Production and biochemical and molecular characterization of a keratinolytic serine protease from chicken feather-degrading Bacillus licheniformis RPk

Canadian Journal of Microbiology

Volumn 55, Issue 4, 2009, Pages 427-436

  Fakhfakh, Nahed ^a   Kanoun, Safia ^a   Manni, Laila ^a   Nasri, Moncef ^a  

^a UNIVERSITY OF SFAX   (Tunisia)

Author keywords

Bacillus licheniformis; Chicken feathers; Dna sequence; Keratinase; Protease; Purification

Indexed keywords

AMINO ACID SEQUENCES; BACILLUS LICHENIFORMIS; CASEINOLYTIC ACTIVITIES; CHICKEN FEATHERS; FEATHER DEGRADATIONS; GEL FILTRATIONS; KERATINASE; KERATINOLYTIC ACTIVITIES; MOLECULAR CHARACTERIZATIONS; OPTIMUM PH; PHENYLMETHYLSULFONYL FLUORIDES; POLLUTED RIVERS; PROTEASE; PROTEASE ACTIVITIES; PURIFIED ENZYMES; SDS PAGES; SERINE PROTEASE; SUBTILISIN CARLSBERG; YEAST EXTRACTS;

AMINATION; AMINES; AMINO ACIDS; BACTERIOLOGY; CALCIUM; DEGRADATION; DIFFUSERS (OPTICAL); DNA; ELECTRON HOLOGRAPHY; ENZYMES; GELATION; GENE ENCODING; MEATS; NUCLEIC ACIDS; ORGANIC ACIDS; PURIFICATION; SODIUM CHLORIDE; SUBSTRATES;

ENZYME ACTIVITY;

BENZYLSULFONYL FLUORIDE; CALCIUM; CARBON; CASEIN; KERATIN; NITROGEN; PROTEINASE INHIBITOR; SERINE PROTEINASE;

BACTERIUM; BIOCHEMISTRY; BIODEGRADATION; ENZYME ACTIVITY; HOMOGENEITY; MOLECULAR ANALYSIS; PH; RIVER POLLUTION; TEMPERATURE EFFECT;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS LICHENIFORMIS; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHICKEN; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SYNTHESIS; FEATHER; GEL FILTRATION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; TEMPERATURE; THERMOSTABILITY; YEAST;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS; CHICKENS; ENZYME STABILITY; FEATHERS; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; RIVERS; SEQUENCE ANALYSIS, DNA; SERINE ENDOPEPTIDASES; SUBSTRATE SPECIFICITY; TUNISIA; WATER POLLUTION;

BACILLUS LICHENIFORMIS; BACTERIA (MICROORGANISMS);

EID: 65349194450     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W08-143     Document Type: Article

