1887

Abstract

CA-3 is a styrene-degrading bacterium capable of accumulating medium-chain-length polyhydroxyalkanoate (mclPHA) when exposed to limiting concentrations of a nitrogen source in the growth medium. Using shotgun proteomics we analysed global proteome expression in CA-3 supplied with styrene as the sole carbon and energy source under N-limiting (condition permissive for mclPHA synthesis) and non-limiting (condition non-permissive for mclPHA accumulation) growth conditions in order to provide insight into the molecular response of CA-3 to limitation of nitrogen when grown on styrene. A total of 1761 proteins were identified with high confidence and the detected proteins could be assigned to functional groups including styrene degradation, energy, nucleotide metabolism, protein synthesis, transport, stress response and motility. Proteins involved in the upper and lower styrene degradation pathway were expressed throughout the 48 h growth period under both nitrogen limitation and excess. Proteins involved in polyhydroxyalkanoate (PHA) biosynthesis, nitrogen assimilation and amino acid transport, and outer membrane proteins were upregulated under nitrogen limitation. PHA accumulation and biosynthesis were only expressed under nitrogen limitation. Nitrogen assimilation proteins were detected on average at twofold higher amounts under nitrogen limitation. Expression of the branched-chain amino acid ABC transporter was up to 16-fold higher under nitrogen-limiting conditions. Branched chain amino acid uptake by nitrogen-limited cultures was also higher than that by non-limited cultures. Outer membrane lipoproteins were expressed at twofold higher levels under nitrogen limitation. This was confirmed by Western blotting (immunochemical detection) of cells grown under nitrogen limitation. Our study provides the first global description of protein expression changes during growth of any organism on styrene and accumulating mclPHA (nitrogen-limited growth).

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.031153-0
2009-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/10/3348.html?itemId=/content/journal/micro/10.1099/mic.0.031153-0&mimeType=html&fmt=ahah

References

  1. Adler J. 1966; Chemotaxis in bacteria. Science 153:708–715
    [Google Scholar]
  2. Arias S., Olivera E. R., Arcos M., Naharro G., Luengo J. M. 2008; Genetic analyses and molecular characterization of the pathways involved in the conversion of 2-phenylethylamine and 2-phenylethanol into phenylacetic acid in Pseudomonas putida U. Environ Microbiol 10:413–432
    [Google Scholar]
  3. Bartolomé-Martin D., Martinez-Garcia E., Mascaraque V., Rubio J., Perera J., Alonso S. 2004; Characterization of a second functional gene cluster for the catabolism of phenylacetic acid in Pseudomonas sp. strain Y2. Gene 341:167–179
    [Google Scholar]
  4. Beltrametti F., Marconi A. M., Bestetti G., Colombo C., Galli E., Ruzzi M., Zennaro E. 1997; Sequencing and functional analysis of styrene catabolism genes from Pseudomonas fluorescens ST. Appl Environ Microbiol 63:2232–2239
    [Google Scholar]
  5. 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
    [Google Scholar]
  6. Brandl H., Gross R. A., Lenz R. W., Fuller R. C. 1988; Pseudomonas oleovorans as a source of poly( β-hydroxyalkanoates) for potential applications as biodegradable polyesters. Appl Environ Microbiol 54:1977–1982
    [Google Scholar]
  7. Cagney G., Park S., Chung C., Tong B., O'Dushlaine C., Shields D. C., Emili A. 2005; Human tissue profiling with multidimensional protein identification technology. J Proteome Res 4:1757–1767
    [Google Scholar]
