Pseudomonas putida response to cadmium: Changes in membrane and cytosolic proteomes

Journal of Proteome Research

Volumn 11, Issue 8, 2012, Pages 4169-4179

  Manara, Anna ^a   Dalcorso, Giovanni ^a   Baliardini, Cecilia ^a   Farinati, Silvia ^a   Cecconi, Daniela ^a   Furini, Antonella ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

cadmium; heavy metals; proteomics; Pseudomonas putida

Indexed keywords

CADMIUM; LEAD; PORIN; PROTEOME; ZINC;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOSOL; ENERGY RESOURCE; EXPOSURE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PSEUDOMONAS PUTIDA;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; CADMIUM; CELL MEMBRANE; CYTOPLASM; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION; METABOLIC NETWORKS AND PATHWAYS; MICROBIAL VIABILITY; PSEUDOMONAS PUTIDA; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); PSEUDOMONAS PUTIDA;

EID: 84864592893     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300281f     Document Type: Article

References (63)

1. Alloway, B. J.; Steinnes, E. Anthropogenic additions of cadmium to soils. In Cadmium in Soils and Plants; McLaughlin, M. J., Singh, B. R., Eds.; Kluwer Academic Publishers: Dordrecht, 1999; pp 97-123.
2. Shull, L. R. Non-technical summary: development of risk-based concentration for arsenic, cadmium, and lead in inorganic commercial fertilizers. Report prepared for the California Department of Food and Agriculture and the Heavy Metal Task Force. Newfield Inc.: West Sacramento, CA, 1998.
3. Hüttermann, A.; Arduini, I.; Godbold, D. L. Metal pollution and forest decline. In Heavy Metal Stress in Plants; Prasad, M. N. V., Hagemeyer, J., Eds.; Springer-Verlag: Berlin, 1999; pp 253-272.
4. Jin, Y. H.; Clark, A. B.; Slebos, R. J.; Al-Refai, H.; Taylor, J. A.; Kunkel, T. A.; Resnick, M. A.; Gordenin, D. A. Cadmium is a mutagen that acts by inhibiting mismatch repair Nat. Genet. 2003, 34, 326-329 (Pubitemid 36792867)
5. Banjerdkij, P.; Vattanaviboon, P.; Mongkolsuk, S. Exposure to cadmium elevated expression of genes in the OxyR and OhrR regulons and induces cross-resistance to peroxide killing treatment in Xanthomonas campestris Appl. Environ. Microbiol. 2005, 71, 1843-1849 (Pubitemid 40546102)
6. Nies, D. H. Efflux-mediated heavy metal resistance in prokaryotes FEMS Microbiol. Rev. 2003, 27, 313-339 (Pubitemid 36700434)
7. Ramos, J. L.; Gallegos, M. T.; Marqués, S.; Ramos-González, M. I.; Espinosa-Urgel, M.; Segura, A. Responses of Gram-negative bacteria to certain environmental stressors Curr. Opin. Microbiol. 2001, 4, 166-171 (Pubitemid 32294418)
8. Moore, C. M.; Helmann, J. D. Metal homeostasis in Bacillus subtilis Curr. Opin. Microbiol. 2005, 8, 188-195
9. Que, Q.; Helmann, J. D. Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins Mol. Microbiol. 2000, 35 (6) 1454-1468 (Pubitemid 30175521)
10. Moore, C. M.; Gaballa, A.; Hui, M.; Ye, R. W.; Helmann, J. D. Genetic and physiological responses of Bacillus subtilis to metal ion stress Mol. Microbiol. 2005, 57, 27-40 (Pubitemid 40896595)
11. Bourdineaud, J.-P.; Baudrimont, M.; Gonzalez, P.; Moreau, J.-L. Challenging the model for induction of metallothionein gene expression Biochemie 2006, 88, 1787-1792 (Pubitemid 44751342)
12. Ruíz, N.; Silhavy, T. J. Sensing external stress: watchdogs of the Escherichia coli cell envelope Curr. Opin. Microbiol. 2005, 8, 122-126 (Pubitemid 40417951)