References (59)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI- BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402. doi:10.1093/nar/25.17.3389. PMID:9254694.
2. Bálint, B., Bagi, Z., Tóth, A., Rákhely, G., Perei, K., and Kovács, K.L. 2005. Utilization of keratin-containing biowaste to produce biohydrogen. Appl. Microbiol. Biotechnol. 69: 404-410. doi:10. 1007/s00253-005-1993-3. PMID:15856225.
3. Bergey, D. 1993. Bergey's manual of determinative bacteriology. 9th ed. Lippincott Williams & Wilins, Baltimore, Maryland.
4. Bockle, B., Glunsky, B., and Muller, R. 1995. Characterization of a keratinolytic serine proteinase from Streptomyces pactum DSM 40530. Appl. Environ. Microbiol. 61: 3705-3710. PMID:7487006.
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. doi:10. 1016/0003-2697(76)90527-3. PMID:942051.
6. Bressollier, P., Letourneau, F., Urdaci, M., and Verneuil, B. 1999. Purification and characterization of a keratinolytic serine protei- nase from Streptomyces albidoflavus. Appl. Environ. Microbiol. 65: 2570-2576. PMID:10347045.
7. Chambliss, G.H. 1993. Carbon source-mediated catabolite repression. In Bacillus subtilis and other gram-positive bacteria. Edited by A.L. Sonenshein, J.A. Hoch, and R. Losick. American Society for Microbiology, Washington, D.C. pp. 213-219.
8. Cheng, S.W., Hu, H.M., Shen, S.W., Takagi, H., Asano, M., and Tsai, Y.C. 1995. Production and characterization of keratinase of a feather-degrading Bacillus licheniformis PWD-1. Biosci. Biotechnol. Biochem. 59: 2239-2243. PMID:8611746.
9. Chitte, R.R., Nalawade, V.K., and Dey, S. 1999. Keratinolytic activity from the broth of a feather-degrading thermophilic Strep- tomyces thermoviolaceus strain SD8. Lett. Appl. Microbiol. 28: 131-136. doi:10.1046/j.1365-2672.1999.00484.x.
10. De Toni, C.H., Richter, M.F., Chagas, J.R., Henriques, J.A.P., and Termignoni, C. 2002. Purification and characterization of an alkaline serine endopeptidase from a feather-degrading Xanthomo- nas maltophilia strain. Can. J. Microbiol. 48: 342-348. doi:10. 1139/w02-027. PMID:12030707.
11. Edman, P., and Begg, G. 1967. A protein sequenator. Eur. J. Bio- chem. 1: 80-91. doi:10.1111/j.1432-1033.1967.tb00047.x. PMID:6059350.
12. El Hadj-Ali, N., Agrebi, R., Ghorbel-Frikha, B., Sellami-Kamoun, A., Kanoun, S., and Nasri, M. 2007. Biochemical and molecular characterization of a detergent stable alkaline serine-protease from a newly isolated Bacillus licheniformis NH1. Enzyme Mi- crob. Technol. 40: 515-523. doi:10.1016/j.enzmictec.2006.05.007.
13. Friedrich, A.B., and Antranikian, G. 1996. Keratin degradation by Fervidobacterium pennavorans, a novel thermophilic anaerobic species of the order thermotogales. Appl. Environ. Microbiol. 62: 2875-2882. PMID:16535379.
14. Gessesse, A., Hatti-Kaul, R., Gashe, B.A., and Mattiasson, B. 2003. Novel alkaline proteases from alkaliphilic bacteria grown on chicken feather. Enzyme Microb. Technol. 32: 519-524. doi:10. 1016/S0141-0229(02)00324-1.
15. Ghorbel, B., Sellami-Kamoun, A., and Nasri, M. 2003. Stability studies of protease from Bacillus cereus BG1. Enzyme Microb. Technol. 32: 513-518. doi:10.1016/S0141-0229(03)00004-8.
16. Gousterova, A., Braikova, D., Goshev, I., Christov, P., Tishinov, K., Vasileva-Tonkova, E., et al. 2005. Degradation of keratin and collagen containing wastes by newly isolated thermoactinomy- cetes or by alkaline hydrolysis. Lett. Appl. Microbiol. 40: 335-340. doi:10.1111/j.1472-765X. 2005.01692.x. PMID:15836735.
17. Gradisar, H., Kern, S., and Friedrich, J. 2000. Keratinase of Dora- tomyces microsporus. Appl. Microbiol. Biotechnol. 53: 196-200. doi:10.1007/s002530050008. PMID:10709982.
18. Hajji, M., Kanoun, S., Nasri, M., and Gharsallah, N. 2007. Purification and characterization of an alkaline serine-protease produced by a newly isolated Aspergillus clavatus ES1. Process Biochem. 42: 791-797. doi:10.1016/j.procbio.2007.01.011.
19. Higgins, D.G., and Sharp, P.M. 1988. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene, 73: 237-244. doi:10.1016/0378-1119(88)90330-7. PMID:3243435.
20. Hinman, R.L. 1994. The changing face of the fermentation industry. Chemtech, 24: 45-48.
21. Ignatova, Z., Gousterova, A., Spassov, G., and Nedkov, P. 1999. Isolation and partial characterization of extracellular keratinase from a wool degrading thermophilic actinomycete strain Ther- moactinomyces candidus. Can. J. Microbiol. 45: 217-222. doi:10.1139/cjm-45-3-217. PMID:10408094.
22. Jacobs, M., Eliasson, M., Uhlen, M., and Flock, J.I. 1985. Cloning, sequencing, and expression of subtilisin Carlsberg from Bacillus licheniformis. Nucleic Acids Res. 13: 8913-8926. doi:10.1093/ nar/13.24.8913. PMID:3001653.
23. Kembhavi, A.A., Kulkarni, A., and Pant, A. 1993. Salt-tolerant and thermostable alkaline protease from Bacillus subtilis NCIM No. 64. Appl. Biochem. Biotechnol. 38: 83-92. doi:10.1007/BF02916414. PMID:8346907.
24. Kidd, R.D., Yennawar, H.P., Sears, P., Wong, C.H., and Farber, G.K. 1996. A weak calcium binding site in subtilisin BPN' has a dramatic effect on protein stability. J. Am. Chem. Soc. 118: 1645-1650. doi:10.1021/ja953443p.
