Isolation and characterization of metalloproteases with a novel domain structure by construction and screening of metagenomic libraries

Applied and Environmental Microbiology

Volumn 75, Issue 8, 2009, Pages 2506-2516

  Waschkowitz, Tanja ^a   Rockstroh, Stephanie ^a   Daniel, Rolf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR PLATES; BIOCHEMICAL ANALYSIS; C-TERMINAL DOMAINS; C-TERMINAL EXTENSIONS; DNA FRAGMENTS; DNA LIGASE; E. COLI; EXTRACELLULAR PROTEASE; INSERT SIZES; ISOLATION AND CHARACTERIZATIONS; METAGENOMIC LIBRARIES; METALLO PROTEASE; METALLOPEPTIDASES; METALLOPROTEASES; MODULAR STRUCTURES; N TERMINALS; NOVEL DOMAINS; OPTIMUM PH; PROREGION; PROTEASE ACTIVITIES; PROTEOLYTIC ACTIVITIES; SIGNAL SEQUENCES; SKIM MILKS; THERMOLYSIN; TOPOISOMERASE; XANTHOMONAS;

CLONING; DNA; ENZYME ACTIVITY; ENZYMES; ESCHERICHIA COLI; GENE ENCODING; LIBRARIES; NUCLEIC ACIDS; POLYSACCHARIDES;

DNA SEQUENCES;

AGAR; BACTERIAL ENZYME; DNA FRAGMENT; METALLOPROTEINASE;

CLONE; COMPARATIVE STUDY; DNA; ENZYME ACTIVITY; GENOME; PLASMID;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE CONSTRUCT; GENE INSERTION; GENE LIBRARY; GENETIC SCREENING; METAGENOMICS; MILK; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PLASMID; PROTEIN DEGRADATION; PROTEIN DOMAIN; SCREENING TEST; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TEMPERATURE; XANTHOMONAS;

CATALYTIC DOMAIN; CLONING, MOLECULAR; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; ENZYME STABILITY; ESCHERICHIA COLI; GENE LIBRARY; HYDROGEN-ION CONCENTRATION; METALLOPROTEASES; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; XANTHOMONAS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; XANTHOMONAS;

EID: 64749114328     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02136-08     Document Type: Article

