Proteomic insights into metabolic adaptations in Alcanivorax borkumensis induced by alkane utilization

Journal of Bacteriology

Volumn 188, Issue 11, 2006, Pages 3763-3773

  Sabirova, Julia S ^a,b   Ferrer, Manuel ^c   Regenhardt, Daniela ^a,d   Timmis, Kenneth N ^a,b   Golyshin, Peter N ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

^d INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKANE; BIOSURFACTANT; CARBON; CARDIOLIPIN; FATTY ACID; GLYOXYLIC ACID; HEXADECANE; HYDROCARBON; LIPOPROTEIN; PETROLEUM; PHOSPHOENOLPYRUVATE; POLYHYDROXYALKANOIC ACID; RIBOFLAVIN; UNSATURATED FATTY ACID; UNSPECIFIC MONOOXYGENASE;

ADAPTATION; ALCANIVORAX; ALCANIVORAX BORKUMENSIS; ALKB1 GENE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; CARBON STORAGE; FATTY ACID OXIDATION; GENE CLUSTER; GLUCONEOGENESIS; MEMBRANE STRUCTURE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS;

ADAPTATION, PHYSIOLOGICAL; ALKANES; BACTERIAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYMES; GENOME, BACTERIAL; HALOMONADACEAE; PROTEOME; PYRUVATES;

ALCANIVORAX BORKUMENSIS; BACTERIA (MICROORGANISMS);

EID: 33744762185     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00072-06     Document Type: Article

References (52)

