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The role of Anr in oxidative stress resistance was investigated in Pseudomonas extremaustralis, a polyhydroxybutyrate-producing Antarctic bacterium. The absence of Anr caused increased sensitivity to hydrogen peroxide under low oxygen tension. This phenomenon was associated with a decrease in the redox ratio, higher oxygen consumption and higher reactive oxygen species production. Physiological responses of the mutant to the oxidized state included an increase in NADP(H)content, catalase activity and exopolysaccharide production. The wild-type strain showed a sharp decrease in the reduced thiol pool when exposed to hydrogen peroxide, not observed in the mutant strain. In silico analysis of the genome sequence of P. extremaustralis revealed putative Anr binding sites upstream from genes related to oxidative stress. Genes encoding several chaperones and cold shock proteins, a glutathione synthase, a sulfate transporter and a thiol peroxidase were identified as potential targets for Anr regulation. Our results suggest a novel role for Anr in oxidative stress resistance and in redox balance maintenance under conditions of restricted oxygen supply. © 2013 SGM.


Documento: Artículo
Título:Anr, the anaerobic global regulator, modulates the redox state and oxidative stress resistance in pseudomonas extremaustralis
Autor:Tribelli, P.M.; Nikel, P.I.; Oppezzo, O.J.; López, N.I.
Filiación:Dpto de Química Biologica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Investigaciones Biotecnológicas 'Dr. Rodolfo A. Ugalde', IQUIBICEN-CONICET, Universidad Nacional de San Martín, Buenos Aires, Argentina
Departamento de Radiobiología, Comisión Nacional de Energía Atómica, Buenos Aires, Argentina
Palabras clave:bacterial protein; catalase; exopolysaccharide; hydrogen peroxide; protein anr; reactive oxygen metabolite; reduced nicotinamide adenine dinucleotide phosphate; thiol; unclassified drug; article; bacterial genome; bacterial strain; binding site; controlled study; enzyme activity; gene sequence; Gram negative aerobic rods and cocci; nonhuman; oxidative stress; oxygen consumption; oxygen tension; priority journal; Pseudomonas extremaustralis; redox stress; wild type; Bacterial Proteins; DNA, Bacterial; Gene Deletion; Gene Expression Regulation, Bacterial; Genome, Bacterial; Hydrogen Peroxide; Molecular Sequence Data; Oxidation-Reduction; Oxidative Stress; Pseudomonas; Sequence Analysis, DNA; Stress, Physiological; Sulfhydryl Compounds; Transcription Factors
Página de inicio:259
Página de fin:268
Título revista:Microbiology (United Kingdom)
Título revista abreviado:Microbiology
CAS:catalase, 9001-05-2; hydrogen peroxide, 7722-84-1; reduced nicotinamide adenine dinucleotide phosphate, 53-57-6; Bacterial Proteins; DNA, Bacterial; Hydrogen Peroxide, 7722-84-1; Sulfhydryl Compounds; Transcription Factors


  • Aebi, H., Catalase in vitro (1984) Methods Enzymol, 105, pp. 121-126
  • Albesa, I., Becerra, M.C., Battán, P.C., Páez, P.L., Oxidative stress involved in the antibacterial action of different antibiotics (2004) Biochem Biophys Res Commun, 317, pp. 605-609
  • Ayub, N.D., Pettinari, M.J., Ruiz, J.A., López, N.I., A polyhydroxybutyrate-producing Pseudomonas sp. isolated from Antarctic environments with high stress resistance (2004) Curr Microbiol, 49, pp. 170-174
  • Ayub, N.D., Tribelli, P.M., López, N.I., Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14-3 during low temperature adaptation (2009) Extremophiles, 13, pp. 59-66
