growth on root surfaces. Appl Environ Microbiol 66:1460–1467
Kim J, Jeon CO, Park W (2008) Dual regulation of zwf-1 by both 2-keto-3-deoxy-6-phosphogluconate and oxidative stress in Pseudomonas putida. Microbiology 154:3905–3916
Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810
Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ (2008) Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135:679–690
Krayl M, Benndorf D, Loffhagen N, Babel W (2003) Use of proteomics and physiological characteristics to elucidate ecotoxic effects of methyl tert-butyl ether in Pseudomonas putida KT2440. Proteomics 3:1544–1552
Kullik I, Toledano MB, Tartaglia LA, Storz G (1995) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177:1275–1284
Kuo CF, Mashino T, Fridovich I (1987) α, β-Dihydroxyisovalerate dehydratase: a superoxide-sensitive enzyme. J Biol Chem 262:4724–4727
Lan L, Murray TS, Kazmierczak BI, He C (2010) Pseudomonas aeruginosa OspR is an oxidative stress sensing regulator that affects pigment production, antibiotic resistance and dissemination during infection. Mol Microbiol 75:76–91
Lee K (1999) Benzene-induced uncoupling of naphthalene dioxygenase activity and enzyme inactivation by production of hydrogen peroxide. 181:2719–2725
Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn WS, Yu MH, Storz G, Ryu SE (2004) Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11:1179–1185
Lee Y, Ahn E, Park S, Madsen EL, Jeon CO, Park W (2006a) Construction of a reporter strain Pseudomonas putida for the detection of oxidative stress caused by environmental pollutants. J Microbiol Biotechnol 16:386–390
Lee Y, Peña-Llopis S, Kang YS, Shin HD, Demple B, Madsen EL, Jeon CO, Park W (2006b) Expression analysis of the fpr (ferredoxin-NADP+ reductase) gene in Pseudomonas putida KT2440. Biochem Biophys Res Commun 339:1246–1254
Lee Y, Yeom J, Kang YS, Kim J, Sung JS, Jeon CO, Park W (2007) Molecular characterization of FprB (ferredoxin-NADP+ reductase) in Pseudomonas putida KT2440. J Microbiol Biotechnol 17:1504–1512
Lee Y, Oh S, Park W (2009) Inactivation of the Pseudomonas putida KT2440 dsbA gene promotes extracellular matrix production and biofilm formation. FEMS Microbiol Lett 297:38–48
Leigh JA, Dodsworth JA (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61:349–377
Li Z, Demple B (1994) SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J Biol Chem 269:18371–18377
Lundberg BE, Wolf RE Jr, Dinauer MC, Xu Y, Fang FC (1999) Glucose 6-phosphate dehydrogenase is required for Salmonella typhimurium virulence and resistance to reactive oxygen and nitrogen intermediates. Infect Immun 67:436–438
Luong TT, Newell SW, Lee CY (2003) Mgr, a novel global regulator in Staphylococcus aureus. J Bacteriol 185:3703–3710
Manara A, DalCorso G, Baliardini C, Farinati S, Cecconi D, Furini A (2012) Pseudomonas putida response to cadmium: changes in membrane and cytosolic proteomes. J Proteome Res 11:4169–4179
Martin RG, Rosner JL (2001) The AraC transcriptional activators. Curr Opin Microbiol 4:132–137
Martin RG, Rosner JL (2003) Analysis of microarray data for the marA, soxS, and rob regulons of Escherichia coli. Methods Enzymol 370:278–280
Martínez-García E, Nikel PI, Chavarría M, de Lorenzo V (2014) The metabolic cost of flagellar motion in Pseudomonas putida KT2440. Environ Microbiol 16:291–303
Matilla MA, Espinosa-Urgel M, Rodríguez-Herva JJ, Ramos JL, Ramos-González MI (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8:R179
Matilla MA, Ramos JL, Bakker PA, Doornbos R, Badri DV, Vivanco JM, Ramos-González MI (2010) Pseudomonas putida KT2440 causes induced systemic resistance and changes in Arabidopsis root exudation. Environ Microbiol Rep 2:381–388
Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59:604–622
Miller CD, Kim YC, Anderson AJ (1997) Cloning and mutational analysis of the gene for the stationary-phase inducible catalase (catC) from Pseudomonas putida. J Bacteriol 179:5241–5245