1. Ahn, K. S., U. Ha, J. Jia, D. Wu, and S. Jin. 2004. The truA gene of Pseudomonas aeruginosa is required for the expression of type III secretory genes. Microbiology 150:539-547.
2. Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
3. Brooke, J. S., and M. A. Valvano. 1996. Molecular cloning of the Haemophilus influenzas gmhA (lpcA) gene encoding a phosphoheptose isomerase required for lipooligosaccharide biosynthesis. J. Bacteriol. 178:3339-3341.
4. Cardini, G., and P. Jurtshuk. 1968. Cytochrome P-450 involvement in the oxidation of n-octane b cell-free extracts of Corynebacterium sp. strain 7E1C. J. Biol. Chem. 243:6070-6072.
5. Chen, Q., D. B. Janssen, and B. Witholt. 1995. Growth on octane alters the membrane lipid fatty acids of Pseudomonas oleovorans due to the induction of alkB and synthesis of octanol. J. Bacteriol. 177:6894-6901.
6. Cowing, D. W., J. C. Bardwell, E. A. Craig, C. Woolford, R. W. Hendrix, and C. A. Gross. 1985. Consensus sequence for Escherichia coli heat shock gene promoters. Proc. Natl. Acad. Sci. USA 82:2679-2683.
7. Cronan, J. E., Jr., C. H. Birge, and P. R. Vagelos. 1969. Evidence for two genes specifically involved in unsaturated fatty acid biosynthesis in Escherichia coli. J. Bacteriol. 100:601-604.
8. Cryle, M. J., and J. J. de Voss. 2004. Carbon-carbon bond cleavage by cytochrome p450 (Biol) (CYP107H1). Chem. Commun. (Cambridge) 7:86-87.
9. Cubitto, M. A., and C. B. Cabezali. 2001. Typing and evaluation of hydrocarbon-degrading activity of a bacterial strain isolated from the Bahia Blanca estuary, Argentina. Rev. Argent. Microbiol. 33:141-148.
10. Dowhan, W. 1997. Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu. Rev. Biochem. 66:199-232.
11. Eggink, G., H. Engel, W. G. Meijer, J. Otten, J. Kingma, and B. Witholt. 1988. Structure and function of the regulatory locus AlkR. J. Biol. Chem. 263:13400-13405.
12. Eggink, G., R. G. Lageveen, B. Altenburg, and B. Witholt. 1987. Controlled and functional expression of the Pseudomonas oleovorans alkane utilizing system in Pseudomonas putida and Escherichia coli. J. Biol. Chem. 262: 17712-17718.
13. Espinosa-Urgel, M., C. Chamizo, and A. Tormo. 1996. A consensus structure for sigma S-dependent promoters. Mol. Microbiol. 21:657-659.
14. Filip, C., G. Fletcher, J. L. Wulff, and C. F. Earhart. 1973. Stabilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 115:717-722.
15. Fujii, T., T. Narikawa, K. Takeda, and J. Kalo. 2004. Biotransformation of various alkanes using the Escherichia coli expressing an alkane hydroxylase system from Gordonia sp. TF6. Biosci. Biotechnol. Biochem. 68:2171-2177.
16. Gensberg, K., A. W. Smith, F. S. Brinkman, and R. E. Hancock. 1999. Identification of oprG, a gene encoding a major outer membrane protein of Pseudomonas aeruginosa. J. Antimicrob. Chemother. 43:607-608.
17. Goodchild, A., N. F. Saunders, H. Ertan, M. Raffery, M. Guilhaus, P. M. Curmi, and R. Cavicchioli. 2004. A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol. Microbiol. 53:309-321.
18. Görg, A., W. Postel, C. Friedrich, R. Kuick, J. R. Strahler, and S. M. Hanash. 1991. Temperature-dependent spot positional variability in 2-dimensional polypeptide patterns. Electrophoresis 12:653-658.
19. Hale, J. E., J. P. Butler, M. D. Knierman, and G. W. Becker. 2000. Increased sensitivity of tryptic peptide detection by MALDI-TOF mass spectrometry is achieved by conversion of lysine to homoarginine. Anal. Biochem. 287:110-117.
20. Hara, A., S. H. Baik, K. Syutsubo, N. Misawa, T. H. Smits, J. B. van Beilen, and S. Harayama. 2004. Cloning and functional analysis of alkB genes in Alcanivorax borkumensis SK2. Environ. Microbiol. 6:191-197.
21. Harayama, S., H. Kishira, Y. Kasai, and K. Shutsubo. 1999. Petroleum biodegradation in marine environments. J. Mol. Microbiol. Biotechnol. 1:63-70.
22. Harley, C. B., and R. P. Reynolds. 1987. Analysis of E. coli promoter sequences. Nucleic Acids Res. 11:2343-2361.
23. Hoang, T. T., and H. P. Schweizer. 1997. Fatty acid biosynthesis in Pseudomonas aeruginosa: cloning and characterization of the fabAB operon encoding beta-hydroxyacyl-acyl carrier protein dehydratase (FabA) and beta-ketoacyl-acyl carrier protein synthase I (FabB). J. Bacteriol. 179:5326-5332.
24. Inouye, S., A. Nakazawa, and T. Nakazawa. 1987. Expression of the regulatory gene xylS on the TOL plasmid is positively controlled by the xylR gene product. Proc. Natl. Acad. Sci. USA 84:5182-5186.
25. Jensen, J. W., and J. S. Schutzbach. 1988. Modulation of dolichyl-phosphomannose synthase activity by changes in the lipid environment of the enzyme. Biochemistry 23:1115-1119.
26. Kasai, Y., H. Kishira, T. Sasaki, K. Syutsubo, K. Watanabe, and S. Harayama. 2002. Predominant growth of Alcanivorax strains in oil-contaminated and nutrient supplemented sea water. Environ. Microbiol. 4:141-147.