  8. Chen S., Bleam W. F., Hickey W. J. 2009; Simultaneous analysis of bacterioferritin gene expression and intracellular iron status in Pseudomonas putida KT2440 by using a rapid dual luciferase reporter assay. Appl Environ Microbiol 75:866–868
    [Google Scholar]
  9. Cowell B. A., Willcox M. D. P., Herbert B., Schneider R. P. 1999; Effect of nutrient limitation on adhesion characteristics of Pseudomonas aeruginosa . J Appl Microbiol 86:944–954
    [Google Scholar]
  10. Craig R., Beavis R. C. 2004; TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20:1466–1467
    [Google Scholar]
  11. del Peso-Santos T., Bartolomé-Martin D., Fernandez C., Alonso S., Garcia J. L., Diaz E., Shingler V., Perera J. 2006; Coregulation by phenylacetyl-coenzyme A-responsive PaaX integrates control of the upper and lower pathways for catabolism of styrene by Pseudomonas sp. strain Y2. J Bacteriol 188:4812–4821
    [Google Scholar]
  12. del Peso-Santos T., Shingler V., Perera J. 2008; The styrene-responsive StyS/StyR regulation system controls expression of an auxiliary phenylacetyl-coenzyme A ligase: implications for rapid metabolic coupling of the styrene upper- and lower-degradative pathways. Mol Microbiol 69:317–330
    [Google Scholar]
  13. Ferenci T. 1999; Regulation by nutrient limitation. Curr Opin Microbiol 2:208–213
    [Google Scholar]
  14. Flynn J. M., Neher S. B., Kim Y. I., Sauer R. T., Baker T. A. 2003; Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell 11:671–683
    [Google Scholar]
  15. Goff M., Ward P. G., O'Connor K. E. 2007; Improvement of the conversion of polystyrene to polyhydroxyalkanoate through the manipulation of the microbial aspect of the process: a nitrogen feeding strategy for bacterial cells in a stirred tank reactor. J Biotechnol 132:283–286
    [Google Scholar]
  16. Goff M., Nikodinovic-Runic J., O'Connor K. 2009; Characterisation of temperature sensitive and lipopolysaccharide over-producing transposon mutants of Pseudomonas putida CA-3 affected in PHA accumulation. FEMS Microbiol Lett 292:297–305
    [Google Scholar]
  17. Grimm A. C., Harwood C. S. 1997; Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene. Appl Environ Microbiol 63:4111–4115
    [Google Scholar]
  18. Guyard-Nicodème M., Bazire A., Hemery G., Meylheuc T., Mollé D., Orange N., Fito-Boncompte L., Feuilloley M., Haras D. other authors 2008; Outer membrane modifications of Pseudomonas fluorescens MF37 in response to hyperosmolarity. J Proteome Res 7:1218–1225
    [Google Scholar]
  19. Hancock R. E., Brinkman F. S. 2002; Function of Pseudomonas porins in uptake and efflux. Annu Rev Microbiol 56:17–38
    [Google Scholar]
  20. Harwood C. S., Parales R. E., Dispensa M. 1990; Chemotaxis of Pseudomonas putida toward chlorinated benzoates. Appl Environ Microbiol 56:1501–1503
    [Google Scholar]
  21. Heipieper H. J., Meulenbeld G., van Oirschot Q., de Bont J. A. M. 1996; Effect of environmental factors on the trans/ cis ratio of unsaturated fatty acids in Pseudomonas putida S12. Appl Environ Microbiol 62:2773–2777
    [Google Scholar]
  22. Hoffmann N., Rehm B. H. A. 2005; Nitrogen-dependent regulation of medium-chain length polyhydroxyalkanoate biosynthesis genes in pseudomonads. Biotechnol Lett 27:279–282
    [Google Scholar]
  23. Junker F., Ramos J. L. 1999; Involvement of the cis/ trans isomerase Cti in solvent resistance of Pseudomonas putida DOT-T1E. J Bacteriol 181:5693–5700
    [Google Scholar]
  24. Kang Z., Wang Q., Zhang H., Qi Q. 2008; Construction of a stress-induced system in Escherichia coli for efficient polyhydroxyalkanoates production. Appl Microbiol Biotechnol 79:203–208