13. Ramos, J. L.; Krell, T.; Daniels, C.; Segura, A.; Duque, E. Responses of Pseudomonas to small toxic molecules by a mosaic of domains Curr. Opin. Microbiol. 2009, 12, 215-220
14. Timmis, K. N. Pseudomonas putida: a cosmopolitan opportunist par excellence Environ. Microbiol. 2000, 4, 779-781 (Pubitemid 36064168)
15. Pardo, R.; Herguedas, M.; Barrado, E.; Vega, M. Biosorption of cadmium, copper, lead and zinc by inactive biomass of Pseudomonas putida Anal. Bioanal. Chem. 2003, 276, 26-32 (Pubitemid 40878069)
16. Tripathi, M.; Munot, H. P.; Shouche, Y.; Meyer, J. M.; Goel, R. Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9 Curr. Microbiol. 2005, 50 (5) 233-237 (Pubitemid 40875198)
17. Wu, X.; Monchy, S.; Taghavi, S.; Zhu, W.; Ramos, J.; van der Lelie, D. Comparative genomics and functional analysis of niche specific adaptation in Pseudomonas putida FEMS Microbiol. Rev. 2011, 35, 299-323
18. Cánovas, D.; Cases, I.; De Lorenzo, V. Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis Environ. Microbiol. 2003, 5, 1242-1256 (Pubitemid 38038937)
19. Miller, C. D.; Pettee, B.; Zhang, C.; Pabst, M.; McLean, J. E.; Anderson, A. J. Copper and cadmium: responses in Pseudomonas putida KT2440 Lett. Appl. Microbiol. 2009, 49, 775-783
20. Kiliç, N. K.; Stensballe, A.; Otzen, D. E.; Dönmez, G. Proteomic changes in response to chromium(VI) toxicity in Pseudomonas aeruginosa Bioresour. Technol. 2010, 101, 2134-2140
21. van Rossum, F.; Bonnin, I.; Fénart, S.; Pauwels, M.; Petit, D.; Saumitou-Laprade, P. Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species Mol. Ecol. 2004, 13, 2959-2967 (Pubitemid 39290223)
22. Farinati, S.; DalCorso, G.; Panigati, M.; Furini, A. Interaction between selected bacterial strains and Arabidopsis halleri modulates shoot proteome and cadmium and zinc accumulation J. Exp. Bot. 2011, 62, 3433-3447
23. Nelson, K. E.; Weinel, C.; Paulsen, I. T.; Dodson, R. J.; Hilbert, H.; Martins, dos Santos, V. A.; Fouts, D. E.; Gill, S. R.; Pop, M.; Holmes, M.; Brinkac, L.; Beanan, M.; DeBoy, R. T.; 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, J. A.; Timmis, K. N.; Düsterhöft, A.; Tümmler, B.; Fraser, C. M. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440 Environ. Microbiol. 2002, 4, 799-808 (Pubitemid 36064171)
24. Farinati, S.; DalCorso, G.; Bona, E.; Corbella, M.; Lampis, S.; Cecconi, D.; Polati, R.; Berta, G.; Vallini, G.; Furini, A. Proteomic analysis of Arabidopsis halleri shoots in response to the heavy metals cadmium and zinc and rhizosphere microorganisms Proteomics 2009, 9, 4837-4850
25. Weisburg, W. G.; Barns, S. M.; Pelletier, D. A.; Lane, D. J. 16S ribosomal DNA amplification for phylogenetic study J. Bacteriol. 1991, 173, 697-703
26. Altschul, S. F.; Madden, T. L.; Shaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25, 3389-3402 (Pubitemid 27359211)
27. Shevchenko, A.; Wilm., M.; Vorm, O; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68, 850-858
28. Fonseca, P.; Moreno, R.; Rojo, F. Genomic analysis of the role of RNase R in the turnover of Pseudomonas putida mRNAs J. Bacteriol. 2008, 190, 6258-6263
29. Rial, D.; Vázquez, J. A.; Murado, M. A. Effects of three heavy metals on the bacteria growth kinetics: a bivariate model for toxicological assessment Appl. Microbiol. Biotechnol. 2011, 90, 1095-1109
