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Oxidative stress response in Pseudomonas putida

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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.

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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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287:15544–15556

    CAS  PubMed Central  PubMed  Google Scholar 

  • Antelmann H, Helmann JD (2011) Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14:1049–1063

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192–208

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Conway T (1992) The Entner–Doudoroff pathway: history, physiology and molecular biology. FEMS Microbiol Rev 9:1–27

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Díaz E, Ferrández A, Prieto MA, García JL (2001) Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65:523–569

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Dubbs JM, Mongkolsuk S (2012) Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol 194:5495–5503

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dwyer DJ, Kohanski MA, Collins JJ (2009) Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 12:482–489

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Farr SB, Kogoma T (1991) Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 55:561–585

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    CAS  PubMed  Google Scholar 

  • Fuhrer T, Fischer E, Sauer U (2005) Experimental identification and quantification of glucose metabolism in seven bacterial species. J Bacteriol 187:1581–1590

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hervás AB, Canosa I, Santero E (2008) Transcriptome analysis of Pseudomonas putida in response to nitrogen availability. J Bacteriol 190:416–420

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418

    CAS  PubMed  Google Scholar 

  • Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776

    CAS  PubMed Central  PubMed  Google Scholar 

  • Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454

    CAS  PubMed Central  PubMed  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ju KS, Parales RE (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74:250–272

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Katsuwon J, Anderson AJ (1989) Response of plant-colonizing pseudomonads to hydrogen peroxide. Appl Environ Microbiol 55:2985–2989

    CAS  PubMed Central  PubMed  Google Scholar 

  • Katsuwon J, Anderson AJ (1990) Catalase and superoxide dismutase of root-colonizing saprophytic fluorescent pseudomonads. Appl Environ Microbiol 56:3576–3582

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuo CF, Mashino T, Fridovich I (1987) α, β-Dihydroxyisovalerate dehydratase: a superoxide-sensitive enzyme. J Biol Chem 262:4724–4727

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Leigh JA, Dodsworth JA (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61:349–377

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luong TT, Newell SW, Lee CY (2003) Mgr, a novel global regulator in Staphylococcus aureus. J Bacteriol 185:3703–3710

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Martin RG, Rosner JL (2001) The AraC transcriptional activators. Curr Opin Microbiol 4:132–137

    CAS  PubMed  Google Scholar 

  • Martin RG, Rosner JL (2003) Analysis of microarray data for the marA, soxS, and rob regulons of Escherichia coli. Methods Enzymol 370:278–280

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59:604–622

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miller CD, Kim YC, Anderson AJ (2001) Competitiveness in root colonization by Pseudomonas putida requires the rpoS gene. Can J Microbiol 47:41–48

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ninfa AJ, Jiang P (2005) PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168–173

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pomposiello PJ, Demple B (2001) Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–114

    CAS  PubMed  Google Scholar 

  • Poole LB (2005) Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433:240–254

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Raiger-Iustman LJ, Ruiz JA (2008) The alternative sigma factor, sigmaS, affects polyhydroxyalkanoate metabolism in Pseudomonas putida. FEMS Microbiol Lett 284:218–224

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Romano AH, Conway T (1996) Evolution of carbohydrate metabolic pathways. Res Microbiol 147:448–455

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Schellhorn HE (1995) Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol Lett 131:113–119

    CAS  PubMed  Google Scholar 

  • Schröder I, Johnson E, de Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27:427–447

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Timmis KN (2002) Pseudomonas putida: a cosmopolitan opportunist par excellence. Environ Microbiol 4:779–781

    PubMed  Google Scholar 

  • Touati D (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1–6

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wackett LP (2003) Pseudomonas putida—a versatile biocatalyst. Nat Biotechnol 21:136–138

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wu J, Weiss B (1992) Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli. J Bacteriol 174:3915–3920

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zheng M, Storz G (2000) Redox sensing by prokaryotic transcription factors. Biochem Pharmacol 59:1–6

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

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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).

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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

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