  • Bernofsky, C., Swan, M., An improved cycling assay for nicotinamide adenine dinucleotide (1973) Anal Biochem, 53, pp. 452-458
  • Carmel-Harel, O., Storz, G., Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress (2000) Annu Rev Microbiol, 54, pp. 439-461
  • Cha, M.K., Kim, W.C., Lim, C.J., Kim, K., Kim, I.H., Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth (2004) J Biol Chem, 279, pp. 8769-8778
  • Cochran, W.L., McFeters, G.A., Stewart, P.S., Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine (2000) J Appl Microbiol, 88, pp. 22-30
  • de Lorenzo, V., Herrero, M., Jakubzik, U., Timmis, K.N., Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria (1990) J Bacteriol, 172, pp. 6568-6572
  • Eschbach, M., Schreiber, K., Trunk, K., Buer, J., Jahn, D., Schobert, M., Long-term anaerobic survival of the opportunistic pathogen Pseudomonas aeruginosa via pyruvate fermentation (2004) J Bacteriol, 186, pp. 4596-4604
  • Fernández-Piñar, R., Ramos, J.L., Rodríguez-Herva, J.J., Espinosa-Urgel, M., A two-component regulatory system integrates redox state and population density sensing in Pseudomonas putida (2008) J Bacteriol, 190, pp. 7666-7674
  • Fuhrer, T., Sauer, U., Different biochemical mechanisms ensure network-wide balancing of reducing equivalents in microbial metabolism (2009) J Bacteriol, 191, pp. 2112-2121
  • Galimand, M., Gamper, M., Zimmermann, A., Haas, D., Positive FNR-like control of anaerobic arginine degradation and nitrate respiration in Pseudomonas aeruginosa (1991) J Bacteriol, 173, pp. 1598-1606
  • Gibon, Y., Larher, F., Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium (1997) Anal Biochem, 251, pp. 153-157
  • Hishinuma, S., Yuki, M., Fujimura, M., Fukumori, F., OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida (2006) Environ Microbiol, 8, pp. 2115-2124
  • Horst, S.A., Jaeger, T., Denkel, L.A., Rouf, S.F., Rhen, M., Bange, F.C., Thiol peroxidase protects Salmonella enterica from hydrogen peroxide stress in vitro and facilitates intracellular growth (2010) J Bacteriol, 192, pp. 2929-2932
  • Huisman, G.W., Wonink, E., Meima, R., Kazemier, B., Terpstra, P., Witholt, B., Metabolism of poly(3-hydroxyalkanoates)(PHAs)by Pseudomonas oleovorans. Identification and sequences of genes and function of the encoded proteins in the synthesis and degradation of PHA (1991) J Biol Chem, 266, pp. 2191-2198
  • Jittawuttipoka, T., Buranajitpakorn, S., Vattanaviboon, P., Mongkolsuk, S., The catalase-peroxidase KatG is required for virulence of Xanthomonas campestris pv. campestris in a host plant by providing protection against low levels of H2O2 (2009) J Bacteriol, 191, pp. 7372-7377
  • Kadouri, D.E., Jurkevitch, E., Okon, Y., Castro-Sowinski, S., Ecological and agricultural significance of bacterial polyhydroxyalkanoates (2005) Crit Rev Microbiol, 31, pp. 55-67
  • Kawakami, T., Kuroki, M., Ishii, M., Igarashi, Y., Arai, H., Differential expression of multiple terminal oxidases for aerobic respiration in Pseudomonas aeruginosa (2010) Environ Microbiol, 12, pp. 1399-1412
  • Kim, E.J., Wang, W., Deckwer, W.D., Zeng, A.P., Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density (2005) Microbiology, 151, pp. 1127-1138
  • Lapaglia, C., Hartzell, P.L., Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus (1997) Appl Environ Microbiol, 63, pp. 3158-3163
  • Larionov, A., Krause, A., Miller, W., A standard curve based method for relative real time PCR data processing (2005) BMC Bioinformatics, 6, p. 62