    [Google Scholar]
  25. Keller A., Nesvizhskii A. I., Kolker E., Aebersold R. 2002; Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383–5392
    [Google Scholar]
  26. Kieboom J., De Bont J. A. M. 2001; Identification and molecular characterization of an efflux system involved in Pseudomonas putida S12 multidrug resistance. Microbiology 147:43–51
    [Google Scholar]
  27. Kieboom J., Dennis J. J., Zylstra G. J., De Bont J. A. M. 1998; Active efflux of organic solvents by Pseudomonas putida S12 is induced by solvents. J Bacteriol 180:6769–6772
    [Google Scholar]
  28. Kim Y. H., Cho K., Yun S.-H., Kim J. Y., Kwon K.-H., Yoo J. S., Kim S. I. 2006; Analysis of aromatic catabolic pathways in Pseudomonas putida KT 2440 using a combined proteomic approach: 2-DE/MS and cleavable isotope-coded affinity tag analysis. Proteomics 6:1301–1318
    [Google Scholar]
  29. Kragelund L., Nybroe O. 1994; Culturability and expression of outer membrane proteins during carbon, nitrogen, or phosphorus starvation of Pseudomonas fluorescens DF57 and Pseudomonas putida DF14. Appl Environ Microbiol 60:2944–2948
    [Google Scholar]
  30. 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
    [Google Scholar]
  31. Kuiper I., Lagendijk E. L., Pickford R., Derrick J. P., Lamers G. E. M., Thomas-Oates J. E., Lugtenberg B. J. J., Bloemberg G. V. 2004; Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51:97–113
    [Google Scholar]
  32. Lageveen R. G., Huisman G. W., Preusting H., Ketelaar P., Eggink G., Witholt B. 1988; Formation of polyesters by Pseudomonas oleovorans: effect of substrates on formation and composition of poly-( R)-3-hydroxyalkanoates and poly-( R)-3-hydroxyalkenoates. Appl Environ Microbiol 54:2924–2932
    [Google Scholar]
  33. Lavallee B., Lessard P., Vanrolleghem P. A. 2005; Review of procaryote metabolism in view of modeling microbial adaptation from fast growth to starvation conditions. J Environ Eng Sci 4:517–532
    [Google Scholar]
  34. Law A. M. J., Aitken M. D. 2006; The effect of oxygen on chemotaxis to naphthalene by Pseudomonas putida G7. Biotechnol Bioeng 93:457–464
    [Google Scholar]
  35. Li L., Komatsu T., Inoue A., Horikoshi K. 1995; A toluene-tolerant mutant of Pseudomonas aeruginosa lacking the outer membrane protein F. Biosci Biotechnol Biochem 59:2358–2359
    [Google Scholar]
  36. Liu H., Sadygov R. G., Yates J. R. I. 2004; A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76:4193–4201
    [Google Scholar]
  37. Lu C.-D., Itoh Y., Nakada Y., Jiang Y. 2002; Functional analysis and regulation of the divergent spuABCDEFGH- spuI operons for polyamine uptake and utilization in Pseudomonas aeruginosa PAO1. J Bacteriol 184:3765–3773
    [Google Scholar]
  38. Lu X., Li L., Wu R., Feng X., Li Z., Yang H., Wang C., Guo H., Galkin A. other authors 2006; Kinetic analysis of Pseudomonas aeruginosa arginine deiminase mutants and alternate substrates provides insight into structural determinants of function. Biochemistry 45:1162–1172
    [Google Scholar]
  39. Luengo J. M., Garcia J. L., Olivera E. R. 2001; The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications. Mol Microbiol 39:1434–1442
    [Google Scholar]
  40. Luengo J. M., Arias S., Sandoval A., Arias-Barrau E., Arcos M., Naharro G., Olivera E. R. 2004; From aromatics to bioplastics: the phenylacetyl-CoA catabolon as a model of catabolic convergence. Rec Res Dev Bioph Biochem 4:257–292
    [Google Scholar]
  41. Martinez-Blanco H., Reglero A., Rodriguez-Aparicio L. B., Luengo J. M. 1990; Purification and biochemical characterization of phenylacetyl-CoA ligase from Pseudomonas putida: a specific enzyme for the catabolism of phenylacetic acid. J Biol Chem 265:7084–7090