References (59)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
3. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
4. Bitar, A. P., M. Cao, and H. Marquis. 2008. The metalloprotease of Listeria monocytogenes is activated by intramolecular autocatalysis. J. Bacteriol. 272: 217-228.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Chuang, Y. C., T. M. Chang, and M. C. Chang. 1997. Cloning and charac- terization of the gene (empV) encoding extracellular metalloprotease from Vibrio vulnificus. Gene 189:163-168.
7. Daniel, R. 2005. The metagenomics of soil. Nat. Rev. Microbiol. 3:470-478.
8. David, V. A., A. H. Deutch, A. Sloma, A. Pawlyk, A. Ally, and D. R. Durham. 1992. Cloning, sequencing and expression of the gene encoding the extra- cellular neutral protease, vibriolysin, of Vibrio proteolyticus. Gene 112:107-112.
9. Elend, C., C. Schmeisser, C. Leggewie, P. Babiak, J. D. Carballeira, H. L. Steele, J.-L. Reymond, K.-E. Jaeger, and W. R. Streit. 2006. Isolation and biochemical characterization of two novel metagenome-derived esterases. Appl. Environ. Microbiol. 72:3637-3645.
10. Finn, R. D., J. Mistry, B. Schuster-Böckler, S. Griffiths-Jones, V. Hollich, T. Lassmann, S. Oxon, M. Marshall, A. Khanna, R. Durbin, S. R. Eddy, E. L. L. Sonnhammer, and A. Bateman. 2006. Pfam: clans, web tools and services. Nucleic Acids Res. 34:D247-D251.
11. Gray, L., N. Mackman, J. M. Nicaud, and I. B. Holland. 1986. The carboxy- terminal region of haemolysin 2001 is required for secretion of the toxin from Escherichia coli. Mol. Gen. Genet. 205:127-133.
12. Guan, C., J. Ju, B. R. Borlee, L. L. Williamson, B. Shen, K. F. Raffa, and J. Handelsman. 2007. Signal mimics derived from a metagenomic analysis of the gypsy moth gut microbiota. Appl. Environ. Microbiol. 73:3669-3676.
13. Gupta, R., Q. K. Berg, and P. Lorenz. 2002. Bacterial alkaline proteases: molecular approaches and industrial applications. Appl. Microbiol. Biotech- nol. 59:15-32.
14. Handelsman, J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
15. Häse, C. C., and R. A. Finkelstein. 1993. Bacterial extracellular zinc-con- taining metalloproteases. Microbiol. Rev. 57:823-837.
16. Henne, A., R. A. Schmitz, M. Bömeke, G. Gottschalk, and R. Daniel. 2000. Screening of environmental DNA libraries for the presence of genes con- ferring lipolytic activity on Escherichia coli. Appl. Environ. Microbiol. 66: 3113-3116.
17. Henne, A., R. Daniel, R. A. Schmitz, and G. Gottschalk. 1999. Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxybutyrate. Appl. Environ. Microbiol. 65:3901-3907.
18. Holmes, M. A., and B. W. Matthews. 1982. Structure of thermolysin refined at 1.6 Å resolution. J. Mol. Biol. 160:623-639.
19. Jones, B. V., F. Sun, and J. R. Marchesi. 2007. Using skimmed milk agar to functionally screen a gut metagenomic library for proteases may lead to false positives. Lett. Appl. Microbiol. 45:418-420.
20. Kim, S.-K., J.-Y. Yang, and J. Cha. 2002. Cloning and sequence analysis of a novel metalloprotease gene of Vibrio parahaemolyticus. Gene 282:277-286.
21. Knietsch, A., T. Waschkowitz, S. Bowien, A. Henne, and R. Daniel. 2003. Construction and screening of metagenomic libraries derived from enrich- ment cultures: generation of a gene bank for genes conferring alcohol oxi- doreductase activity on Escherichia coli. Appl. Environ. Microbiol. 69:1408-1416.
22. Kothary, M. H., B. A. McCardell, C. D. Frazar, D. Deer, and B. D. Tall. 2007. Characterization of the zinc-containing metalloprotease encoded by zpx and development of a species-specific detection method for Enterobacter sakaza- kii. Appl. Environ. Microbiol. 73:4142-4151.
23. Kumar, C. G., and H. Takagi. 1999. Microbial alkaline proteases: from a bioindustrial viewpoint. Biotechnol. Adv. 17:561-594.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 270:680-685.
25. Lee, B.-M., Y.-J. Park, D.-S. Park, H.-W. Kang, J.-G. Kim, E.-S. Song, I.-C. Park, U.-H. Yoon, J.-H. Hahn, B.-S. Koo, G.-B. Lee, H. Kim, H.-S. Park, K.-O. Yoon, J.-H. Kim, C. Jung, N.-H. Koh, J.-S. Seo, and S.-J. Go. 2005. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC 10331, the bacterial blight pathogen. Nucleic Acids Res. 33:577-586.
26. Lee, D.-G., J. H. Jeon, M. K. Jang, N. Y. Kim, J. H. Lee, J.-H. Lee, S.-J. Kim, G.-D. Kim, and S.-H. Lee. 2007. Screening and characterization of a novel fibrinolytic metalloprotease from a metagenomic library. Biotechnol. Lett. 29:465-472.
27. Lee, S.-O., J. Kato, K. Nakashima, A. Kuroda, T. Ikeda, N. Takiguchi, and H. Ohtake. 2002. Cloning and characterization of extracellular metal pro- tease gene of the algicidal marine bacterium Pseudoalteromonas sp. strain A28. Biosci. Biotechnol. Biochem. 66:1366-1369.
28. Leyns, F., M. de Cleene, J. Swings, and J. de Ley. 1984. The host range of the genus Xanthomonas. Bot. Rev. 50:305-355.
29. Lorenz, P. J., and J. Eck. 2005. Metagenomics and industrial applications. Nat. Rev. Microbiol. 3:510-516.
30. + anti- porter activity on Escherichia coli: characterization of the recovered genes and the corresponding gene products. J. Bacteriol. 183:6645-6653.
31. Marchler-Bauer, A., J. B. Anderson, M. K. Derbyshire, C. DeWeese-Scott, N. R. Gonzales, M. Gwadz, L. Hao, S. He, D. I. Hurwitz, J. D. Jackson, Z. Ke, D. Krylov, C. J. Lanczycki, C. A. Liebert, C. Liu, F. Lu, S. Lu, G. H. Marchler, M. Mullokandov, J. S. Song, N. Thanki, R. A. Yamashita, J. J. Yin, D. Zhang, and S. H. Bryant. 2007. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35:D237-D240.