  • López, N.I., Floccari, M.E., Garcia, A.F., Steinbüchel, A., Méndez, B.S., Effect of poly-3-hydroxybutyrate content on the starvation survival of bacteria in natural waters (1995) FEMS Microbiol Ecol, 16, pp. 95-101
  • López, N.I., Pettinari, M.J., Stackebrandt, E., Tribelli, P.M., Põtter, M., Steinbüchel, A., Méndez, B.S., Pseudomonas extremaustralis sp. nov., a poly(3-hydroxybutyrate)producer isolated from an Antarctic environment (2009) Curr Microbiol, 59, pp. 514-519
  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent (1951) J Biol Chem, 193, pp. 265-275
  • Lu, J., Yang, F., Li, Y., Zhang, X., Xia, B., Jin, C., Reversible conformational switch revealed by the redox structures of Bacillus subtilis thiol peroxidase (2008) Biochem Biophys Res Commun, 373, pp. 414-418
  • Mailloux, R.J., Lemire, J., Appanna, V.D., Metabolic networks to combat oxidative stress in Pseudomonas fluorescens (2011) Antonie Van Leeuwenhoek, 99, pp. 433-442
  • Martínez-Antonio, A., Collado-Vides, J., Identifying global regulators in transcriptional regulatory networks in bacteria (2003) Curr Opin Microbiol, 6, pp. 482-489
  • Mishra, S., Imlay, J., Why do bacteria use so many enzymes to scavenge hydrogen peroxide? (2012) Arch Biochem Biophys, 525, pp. 145-160
  • Nikel, P.I., Pettinari, M.J., Ramírez, M.C., Galvagno, M.A., Méndez, B.S., Escherichia coli arcA mutants: Metabolic profile characterization of microaerobic cultures using glycerol as a carbon source (2008) J Mol Microbiol Biotechnol, 15, pp. 48-54
  • O'Callaghan, J.F., Reen, F.J., Adams, C., O'Gara, F., Low oxygen induces the type III secretion system in Pseudomonas aeruginosa via modulation of the small RNAs rsmZ and rsmY (2011) Microbiology, 157, pp. 3417-3428
  • O'Callaghan, J.J., Reen, F.J., Adams, C., Casey, P.G., Gahan, C.G., O'Gara, F., A novel host-responsive sensor mediates virulence and type III secretion during Pseudomonas aeruginosa-host cell interactions (2012) Microbiology, 158, pp. 1057-1070
  • Panmanee, W., Gomez, F., Witte, D., Pancholi, V., Britigan, B.E., Hassett, D.J., The peptidoglycan-associated lipoprotein OprL helps protect a Pseudomonas aeruginosa mutant devoid of the transactivator OxyR from hydrogen peroxide-mediated killing during planktonic and biofilm culture (2008) J Bacteriol, 190, pp. 3658-3669
  • Partridge, J.D., Sanguinetti, G., Dibden, D.P., Roberts, R.E., Poole, R.K., Green, J., Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components (2007) J Biol Chem, 282, pp. 11230-11237
  • Quelas, J.I., López-García, S.L., Casabuono, A., Althabegoiti, M.J., Mongiardini, E.J., Pérez-Giménez, J., Couto, A., Lodeiro, A.R., Effects of N-starvation and C-source on Bradyrhizobium japonicum exopolysaccharide production and composition, and bacterial infectivity to soybean roots (2006) Arch Microbiol, 186, pp. 119-128
  • Ray, A., Williams, H.D., The effects of mutation of the anr gene on the aerobic respiratory chain of Pseudomonas aeruginosa (1997) FEMS Microbiol Lett, 156, pp. 227-232
  • Romeo, T., Gong, M., Liu, M.Y., Brun-Zinkernagel, A.M., Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties (1993) J Bacteriol, 175, pp. 4744-4755
  • Sabra, W., Kim, E.J., Zeng, A.P., Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures (2002) Microbiology, 148, pp. 3195-3202
  • Salunkhe, P., Töpfer, T., Buer, J., Tümmler, B., Genomewide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide (2005) J Bacteriol, 187, pp. 2565-2572