    [Google Scholar]
  42. Miyamoto S., Tokuda H. 2007; Diverse effects of phospholipids on lipoprotein sorting and ATP hydrolysis by the ABC transporter LolCDE complex. Biochim Biophys Acta 17681848–1854
    [Google Scholar]
  43. Mooney A., O'Leary N. D., Dobson A. D. 2006a; Cloning and functional characterization of the styE gene, involved in styrene transport in Pseudomonas putida CA-3. Appl Environ Microbiol 72:1302–1309
    [Google Scholar]
  44. Mooney A., Ward P. G., O'Connor K. 2006b; Microbial degradation of styrene: biochemistry, molecular genetics, and perspectives for biotechnological applications. Appl Microbiol Biotechnol 72:1–10
    [Google Scholar]
  45. Narita S.-i., Tokuda H. 2006; An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett 580:1164–1170
    [Google Scholar]
  46. 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. other authors 2002; Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808
    [Google Scholar]
  47. Neuwald A. F., Aravind L., Spouge J. L., Koonin E. V. 1999; A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43
    [Google Scholar]
  48. Nogales J., Macchi R., Franchi F., Barzaghi D., Fernandez C., García J. L., Bertoni G., Díaz E. 2007; Characterization of the last step of the aerobic phenylacetic acid degradation pathway. Microbiology 153:357–365
    [Google Scholar]
  49. O'Connor K., Buckley C. M., Hartmans S., Dobson A. D. W. 1995; Possible regulatory role for nonaromatic carbon sources in styrene degradation by Pseudomonas putida CA-3. Appl Environ Microbiol 61:544–548
    [Google Scholar]
  50. O'Connor K. E., Duetz W., Wind B., Dobson A. D. W. 1996; The effect of nutrient limitation on styrene metabolism in Pseudomonas putida CA-3. Appl Environ Microbiol 62:3594–3599
    [Google Scholar]
  51. O'Connor K. E., Witholt B., Duetz W. 2001; p-Hydroxyphenylacetic acid metabolism in Pseudomonas putida F6. J Bacteriol 183:928–933
    [Google Scholar]
  52. O'Leary N. D., O'Connor K. E., Duetz W., Dobson A. D. W. 2001; Transcriptional regulation of styrene degradation in Pseudomonas putida CA-3. Microbiology 147:973–979
    [Google Scholar]
  53. O'Leary N. D., Duetz W. A., Dobson A. D., O'Connor K. E. 2002a; Induction and repression of the sty operon in Pseudomonas putida CA-3 during growth on phenylacetic acid under organic and inorganic nutrient-limiting continuous culture conditions. FEMS Microbiol Lett 208:263–268
    [Google Scholar]
  54. O'Leary N. D., O'Connor K. E., Dobson A. D. W. 2002b; Biochemistry, genetics and physiology of microbial styrene degradation. FEMS Microbiol Rev 26:403–417
    [Google Scholar]
  55. O'Leary N. D., O'Connor K. E., Ward P., Goff M., Dobson A. D. W. 2005; Genetic characterization of accumulation of polyhydroxyalkanoate from styrene in Pseudomonas putida CA-3. Appl Environ Microbiol 71:4380–4387
    [Google Scholar]
  56. Olivera E. R., Minambres B., Garcia B., Muntiz C., Moreno M. A., Ferrandez A., Diaz E., Garcia J. L., Luengo J. M. 1998; Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-CoA catabolon. Proc Natl Acad Sci U S A 95:6419–6424
    [Google Scholar]
  57. O'Toole G. A., Kolter R. 1998; Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461
    [Google Scholar]
  58. Park S. J., Lee S. Y. 2005; Systems biological approach for the production of various polyhydroxyalkanoates by metabolically engineered Escherichia coli . Macromol Symp 224:1–10
    [Google Scholar]
  59. Park J. H., Lee S. Y., Kim T. Y., Kim H. U. 2008; Application of systems biology for bioprocess development. Trends Biotechnol 26:404–412
    [Google Scholar]