32. Mirete, S., C. G. de Figueras, and J. E. González-Pastor. 2007. Novel nickel- resistance genes from the rhizosphere metagenome of acid mine drainage- adapted plants. Appl. Environ. Microbiol. 73:6001-6011.
33. Miyamoto, K., E. Nukui, M. Hirose, F. Nagai, T. Sato, Y. Inamori, and H. Tsujibo. 2002. A metalloprotease (MprIII) involved in the chitinolytic system of a marine bacterium, Alteromonas sp. strain O-7. Appl. Environ. Microbiol. 68:5563-5570.
34. Miyamoto, K., H. Tsujibo, E. Nukui, H. Itoh, Y. Kaidzu, and Y. Inamori. 2002. Isolation and characterization of the genes encoding two metallopro- teases (MprI and MprII) from a marine bacterium, Alteromonas sp. strain O-7. Biosci. Biotechnol. Biochem. 66:416-421.
35. Miyoshi, S., K. Kawata, K. Tomochika, S. Shinoda, and S. Yamamoto. 2001. The C-terminal domain promotes the hemorrhagic damage caused by Vibrio vulnificus metalloprotease. Toxicon 39:1883-1886.
36. Miyoshi, S., and S. Shinoda. 2000. Microbial metalloproteases and patho- genesis. Microbes Infect. 2:91-98.
37. Pfennig, N., and K. D. Lippert. 1966. U ̈ ber das Vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch. Microbiol. 55:245-256.
38. Pugsley, A. P. 1993. The complete general secretory pathway in gram-neg- ative bacteria. Microbiol. Rev. 57:50-108.
39. Rao, M. B., A. M. Tanksale, M. S. Ghatge, and V. V. Deshpande. 1998. Molecular and biotechnological aspects of microbial proteases. Microbiol. Mol. Biol. Rev. 62:597-635.
40. Rawlings, N. D., and A. J. Barret. 1995. Evolutionary families of metallopep- tidases. Methods Enzymol. 248:183-228.
41. Rawlings, N. D., and A. J. Barrett. 2004. Introduction: metallopeptidases and their clans, p. 231-267. In A. J. Barrett, N. D. Rawlings, and J. F. Woessner (ed.), Handbook of proteolytic enzymes, 2nd ed. Elsevier, London, United Kingdom.
42. Rawlings, N. D., F. R. Morton, and A. J. Barrett. 2006. MEROPS: the peptidase database. Nucleic Acids Res. 34:D270-D272.
43. Riesenfeld, C. S., P. D. Schloss, and J. Handelsman. 2004. Metagenomics: genomic analysis of microbial communities. Annu. Rev. Genet. 38:525-552.
44. Rondon, M. R., P. R. August, A. D. Bettermann, S. F. Brady, T. H. Gross- man, M. R. Liles, K. A. Loiacono, B. A. Lynch, L. A. MacNeil, C. Minor, C. L. Tiong, M. Gilman, M. S. Osburne, J. Clardy, J. Handelsman, and R. M. Goodman. 2000. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Envi- ron. Microbiol. 66:2541-2547.
45. Rovere, C., J. Luis, J. C. Lissitzky, A. Basak, J. Marvaldi, M. Chretien, and N. G. Seidah. 1999. The RGD motif and the C-terminal segment of proprotein convertase 1 are critical for its cellular trafficking but not for its intracellular binding to integrin α5β1. J. Biol. Chem. 274:12461-12467.
46. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajan- dream, and B. Barrell. 2000. Artemis: sequence visualization and annota- tion. Bioinformatics 16:944-945.
47. Santosa, D. A. 2001. Rapid extraction and purification of environmental DNA for molecular cloning applications and molecular diversity studies. Mol. Biotechnol. 17:59-64.
48. Schmitz, J. E., A. Daniel, M. Collin, R. Schuch, and A. Fischetti. 2008. Rapid DNA library construction for functional genomic and metagenomic screen- ing. Appl. Environ. Microbiol. 74:1649-1652.
49. Seidah, N. G., and M. Chretien. 1997. Eukaryotic protein processing: endo- proteolysis of precursor proteins. Curr. Opin. Biotechnol. 8:602-607.
50. Shinde, U., and M. Inonye. 2000. Intramolecular chaperones: polypeptide extensions that modulate protein folding. Semin. Cell Dev. Biol. 11:35-44.
51. Tang, B., S. Nirasawa, M. Kitaoka, C. Marie-Claire, and K. Hayashi. 2003. General function of N-terminal propeptide on assisting protein folding and inhibiting catalytic activity based on observations with a chimeric thermoly- sin-like protease. Biochem. Biophys. Res. Commun. 301:1093-1098.
52. Titani, T., M. A. Mermodson, L. H. Ericsson, K. A. Walsh, and H. Neurath. 1972. Amino acid sequence of thermolysin. Nat. New Biol. 238:35-37.
53. Van Hellemond, E. W., D. B. Janssen, and M. W. Fraaije. 2007. Discovery of a novel styrene monooxygenase originating from the metagenome. Appl. Environ. Microbiol. 73:5832-5839.
54. Wilkinson, D. E., T. Jeanicke, and D. A. Cowan. 2002. Efficient molecular cloning of environmental DNA from geothermal sediments. Biotechnol. Lett. 24:155-161.
55. Xiong, H., L. Song, Y. Xu, M.-Y. Tsoi, S. Dobretsov, and P.-Y. Qian. 2007. Characterization of proteolytic bacteria from the Aleutian deep-sea and their proteases. J. Ind. Microbiol. Biotechnol. 34:63-71.
56. Yamagata, Y., R. Abe, Y. Fujita, and E. Ichishima. 1995. Molecular cloning and nucleotide sequence of the 90K serine protease gene, hspK, from Ba- cillus subtilis (natto) no. 16. Curr. Microbiol. 31:340-344.
57. Yeats, C., S. Bentley, and A. Bateman. 2003. New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol. 3:3.
58. Yun, J., S. Kang, S. Park, H. Yoon, M.-J. Kim, S. Heu, and S. Ryu. 2004. Characterization of a novel amylolytic enzyme encoded by a gene from a soil-derived metagenomic library. Appl. Environ. Microbiol. 70:7229-7235.
59. Zhou, A., S. Martin, G. Lipkind, J. La Mendola, and D. F. Steiner. 1998. Regulatory roles of the P domain of the subtilisin-like prohormone convertases. J. Biol. Chem. 273:11107-11114.