30. Sharma, S.; Sundaram, C. S.; Luthra, P. M.; Singh, Y.; Sirdeshmukh, R.; Gade, W. N. Role of proteins in resistance mechanism of Pseudomonas fluorescens against heavy metal induced stress with proteomics approach J. Biotechnol. 2006, 126, 374-382 (Pubitemid 44528785)
31. Conejo, M. C.; García, I.; Martínez-Martínez, L.; Picabea, L.; Pascual, A. Zinc eluted from siliconized latex urinary catheters decreases OprD expression, causing carbapenem resistance in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 2003, 47, 2313-2315 (Pubitemid 36753590)
32. Caille, O.; Rossier, C.; Perron, K. A Copper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa J. Bacteriol. 2007, 189, 4561-4568 (Pubitemid 47025567)
33. Lin, Y. M.; Wu, S. J.; Chang, T. W.; Wang, C. F.; Suen, C. S.; Hwang, M. J.; Chang, M. D. T.; Chen, Y. T.; Liao, Y. D. Outer membrane protein I of Pseudomonas aeruginosa is a target of cationic antimicrobial peptide/protein J. Biol. Chem. 2010, 285, 8985-8994
34. Hancock, R. E. W.; Brinkman, F. S. L. Function of Pseudomonas porins in uptake and efflux Annu. Rev. Microbiol. 2002, 56, 17-38 (Pubitemid 35217446)
35. Bodilis, J.; Barray, S. Molecular evolution of the major outer-membrane protein gene (oprF) of Pseudomonas Microbiology 2006, 152, 1075-1088
36. Roma-Rodrigues, C.; Pedro, M.; Santos, P. M.; Benndorf, D.; Rapp, E.; Sá-Correi, I. Response of Pseudomonas putida KT2440 to phenol at the level of membrane proteome J. Proteomics 2010, 73, 1461-1478
37. Rodriguez-Herva, J. J.; Ramos-Gonzalez, M. I.; Ramos, J. L. The Pseudomonas putida peptidoglycan-associated outer membrane lipoprotein is involved in maintenance of the integrity of the cell cell envelope J. Bacteriol. 1996, 178, 1699-1706 (Pubitemid 26085619)
38. Leedjärv, A.; Ivask, A.; Virta, M. Interplay of different transporters in the mediation of divalent heavy metal resistance in Pseudomonas putida KT2440 J. Bacteriol. 2008, 190, 2680-2689 (Pubitemid 351508168)
39. Rensing, C.; Pribyl, T.; Nies, D. H. New functions for the three subunits of the CzcCBA cation-proton antiporter J. Bacteriol. 1997, 179, 6871-6879 (Pubitemid 27492467)
40. Hu, N.; Zhao, B. Key genes involved in heavy-metal resistance in Pseudomonas putida CD2 FEMS Microbiol. Lett 2007, 267, 17-22 (Pubitemid 46066534)
41. Desai, P. J.; Garges, E.; Attardo Genco, C. Pathogenic Neisseriae can use hemoglobin, transferrin, and lactoferrin independently of the tonB locus J. Bacteriol. 2000, I, 5586-5591
42. Zhao, Q.; Poole, K. A second tonB gene in Pseudomonas aeruginosa is linked to the exbB and exbD genes FEMS Microbiol. Lett. 2000, 184, 127-132 (Pubitemid 30109592)
43. Boukhalfa, H.; Crumbliss, A. L. Chemical aspects of siderophore mediated iron transport Biometals 2002, 15, 325-339 (Pubitemid 35221353)
44. Guerinot, M. L. Microbial iron transport Annu. Rev. Microbiol. 1994, 48, 743-772 (Pubitemid 24334115)
45. Krewulak, K. A.; Vogel, H. J. TonB or not TonB: is that the question? Biochem. Cell Biol. 2011, 89, 87-97
46. Heim, S.; Ferrer, M.; Heuer, H.; Regenhardt, D.; Nimtz, M.; Timmis, K. N. 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 2003, 5, 1257-1269 (Pubitemid 38038938)
47. Dao, K. H. T.; Hamer, K. E.; Clark, C. L.; Harshman, L. G. Pyroverdine production by Pseudomonas aeruginosa exposed to metals or an oxidative stress agent Ecol. Appl. 1999, 9, 441-448 (Pubitemid 29221221)