  60. Patel C. N., Wortham B. W., Lines J. L., Fetherston J. D., Perry R. D., Oliveira M. A. 2006; Polyamines are essential for the formation of plague biofilm. J Bacteriol 188:2355–2363
    [Google Scholar]
  61. Patrauchan M. A., Sarkisova S. A., Franklin M. J. 2007; Strain-specific proteome responses of Pseudomonas aeruginosa to biofilm-associated growth and to calcium. Microbiology 153:3838–3851
    [Google Scholar]
  62. Pötter M., Steinbüchel A. 2005; Poly(3-hydroxybutyrate) granule-associated proteins: impacts on poly(3-hydroxybutyrate) synthesis and degradation. Biomacromolecules 6:552–560
    [Google Scholar]
  63. Pötter M., Muller H., Reinecke F., Wieczorek R., Fricke F., Bowien B., Friedrich B., Steinbüchel A. 2004; The complex structure of polyhydroxybutyrate (PHB) granules: four orthologous and paralogous phasins occur in Ralstonia eutropha . Microbiology 150:2301–2311
    [Google Scholar]
  64. Raberg M., Reinecke F., Reichelt R., Malkus U., König S., Pötter M., Fricke W. F., Pohlmann A., Voigt B. other authors 2008; Ralstonia eutropha H16 flagellation changes according to nutrient supply and state of poly(3-hydroxybutyrate) accumulation. Appl Environ Microbiol 74:4477–4490
    [Google Scholar]
  65. Raghava G. P. S. 2006; MANGO: prediction of Genome Ontology (GO) class of a protein from its amino acid and dipeptide composition using nearest neighbor approach. CASP7 93
    [Google Scholar]
  66. Ramos J. L., Gallegos M.-T., Marqués S., Ramos-González M.-I., Espinosa-Urgel M., Segura A. 2001; Responses of Gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 4:166–171
    [Google Scholar]
  67. Ramos J. L., Duque E., Gallegos M.-T., Godoy P., Ramos-González M. I., Rojas A., Terán W., Segura A. 2002; Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56:743–768
    [Google Scholar]
  68. Ramos-Gonzalez M.-I., Ruiz-Cabello F., Brettrar I., Garrido F., Ramos J. L. 1992; Tracking genetically engineered bacteria: monoclonal antibodies against surface determinants of the soil bacterium Pseudomonas putida 2440. J Bacteriol 174:2978–2985
    [Google Scholar]
  69. Rehm B. H. 2007; Biogenesis of microbial polyhydroxyalkanoate granules: a platform technology for the production of tailor-made bioparticles. Curr Issues Mol Biol 9:41–62
    [Google Scholar]
  70. Sandoval A., Arias-Barrau E., Arcos M., Naharro G., Olivera E. R., Luengo J. M. 2007; Genetic and ultrastructural analysis of different mutants of Pseudomonas putida affected in the poly-3-hydroxy-n-alkanoate gene cluster. Environ Microbiol 9:737–751
    [Google Scholar]
  71. Santos P. M., Benndorf D., Sa-Correia I. 2004; Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics. Proteomics 4:2640–2652
    [Google Scholar]
  72. Santos P. M., Roma V., Benndorf D., von Bergen M., Harms H., Sa-Correia I. 2007; Mechanistic insights into the global response to phenol in the phenol-biodegrading strain Pseudomonas sp. M1 revealed by quantitative proteomics. OMICS 11:233–251
    [Google Scholar]
  73. Scheiner D. 1976; Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10:31–36
    [Google Scholar]
  74. Schlegel H. G., Kaltwasser H., Gottschalk G. 1961; A submersion method for culture of hydrogen-oxidizing bacteria: growth physiological studies. Arch Mikrobiol 38:209–222 in German
    [Google Scholar]
  75. Shevchenko A., Wilm M., Vorm O., Mann M. 1996; Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858
    [Google Scholar]
  76. Smith J. L. 2004; The physiological role of ferritin-like compounds in bacteria. Crit Rev Microbiol 30:173–185
    [Google Scholar]