Miller CD, Kim YC, Anderson AJ (2001) Competitiveness in root colonization by Pseudomonas putida requires the rpoS gene. Can J Microbiol 47:41–48
Miller CD, Pettee B, Zhang C, Pabst M, McLean JE, Anderson AJ (2009) Copper and cadmium: responses in Pseudomonas putida KT2440. Lett Appl Microbiol 49:775–783
Miura K, Inouye S, Nakazawa A (1998) The rpoS gene regulates OP2, an operon for the lower pathway of xylene catabolism on the TOL plasmid, and the stress response in Pseudomonas putida mt-2. Mol Gen Genet 259:72–78
Mukhopadhyay P, Zheng M, Bedzyk LA, LaRossa RA, Storz G (2004) Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc Natl Acad Sci U S A 101:745–750
Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, 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 JA, Timmis KN, 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
Nikel PI, De Lorenzo V (2012) Implantation of unmarked regulatory and metabolic modules in Gram negative bacteria with specialised mini-transposon delivery vectors. J Biotechnol 163:143–154
Nikel PI, Chavarría M, Martínez-García E, Taylor AC, de Lorenzo V (2013) Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440. Microb Cell Factories 12:50
Ninfa AJ, Jiang P (2005) PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168–173
Ninfa AJ, Jiang P, Atkinson MR, Peliska JA (2000) Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr Top Cell Regul 36:31–75
Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K, Hassett DJ (2000) Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J Bacteriol 182:4533–4544
Paget MS, Buttner MJ (2003) Thiol-based regulatory switches. Annu Rev Genet 37:91–121
Park W, Jeon CO, Cadillo H, DeRito C, Madsen EL (2004) Survival of naphthalene-degrading Pseudomonas putida NCIB 9816-4 in naphthalene-amended soils: toxicity of naphthalene and its metabolites. Appl Microbiol Biotechnol 64:429–435
Park S, You X, Imlay JA (2005) Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc Natl Acad Sci U S A 102:9317–9322
Park W, Peña-Llopis S, Lee Y, Demple B (2006) Regulation of superoxide stress in Pseudomonas putida KT2440 is different from the SoxR paradigm in Escherichia coli. Biochem Biophys Res Commun 341:51–56
Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V (2013) Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLoS Genet 9:e1003764
Petruschka L, Adolf K, Burchhardt G, Dernedde J, Jürgensen J, Herrmann H (2002) Analysis of the zwf-pgl-eda-operon in Pseudomonas putida strains H and KT2440. FEMS Microbiol Lett 215:89–95
Poblete-Castro I, Becker J, Dohnt K, dos Santos VM, Wittmann C (2012) Industrial biotechnology of Pseudomonas putida and related species. Appl Microbiol Biotechnol 93:2279–2290
Pomposiello PJ, Demple B (2001) Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–114
Poole LB (2005) Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433:240–254
Poole LB, Ellis HR (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35:56–64
Puchałka J, Oberhardt MA, Godinho M, Bielecka A, Regenhardt D, Timmis KN, Papin JA, Martins dos Santos VA (2008) Genome-scale reconstruction and analysis of the Pseudomonas putida KT2440 metabolic network facilitates applications in biotechnology. PLoS Comput 4:e1000210
Raiger-Iustman LJ, Ruiz JA (2008) The alternative sigma factor, sigmaS, affects polyhydroxyalkanoate metabolism in Pseudomonas putida. FEMS Microbiol Lett 284:218–224
Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56:743–768
Ray P, Girard V, Gault M, Job C, Bonneu M, Mandrand-Berthelot MA, Singh SS, Job D, Rodrigue A (2013) Pseudomonas putida KT2440 response to nickel or cobalt induced stress by quantitative proteomics. Metallomics 5:68–79
Romano AH, Conway T (1996) Evolution of carbohydrate metabolic pathways. Res Microbiol 147:448–455
Santos PM, Benndorf D, Sá-Correia I (2004) Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics. Proteomics 4:2640–2652
Schellhorn HE (1995) Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol Lett 131:113–119
Schröder I, Johnson E, de Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27:427–447