27. Kasai, Y., H. Kishira, K. Syutsubo, and S. Harayama. 2001. Molecular detection of marine bacterial populations on beaches contaminated by the Nakhodka tanker oil-spill accident. Environ. Microbiol. 3:246-255.
28. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
29. Kuiper, I., E. L. Lagendijk, R. Pickford, J. P. Derrick, G. E. Lamers, J. E. Thomas-Oates, B. J. Lugtenberg, and G. V. Bloemberg. 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.
30. Lebcault, J. M., E. T. Lode, and M. J. Coon. 1971. Fatty acid and hydrocarbon hydroxylation in yeast: role of cytochrome P-450 in Candida tropicalis. Biochem. Biophys. Res. Commun. 5:413-419.
31. Lindum, P. W., U. Anthoni, C. Christophersen, L. Eberl, S. Molin, and M. Givskov. 1998. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180:6384-6388.
32. Marin, M. M., T. H. Smits, J. B. van Beilen, and F. Rojo. 2001. The alkane hydroxylase gene of Burkholderia cepacia RR10 is under catabolite repression control. J. Bacteriol. 183:4202-4209.
33. Müller, R., O. Asperger, and H. P. Kleber. 1989. Purification of cytochrome P-450 from n-hexadecane-grown Acinetobacter calcoaceticus. Biomed. Biochim. Acta 48:243-254.
34. 2+-ATPaSe of sarcoplasmic reticulum. Biochemistry 23:130-135.
35. Nelson, D. R., T. Kamataki, D. Waxman, F. P. Guengerich, R. W. Estabrook, R. Feyereisen, F. J. Gonzalez, M. J. Coon, I. C. Gunsalus, and O. Gotoh. 1993. The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol. 12:1-51.
36. Ratajczak, A., W. Geissdorter, and W. Hillen. 1998. Alkane hydroxylase from Acinetobacter sp. strain ADP1 is encoded by alkM and belongs to a new family of bacterial integral-membrane hydrocarbon hydroxylases. Appl. Environ. Microbiol. 64:1175-1179.
37. Röling, W. F. M., M. G. Milner, D. M. Jones, F. Fratepietro, R. P. J. Swannell, F. Daniel, and I. M. Head. 2004. Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl. Environ. Microbiol. 70:2603-2613.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
39. Silbert, D. F., and P. R. Vagelos. 1967. Fatty acid mutant of E. coli lacking a beta-hydroxydecanoyl thioester dehydrase. Proc. Natl. Acad. Sci. USA 58: 1579-1586.
40. Smits, T. H., S. B. Balada, B. Witholt, and J. B. van Beilen. 2002. Functional analysis of alkane hydroxylases from gram-negative and gram-positive bacteria. J. Bacteriol. 184:1733-1742.
41. Smits, T. H. M., M. Röthlisberger, B. Witholt, and J. B. van Beilen. 1999. Molecular screening for alkane hydroxylase genes in gram-negative and gram-positive strains. Environ. Microbiol. 1:307-317.
42. Strocchi, M., M. Ferrer, K. N. Timmis, and P. N. Golyshin. 2005. Low temperature-induced systems failure in Escherichia coli: insights from rescue by cold-adapted chaperones. Proteomics 6:193-206.
43. Syutsubo, K., H. Kishira, and S. Harayama. 2001. Development of specific oligonucleotide probes for the identification and in situ detection of hydrocarbon-degrading Alcanivorax strains. Environ. Microbiol. 3:371-379.
44. Tokuda, H., and S. Matsuyma. 2004. Sorting of lipoproteins to the outer membrane in E. coli. Biochim. Biophys. Acta 11:1-3.
45. van Beilen, J. B., E. G. Funhoff, A. van Loon, A. Just, L. Kaysser, M. Bouza, R. Holtackers, M. Röthlisberger, Z. Li, and B. Witholt. 2006. Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl. Environ. Microbiol. 72:59-65.
46. van Beilen, J. B., M. M. Marin, T. H. Smits, M. Röthlisberger, A. G. Franchini, B. Witholt, and F. Rojo. 2004. Characterization of two alkane hydroxylase genes from the marine hydrocarbonoclastic bacterium Alcanivorax borkumensis. Environ. Microbiol. 6:264-273.
47. von Wallbrunn, A., H. J. Heipieper, and F. Meinhardt. 2002. Cis/trans isomerisation of unsaturated fatty acids in a cardiolipin synthase knock-out mutant of Pseudomonas putida P8. Appl. Microbiol. Biotechnol. 60:179-185.
48. Whyte, L. G., T. H. Smits, D. Labbe, B. Witholt, C. W. Greer, and J. B. van Beilen. 2002. Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococais strains Q15 and NRRL B-16531. Appl. Environ. Microbiol. 68:5933-5942.
49. Wissing, J., S. Heim, L. Flohe, U. Billitewski, and R. Frank. 2000. Enrichment of hydrophobic proteins via Triton X-114 phase partitioning and hydroxyapatite column chromatography for mass spectrometry. Electrophoresis 21:2589-2593.
50. Yakimov, M. M., P. N. Golyshin, S. Lang, E. R. Moore, W. R. Abraham, H. Lunsdort, and K. N. Timmis. 1998. Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int. J. Syst. Bacteriol. 48:339-348.
51. Yakimov, M. M., K. N. Timmis, V. Wray, and H. L. Fredrickson. 1995. Characterization of a new lipopeptide surfactant produced by thermotoler ant and halotolerant subsurface Bacillus licheniformis BASSO. Appl. Environ. Microbiol. 61:1706-1713.
52. Yates, J. M., G. Morris, and M. R. Brown. 1989. Effect of iron concentration and growth rate on the expression of protein G in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 49:259-262.