Possible involvement of an extracellular superoxide dismutase (SodA) as a radical scavenger in poly(cis-1,4-isoprene) degradation

Applied and Environmental Microbiology

Volumn 74, Issue 24, 2008, Pages 7643-7653

  Schulte, Carina ^a   Arenskötter, Matthias ^a   Berekaa, Mahmoud M ^a   Arenskötter, Quyen ^a   Priefert, Horst ^a   Steinbüchel, Alexander ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINATION; AMINES; AMINO ACIDS; CELL CULTURE; DEGRADATION; ENZYMES; ESCHERICHIA COLI; GROWTH (MATERIALS); MANGANESE; METAL REFINING; ORGANIC ACIDS; OXYGEN; PROTEINS; SILICA; SILICATE MINERALS;

AEROBIC GROWTHS; ANTIBODY DETECTIONS; DOUBLE MUTANTS; ENERGY SOURCES; EXTRACELLULAR; EXTRACELLULAR SUPEROXIDE DISMUTASE; GORDONIA; MATURE PROTEINS; MICROCOCCUS LUTEUS; MINERAL SALTS; MYCOBACTERIUM SMEGMATIS; OPTIMAL GROWTHS; OXIDATIVE DAMAGES; PRESENCE OF WATERS; RADICAL SCAVENGERS; REACTIVE OXYGEN INTERMEDIATES; SOD ACTIVITIES; SOLE CARBONS; SOLUBLE SUBSTRATES; SUPERNATANTS; TERMINAL SEQUENCES; WILD TYPES;

ENZYME ACTIVITY;

SCAVENGER; SUPEROXIDE DISMUTASE;

AMINO ACID; ANTIBODY; BIODEGRADATION; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GENE EXPRESSION; GROWTH RATE; MANGANESE; MUTATION; PEPTIDE; RADICAL; RECOMBINATION; SCAVENGING (CHEMISTRY);

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; DEGRADATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE DISRUPTION; GENE EXPRESSION; GORDONIA; MICROCOCCUS LUTEUS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

ACTINOMYCETALES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CULTURE MEDIA; DNA, BACTERIAL; ESCHERICHIA COLI; FREE RADICALS; GENE DELETION; GENETIC COMPLEMENTATION TEST; HEMITERPENES; LATEX; MICROCOCCUS LUTEUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MYCOBACTERIUM SMEGMATIS; OXIDANTS; PARAQUAT; SEQUENCE HOMOLOGY, AMINO ACID; SUPEROXIDE DISMUTASE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GORDONIA POLYISOPRENIVORANS; GORDONIA WESTFALICA; MICROCOCCUS LUTEUS; MYCOBACTERIUM SMEGMATIS;

EID: 57449112526     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01490-08     Document Type: Article

References (58)