48. Thompson, D. K.; Chourey, K.; Wickham, G. S.; Thieman, S. B.; VerBerkmoes, N. C.; Zhang, B.; McCarthy, A. T.; Rudisill, M. A.; Shah, M.; Hettich, R. L. Proteomics reveals a core molecular response of Pseudomonas putida F1 to acute chromate challenge BMC Genomics 2010, 11, 1-311
49. Dueholm, M. S.; Petersen, S. V.; Sønderkær, M.; Larsen, P.; Christiansen, G.; Hein, K. L.; Enghild, J. J.; Nielsen, J. L.; Nielsen, K. L.; Nielsen, P. H.; Otzen, D. E. Functional amyloid in Pseudomonas Mol. Microbiol. 2010, 77, 1009-1020
50. Popova, O. B.; Sanina, N. M.; Likhatskaya, G. N.; Bezverbnaya, I. P. Effects of copper and cadmium ions on the physicochemical properties of lipids of the marine bacterium Pseudomonas putida IB28 at different growth temperatures Russ. J. Mar. Biol. 2008, 34, 179-185 (Pubitemid 352016152)
51. Lai, C. Y.; Cronan, J. E. Isolation and Characterization of β-ketoacyl-acyl carrier protein reductase (fabG) mutants of Escherichia coli and Salmonella enterica Serovar Typhimurium J. Bacteriol. 2004, 1869-1878 (Pubitemid 38314532)
52. Göthel, S. F.; Marahiel, M. A. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts Cell. Mol. Life Sci. 1999, 55, 423-436 (Pubitemid 29178881)
53. Dartigalongue, C.; Raina, S. A new heat-shock gene, ppiD, encodes a peptidyl- prolyl isomerase required for folding of outer membrane proteins in Escherichia coli EMBO J. 1998, 17, 3968-3980 (Pubitemid 28333982)
54. Lakshmipathy, S. K.; Gupta, R.; Pinkert, S.; Etchells, S. A.; Hart, F. U. Versatility of trigger factor interactions with ribosome-nascent chain complexes J. Biol. Chem. 2010, 285, 27911-27923
55. Gottesman, S. Proteolysis in bacterial regulatory circuits Annu. Rev. Cell Dev. Biol. 2003, 19, 565-587 (Pubitemid 37487361)
56. Porankiewicz, J.; Wang, J.; Clarke, A. K. New insights into the ATP-dependent Clp protease: Escherichia coli and beyond Mol. Microbiol. 1999, 32, 449-458 (Pubitemid 29233891)
57. Braun, M.; Silhavy, T. J. Imp/OstA is required for cell envelope biogenesis in Escherichia coli Mol. Microbiol. 2002, 45, 1289-1302 (Pubitemid 35015353)
58. Aono, R.; Negishi, T.; Nakajima, H. Cloning of organic solvent tolerance gene ostA that determiners n-hexane tolerance level in Escherichia coli Appl. Environ. Microbiol. 1994, 60, 4626-4626
59. McEldowney, S. Effect of cadmium and zinc on attachment and detachment interactions of Pseudomonas fluorescens H2 with glass Appl. Environ. Microbiol. 1994, 60, 2759-2765 (Pubitemid 24242266)
60. Shitashiro, M.; Kato, J.; Fukumura, T.; Kuroda, A.; Ikeda, T.; Takiguchi, N.; Ohtake, H. Evaluation of bacterial aerotaxis for its potential use in detecting the toxicity of chemicals to microorganisms J. Biotechnol. 2003, 101, 11-18 (Pubitemid 36071446)
61. Geszvain, K.; Yamaguchi, A.; Maybee, J.; Tebo, B. M. Mn(II) oxidation in Pseudomonas putida GB-1 is influenced by flagella synthesis and surface substrate Arch. Microbiol. 2011, 193, 605-614
62. Chen., L.; Xie, Q. W.; Nathan, C. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates Mol. Cell 1998, 1, 795-805 (Pubitemid 128379064)
63. Mongkolsuk, S.; Loprasert, S.; Whangsuk, W.; Fuangthong, M.; Atichartpongkun, S. Characterization of transcription organization and analysis of unique expression patterns of an alkyl hydroperoxide reductase C gene (ahpC) and the peroxide regulator operon ahpF-oxyR-orfX from Xanthomonas campestris pv. phaseoli J. Bacteriol. 1997, 179, 3950-3955 (Pubitemid 27259914)