  • Schreiber, K., Krieger, R., Benkert, B., Eschbach, M., Arai, H., Schobert, M., Jahn, D., The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration (2007) J Bacteriol, 189, pp. 4310-4314
  • Somprasong, N., Jittawuttipoka, T., Duang-Nkern, J., Romsang, A., Chaiyen, P., Schweizer, H.P., Vattanaviboon, P., Mongkolsuk, S., Pseudomonas aeruginosa thiol peroxidase protects against hydrogen peroxide toxicity and displays atypical patterns of gene regulation (2012) J Bacteriol, 194, pp. 3904-3912
  • Sonnleitner, E., Gonzalez, N., Sorger-Domenigg, T., Heeb, S., Richter, A.S., Backofen, R., Williams, P., Bläsi, U., The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal (2011) Mol Microbiol, 80, pp. 868-885
  • Thomas, M., Nicklee, T., Hedley, D.W., Differential effects of depleting agents on cytoplasmic and nuclear non-protein sulphydryls: A fluorescence image cytometry study (1995) Br J Cancer, 72, pp. 45-50
  • Tolla, D.A., Savageau, M.A., Regulation of aerobic-to-anaerobic transitions by the FNR cycle in Escherichia coli (2010) J Mol Biol, 397, pp. 893-905
  • Trevelyan, W.E., Harrison, J.S., Studies on yeast metabolism. I. Fractionation and microdetermination of cell carbohydrate (1956) J Biochem, 63, pp. 23-24
  • Tribelli, P.M., Méndez, B.S., López, N.I., Oxygen-sensitive global regulator, Anr, is involved in the biosynthesis of poly(3-hydroxybutyrate)in Pseudomonas extremaustralis (2010) J Mol Microbiol Biotechnol, 19, pp. 180-188
  • Tribelli, P.M., Raiger Iustman, L.J., Catone, M.V., Di Martino, C., Revale, S., Méndez, B.S., López, N.I., Genome sequence of the polyhydroxybutyrate producer Pseudomonas extremaustralis, a highly stress-resistant Antarctic bacterium (2012) J Bacteriol, 194, pp. 2381-2382
  • Trunk, K., Benkert, B., Quäck, N., Münch, R., Scheer, M., Garbe, J., Jänsch, L., Wehland, J., Anaerobic adaptation in Pseudomonas aeruginosa: Definition of the Anr and Dnr regulons (2010) Environ Microbiol, 12, pp. 1719-1733. , & other authors
  • Ugidos, A., Morales, G., Rial, E., Williams, H.D., Rojo, F., The coordinate regulation of multiple terminal oxidases by the Pseudomonas putida ANR global regulator (2008) Environ Microbiol, 10, pp. 1690-1702
  • Wei, Q., Le Minh, P.N., Dötsch, A., Hildebrand, F., Panmanee, W., Elfarash, A., Schulz, S., Charlier, D., Global regulation of gene expression by OxyR in an important human opportunistic pathogen (2012) Nucleic Acids Res, 40, pp. 4320-4333. , & other authors


---------- APA ----------
Tribelli, P.M., Nikel, P.I., Oppezzo, O.J. & López, N.I. (2013) . Anr, the anaerobic global regulator, modulates the redox state and oxidative stress resistance in pseudomonas extremaustralis. Microbiology (United Kingdom), 159(2), 259-268.
---------- CHICAGO ----------
Tribelli, P.M., Nikel, P.I., Oppezzo, O.J., López, N.I. "Anr, the anaerobic global regulator, modulates the redox state and oxidative stress resistance in pseudomonas extremaustralis" . Microbiology (United Kingdom) 159, no. 2 (2013) : 259-268.
---------- MLA ----------
Tribelli, P.M., Nikel, P.I., Oppezzo, O.J., López, N.I. "Anr, the anaerobic global regulator, modulates the redox state and oxidative stress resistance in pseudomonas extremaustralis" . Microbiology (United Kingdom), vol. 159, no. 2, 2013, pp. 259-268.
---------- VANCOUVER ----------
Tribelli, P.M., Nikel, P.I., Oppezzo, O.J., López, N.I. Anr, the anaerobic global regulator, modulates the redox state and oxidative stress resistance in pseudomonas extremaustralis. Microbiology. 2013;159(2):259-268.