1. Alamuri, P., and R. J. Maier. 2006. Methionine sulfoxide reductase in Heliobacter pylori: interaction with methionine-rich proteins and stress-induced expression. J. Bacteriol. 188:5839-5850.
2. Alcendor, D. J., G. D. Chapman, and B. L. Beaman. 1995. Isolation, sequencing and expression of the superoxide dismutase-encoding gene (sod) of Nocardia asteroides strain GUH-2. Gene 164:143-147.
3. Almiron, M., A. Link, D. Furlong, and R. Kolter. 1992. A novel DNA binding protein with regulatory and protective roles in starved E. coli. Genes Dev. 6:2646-2654.
4. Arenskötter, M., D. Baumeister, R. Kalscheuer, and A. Steinbüchel. 2003. Identification and application of plasmids suitable for transfer of foreign DNA to members of the genus Gordonia. Appl. Environ. Microbiol. 69: 4971-4974.
5. Arenskötter, M., D. Bröker, and A. Steinbüchel. 2004. Biology of the metabolically diverse genus Gordonia. Appl. Environ. Microbiol. 70:3195-3204.
6. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology, 1st ed., vol. 1. John Wiley & Sons, New York, NY.
7. Banh, Q., M. Arenskötter, and A. Steinbüchel. 2005. Establishment of Tn5096-based transposon mutagenesis in Gordonia polyisoprenivorans. Appl. Environ. Microbiol. 71:5077-5084.
8. Barnard, D., and P. M. Lewis. 1988. Oxidative ageing, p. 621-673. In A. D. Roberts (ed.), Natural rubber: science and technology, part II. Oxford University Press, New York, NY.
9. Barr, D. P., and S. D. Aust. 1994. Effect of superoxide and superoxide-dismutase on lignin peroxidase-catalyzed veratryl alcohol oxidation. Arch. Biochem. Biophys. 311:378-382.
10. Beaman, B. L., S. M. Scates, S. E. Moring, R. Deem, and H. P. Misra. 1983. Purification and properties of a unique superoxide dismutase from Nocardia asteroides. J. Biol. Chem. 258:91-96.
11. Beauchamp, C., and I. Fridovich. 1971. Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal. Biochem. 44:276-287.
12. Birnboim, H. C., and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513-1523.
13. Braaz, R., P. Fischer, and D. Jendrossek. 2004. Novel type of heme-dependent oxygenase catalyzes oxidative cleavage of rubber (poly-cis-1,4-isoprene). Appl. Environ. Microbiol. 70:7388-7395.
14. Braaz, R., W. Armbruster, and D. Jendrossek. 2005. Heme-dependent rubber oxygenase RoxA of Xanthomonas sp. cleaves the carbon backbone of poly(cis-1,4-isoprene) by a dioxygenase mechanism. Appl. Environ. Microbiol. 71:2473-2478.
15. 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.
16. Braunstein, M., A. M. Brown, S. Kurtz, and W. R. Jacobs, Jr. 2001. Two nonredundant SecA homologues function in Mycobacteria. J. Bacteriol. 183: 6979-6990.
17. Braunstein, M., B. J. Espinosa, J. Chan, J. T. Belisie, and W. R. Jacobs. 2003. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 48:453-464.
18. Bröker, D., D. Dietz, M. Arenskötter, and A. Steinbüchel. 2008. The genomes of the non-clearing-zone-forming and natural rubber-degrading species Gordonia polyisoprenivorans and Gordonia westfalica harbor genes expressing Lcp activity in Streptomyces strains. Appl. Environ. Microbiol. 74:2288-2297.
19. Bullock, W. O., J. M. Fernandez, and J. M. Short. 1987. XL1-Blue: high efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection. BioTechniques 5:376-378.
20. Carlioz, A., and D. Touati. 1986. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 5:623-630.
21. Cundell, A. M., and A. P. Mulcock. 1974. The biodegradation of vulcanized rubber. Dev. Ind. Microbiol. 16:88-96.
22. +-cytotoxic-T-cell responses to novel epitopes in Mycobacterium tuberculosis superoxide dismutase, alanine dehydrogenase, and glutamine synthetase. Infect. Immun. 72:2412-2415.
23. Enoki, M., Y. Doi, and T. Iwata. 2003. Oxidative degradation of cis- and trans-polyisoprenes and vulcanized natural rubber with enzyme-mediator systems. Biomacromolecules 4:314-320.
24. Farr, S. B., and T. Kogoma. 1991. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 55:561-585.
25. Fridovich, I. 1986. Superoxide dismutases. Adv. Enzymol. 58:61-97.
26. Fridovich, I. 1995. Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64:97-112.
27. Hassan, H. M., and I. Fridovich. 1978. Regulation and role of superoxide dismutase. Biochem. Soc. Trans. 6:356-361.
28. Hein, S., H. Tran, and A. Steinbüchel. 1998. Synechocystis sp. PCC6803 possesses a two-component polyhydroxyalkanoic acid synthase similar to that of anoxygenic purple sulfur bacteria. Arch. Microbiol. 170:162-170.
29. Hjelm, H., K. Hjelm, and J. Sjöquist. 1972. Protein A from Staphylococcus aureus. Its isolation by affinity chromatography and its use as an immunosorbent for isolation of immunoglobulins. FEBS Lett. 28:73-76.
30. Ibrahim, E. M. A., M. Arenskötter, H. Luftmann, and A. Steinbüchel. 2006. Identification of poly(cis-1,4-isoprene) degradation intermediates during growth of moderately thermophilic actinomycetes on rubber and cloning of a functional lcp homologue from Nocardia farcinica strain E1. Appl. Environ. Microbiol. 72:2275-2282.