  77. Sobolevsky T. G., Revelsky A. I., Revelsky I. A., Miller B., Oriedo V. 2004; Simultaneous determination of fatty, dicarboxylic and amino acids based on derivatization with isobutyl chloroformate followed by gas chromatography-positive ion chemical ionization mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 800:101–107
    [Google Scholar]
  78. Squires C., Squires C. L. 1992; The Clp proteins: proteolysis regulators or molecular chaperones?. J Bacteriol 174:1081–1085
    [Google Scholar]
  79. Taylor M., Tuffin M., Burton S., Eley K., Cowan D. 2008; Microbial responses to solvent and alcohol stress. Biotechnol J 3:1388–1397
    [Google Scholar]
  80. Tessmer N., Konig S., Malkus U., Reichelt R., Pötter M., Steinbuchel A. 2007; Heat-shock protein HspA mimics the function of phasins sensu stricto in recombinant strains of Escherichia coli accumulating polythioesters or polyhydroxyalkanoates. Microbiology 153:366–374
    [Google Scholar]
  81. Velasco A., Alonso S., Garcıa J. L., Perera J., Diaz E. 1998; Genetic and functional analysis of the styrene catabolic cluster of Pseudomonas sp. strain Y2. J Bacteriol 180:1063–1071
    [Google Scholar]
  82. VerBerkmoes N. C., Shah M. B., Lankford P. K., Pelletier D. A., Strader M. B., Tabb D. L., McDonald W. H., Barton J. W., Hurst G. B. other authors 2006; Determination and comparison of the baseline proteomes of the versatile microbe Rhodopseudomonas palustris under its major metabolic states. J Proteome Res 5:287–298
    [Google Scholar]
  83. Volker U., Engelmann S., Maul B., Roethdorf S., Voelker A., Schmid R. 1994; Analysis of the induction of stress proteins of Bacillus subtilis . Microbiology 140:741–752
    [Google Scholar]
  84. Volkers R. J. M., de Jong A. L., Hulst A. G., van Baar B. L. M., de Bont J. A. M., Wery J. 2006; Chemostat-based proteomic analysis of toluene-affected Pseudomonas putida S12. Environ Microbiol 8:1674–1679
    [Google Scholar]
  85. von Wallbrunn A., Richnow H. H., Neumann G., Meinhardt F., Heipieper H. J. 2003; Mechanism of cis–trans isomerization of unsaturated fatty acids in Pseudomonas putida . J Bacteriol 185:1730–1733
    [Google Scholar]
  86. Wältermann M., Steinbüchel A. 2005; Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187:3607–3619
    [Google Scholar]
  87. Ward P. G., O'Connor K. E. 2005; Induction and quantification of phenylacyl-CoA ligase enzyme activities in Pseudomonas putida CA-3 grown on aromatic carboxylic acids. FEMS Microbiol Lett 251:227–232
    [Google Scholar]
  88. Ward P. G., de Roo G., O'Connor K. E. 2005; Accumulation of polyhydroxyalkanoate from styrene and phenylacetic acid by Pseudomonas putida CA-3. Appl Environ Microbiol 71:2046–2052
    [Google Scholar]
  89. Ward P. G., Goff M., Donner M., Kaminsky W., O'Connor K. E. 2006; A two step chemo-biotechnological conversion of polystyrene to a biodegradable thermoplastic. Environ Sci Technol 40:2433–2437
    [Google Scholar]
  90. Washburn M. P., Ulaszek R. R., Yates J. R. I. 2003; Reproducibility of quantitative proteomic analyses of complex biological mixtures by multi-dimensional protein identification technology. Anal Chem 75:5054–5061
    [Google Scholar]
  91. Welinder K. G. 1991; Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily. Biochim Biophys Acta 1080:215–220
    [Google Scholar]
  92. Whang L.-M., Liu P.-W. G., Ma C.-C., Cheng S.-S. 2008; Application of biosurfactants, rhamnolipid, and surfactin, for enhanced biodegradation of diesel-contaminated water and soil. J Hazard Mater 151:155–163
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.031153-0
Loading
/content/journal/micro/10.1099/mic.0.031153-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error