Schweigert N, Zehnder AJ, Eggen RI (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3:81–91
Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181
Shamim S, Rehman A (2013) Antioxidative enzyme profiling and biosorption ability of Cupriavidus metallidurans CH34 and Pseudomonas putida mt2 under cadmium stress. J Basic Microbiol. doi:10.1002/jobm.201300038
Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222
Tavita K, Mikkel K, Tark-Dame M, Jerabek H, Teras R, Sidorenko J, Tegova R, Tover A, Dame RT, Kivisaar M (2012) Homologous recombination is facilitated in starving populations of Pseudomonas putida by phenol stress and affected by chromosomal location of the recombination target. Mutat Res 737:12–24
Temple L, Sage A, Christie GE, Phibbs PV Jr (1994) Two genes for carbohydrate catabolism are divergently transcribed from a region of DNA containing the hexC locus in Pseudomonas aeruginosa PAO1. J Bacteriol 176:4700–4709
Timmis KN (2002) Pseudomonas putida: a cosmopolitan opportunist par excellence. Environ Microbiol 4:779–781
Touati D (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1–6
Venturi V, Ottevanger C, Bracke M, Weisbeek P (1995) Iron regulation of siderophore biosynthesis and transport in Pseudomonas putida WCS358: involvement of a transcriptional activator and of the Fur protein. Mol Microbiol 15:1081–1093
Wackett LP (2003) Pseudomonas putida—a versatile biocatalyst. Nat Biotechnol 21:136–138
Wang X, Mukhopadhyay P, Wood MJ, Outten FW, Opdyke JA, Storz G (2006) Mutational analysis to define an activating region on the redox-sensitive transcriptional regulator OxyR. J Bacteriol 188:8335–8342
Woodmansee AN, Imlay JA (2002) Reduced flavins promote oxidative DNA damage in non-respiring Escherichia coli by delivering electrons to intracellular free iron. J Biol Chem 277:34055–34066
Wu J, Weiss B (1992) Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli. J Bacteriol 174:3915–3920
Yeom J, Jeon CO, Madsen EL, Park W (2009a) Ferredoxin-NADP+ reductase from Pseudomonas putida functions as a ferric reductase. J Bacteriol 191:1472–1479
Yeom J, Jeon CO, Madsen EL, Park W (2009b) In vitro and in vivo interactions of ferredoxin-NADP+ reductases in Pseudomonas putida. J Biochem 145:481–491
Yeom J, Imlay JA, Park W (2010a) Iron homeostasis affects antibiotic-mediated cell death in Pseudomonas species. J Biol Chem 285:22689–22695
Yeom S, Yeom J, Park W (2010b) Molecular characterization of FinR, a novel redox-senxing transcriptional regulator in Pseudomonas putida KT2440. Microbiology 156:1487–1496
Yeom S, Yeom J, Park W (2010c) NtrC-sensed nitrogen availability is important for oxidative stress defense in Pseudomonas putida KT2440. J Microbiol 48:153–159
Yeom J, Lee Y, Park W (2012) ATP-dependent RecG helicase is required for the transcriptional regulator OxyR function in Pseudomonas species. J Biol Chem 287:24492–24504
Yu H, Kim BJ, Rittmann BE (2001) The roles of intermediates in biodegradation of benzene, toluene, and p-xylene by Pseudomonas putida F1. Biodegradation 12:455–463
Yun SH, Kim YH, Joo EJ, Choi JS, Sohn JH, Kim SI (2006) Proteome analysis of cellular response of Pseudomonas putida KT2440 to tetracycline stress. Curr Microbiol 53:95–101
Zheng M, Storz G (2000) Redox sensing by prokaryotic transcription factors. Biochem Pharmacol 59:1–6
Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570
Zimmer DP, Soupene E, Lee HL, Wendisch VF, Khodursky AB, Peter BJ, Bender RA, Kustu S (2000) Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci U S A 97:14674–14679
Acknowledgments
This work was supported by the Mid-career Researcher Program through an NRF grant (2014R1A2A2A05007010) funded by the Ministry of Science, ICT, & Future Planning (MSIP).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kim, J., Park, W. Oxidative stress response in Pseudomonas putida . Appl Microbiol Biotechnol 98, 6933–6946 (2014). https://doi.org/10.1007/s00253-014-5883-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-5883-4