31. Jendrossek, D., and S. Reinhardt. 2003. Sequence analysis of a gene product synthesized by Xanthomonas sp. during growth on natural rubber latex. FEMS Microbiol. Lett. 224:61-65.
32. Juhnke, S., N. Peitzsch, N. Hübener, C. Große, and D. H. Nies. 2002. New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch. Microbiol. 179:15-25.
33. Kurihara, H., H. Wariishi, and H. Tanaka. 2002. Chemical stress-responsive genes from the lignin-degrading fungus Phanerochaete chrysosporium exposed to dibenzo-p-dioxin. FEMS Microbiol. Lett. 212:217-220.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
35. Linos, A., M. M. Berekaa, R. Reichelt, U. Keller, J. Schmitt, H. C. Flemming, R. M. Kroppenstedt, and A. Steinbüchel. 2000. Biodegradation of cis-1,4-polyisoprene rubbers by distinct actinomycetes: microbial strategies and detailed surface analysis. Appl. Environ. Microbiol. 66:1639-1645.
36. Linos, A., and A. Steinbüchel. 2001. Biodegradation of natural and synthetic rubbers, p. 321-359. In T. Koyama and A. Steinbüchel (ed.), Biopolymers, vol. 2. Wiley-VCH, Weinheim, Germany.
37. Loprasert, S., P. Vattanaviboon, W. Praituan, S. Chamnongpol, and S. Mongkolsuk. 1996. Regulation of the oxidative stress protective enzymes, catalase and superoxide dismutase in Xanthomonas - a review. Gene 179: 33-37.
38. Martinez, A., and R. Kolter. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179:5188-5194.
39. Mishra, R. N., S. L. Singla-Pareek, S. Nair, S. K. Sopory, and M. K. Reddy. 2002. Directional genome walking using PCR. BioTechniques 33:830-832.
40. Misra, H. P., and I. Fridovich. 1978. Inhibition of superoxide dismutases by azide. Arch. Biochem. Biophys. 189:317-322.
41. Ohta, Y., I. Ishiguro, J. Naito, and R. Shinohara. 1984. Role of cytosolic superoxide dismutase as a stimulator in anthranilamide hydroxylation by a microsomal monooxygenase system in rat liver. J. Biochem. 96:1323-1336.
42. Polle, A. 2001. Dissecting the superoxide dismutase-ascorbate- glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol. 126:445-462.
43. Porqué, P. G., A. Baldestein, and P. Reichards. 1970. The involvement of the thioredoxin system in the reaction of methionine sulfoxide and sulfate. J. Biol. Chem. 245:2371-2374.
44. Rose, K., and A. Steinbüchel. 2005. Biodegradation of natural rubber and related compounds: recent insights into a rare and hardly understood catabolic capability of microorganisms. Appl. Environ. Microbiol. 71:2803-2812.
45. Rose, K., K. B. Tenberge, and A. Steinbüchel. 2005. Identification and characterization of genes from Streptomyces sp. strain K30 responsible for clear zone formation on natural rubber latex and poly(cis-1,4-isoprene) rubber degradation. Biomacromolecules 6:180-188.
46. Sambrook, J. E., F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
47. Sato, S., Y. Honda, M. Kuwahara, and T. Watanabe. 2003. Degradation of vulcanized and nonvulcanized polyisoprene rubbers by lipid peroxidation catalyzed by oxidative enzymes and transition metals. Biomacromolecules 4:321-329.
48. Schlegel, H. G., H. Kaltwasser, and G. Gottschalk. 1961. Ein Submersverfahren zur Kultur wasserstoffoxidierender Bakterien: Wachstumsphysiologische Untersuchungen. Arch. Mikrobiol. 38:209-222.
49. Scott, M. D., S. R. Meshnick, and J. W. Eaton. 1987. Superoxide dismutase-rich bacteria. J. Biol. Chem. 262:3640-3645.
50. Snapper, S. B., R. E. Melton, S. Mustafa, T. Kieser, and W. R. Jacobs, Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
51. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
52. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
53. Tsuchii, A., T. Suzuki, and K. Takeda. 1985. Microbial degradation of natural rubber vulcanizates. Appl. Environ. Microbiol. 50:965-970.
54. Tullius, M. V., G. Harth, and M. A. Horwitz. 2001. High extracellular levels of Mycobacterium tuberculosis glutamine synthetase and superoxide dismutase in actively growing cultures are due to high expression and extracellular stability rather than to a protein-specific export mechanism. Infect. Immun. 69:6348-6363.
55. Warneke, S., M. Arenskötter, K. B. Tenberge, and A. Steinbüchel. 2007. Bacterial degradation of poly(trans-1,4- isoprene) (gutta percha). Microbiology 153:347-356.
56. Weber, K., and M. Osborn. 1969. The reliability of molecular weight determinations by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Biol. Chem. 244:4406-4412.
57. Yang, S., R. S. Wu, and R. Y. Kong. 2002. Biodegradation and enzymatic responses in the marine diatom Skeletonema costatum upon exposure to 2,4-dichlorophenol. Aquat. Toxicol. 59:191-200.
58. Yikmis, M., M. Arenskötter, K. Rose, N. Lange, H. Wernsmann, L. Wiefel, and A. Steinbüchel. 2008. Secretion and transcriptional regulation of the latex clearing protein Lcp by the rubber-degrading bacterium Streptomyces sp. strain K30. Appl. Environ. Microbiol. 74:5373-5382.