25. Kim, J.M., Lim, W.J., and Suh, H.J. 2001. Feather-degrading Bacillus species from poultry waste. Process Biochem. 37: 287-291. doi:10.1016/S0032-9592(01)00206-0.
26. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685. doi:10.1038/227680a0. PMID:5432063.
27. Lin, X., Lee, C.G., Casale, E.S., and Shih, J.C.H. 1992. Purification and characterization of a keratinase from a feather-degrading Bacillus licheniformis strain. Appl. Environ. Microbiol. 58: 3271-3275. PMID:16348784.
28. Lin, X., Kelemen, D.W., Miller, E.S., and Shih, J.C.H. 1995. Nu-cleotide sequence and expression of kerA, the gene encoding a keratinolytic protease of Bacillus licheniformis PWD-1. Appl. Environ. Microbiol. 61: 1469-1474. PMID:7747965.
29. Lin, X., Shih, J.C.H., and Swaisgood, H. 1996. Hydrolysis of feather keratin by immobilized keratinase. Appl. Environ. Mi-crobiol. 62: 4273-4275. PMID:16535453.
30. Lin, S.J., Yoshimura, E., Sakai, H., Wakagi, T., and Matsuzawa, H. 1999. Weakly bound calcium ions involved in the thermostability of aqualysin I, a heat-stable subtilisin-type protease of Ther- mus aquaticus YT-1. Biochim. Biophys. Acta. 1433: 132-138. PMID:10446366.
31. Manni, L., Jellouli, K., Agrebi, R., Bayoudh, A., and Nasri, M. 2008. Biochemical and molecular characterization of a novel calcium-dependent metalloprotease from Bacillus cereus SV1. Process Biochem. 43: 522-530. doi:10.1016/j.procbio.2008.01. 016.
32. Miller, J.H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y. pp. 431-135.
33. Mukhopadhyay, R.P., and Chandra, A.L. 1990. Keratinase of a streptomycete. Indian J. Exp. Biol. 28: 575-577. PMID:1698173.
34. Naidu, K.S.B., and Devi, K.L. 2005. Optimization of thermostable alkaline protease production from species of Bacillus using rice bran. Afr. J. Biotechnol. 4: 724-726.
35. Nam, G.W., Lee, D.W., Lee, H.S., Lee, N.J., Kim, B.C., Choe, E.A., et al. 2002. Native-feather degradation by Fervidobacter- ium islandicum AW-1, a newly isolated keratinase-producing thermophilic anaerobe. Arch. Microbiol. 178: 538-547. doi:10.1007/s00203-002-0489-0. PMID:12420177.
36. Nedkov, P., Oberthür, W., and Braunitzer, G. 1985. Determination of the complete amino-acid sequence of subtilisin DY and its comparison with the primary structures of the subtilisins BPN', Carlsberg, and amylosacchariticus. Biol. Chem. Hoppe Seyler. 366: 421-430. PMID:3927935.
37. Noval, J.J., and Nickerson, W.J. 1959. Decomposition of native keratin by Streptomyces fradiae. J. Bacteriol. 77: 251-263. PMID:13641184.
38. Onifade, A.A., Al-Sane, N.A., Al-Musallam, A.A., and Al-Zarban, S. 1998. A review: Potentials for biotechnological applications of keratin-degrading microorganisms and their enzymes for nutritional improvement of feathers and other keratins as livestock feed resources. Bioresour. Technol. 66: 1-11. doi:10.1016/ S0960-8524(98)00033-9.
39. Papadopoulos, M.C., El-Boushy, A.R., Roodbeen, A.E., and Ketelaars, E.H. 1986. Effects of processing time and moisture content on amino acid composition and nitrogen characteristics of feather meal. Anim. Feed Sci. Technol. 14: 279-290. doi:10. 1016/0377-8401(86)90100-8.
40. Parry, D.A.D., and North, A.C.T. 1998. Hard keratin intermediate filament chains: substructure of the N- and C-terminal domains and the predicted structure and function of the C-terminal domains of type I and type II chains. J. Struct. Biol. 122: 67-75. doi:10.1006/jsbi.1998.3967. PMID:9724606.
41. Ramnani, P., Singh, R., and Gupta, R. 2005. Keratinolytic potential of Bacillus licheniformis RG1: structural and biochemical mechanism of feather degradation. Can. J. Microbiol. 51: 191-196. doi:10.1139/w04-123. PMID:15920616.
42. Riessen, S., and Antranikian, G. 2001. Isolation of Thermoanaero- bacter keratinophilus sp. nov., a novel thermophilic, anaerobic bacterium with keratinolytic activity. Extremophiles, 5: 399408. doi:10.1007/s007920100209. PMID:11778841.
43. Rozs, M., Manczinger, L., Vagvolgyi, C., and Kevei, F. 2001. Secretion of a trypsin-like thiol protease by a new keratinoly- tic strain of Bacillus licheniformis. FEMS Microbiol. Lett. 205: 221-224. doi:10.1111/j.1574-6968.2001.tb10951.x. PMID:11750806.
44. Sangali, S., and Brandelli, A. 2000. Feather keratin hydrolysis by a Vibrio sp. strain kr2. J. Appl. Microbiol. 89: 735-743. doi:10. 1046/j.1365-2672.2000.01173.x. PMID:11119146.
45. Sanger, F., Nicklen, S., and Coulson, A.R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74: 5463-5467. doi:10.1073/pnas.74.12.5463. PMID:271968.
46. Shih, J.C.H. 1993. Recent developments in poultry waste digestion and feather utilization. A review. Poult. Sci. 72: 1617-1620.
47. Smith, C.A., Toogood, H.S., Baker, H.M., Daniel, R.M., and Baker, E.N. 1999. Calcium-mediated thermostability in the subtilisin superfamily: the crystal structure of Bacillus AK.1 protease at 1.8 A resolution. J. Mol. Biol. 294: 1027-1040. doi:10.1006/jmbi.1999.3291. PMID:10588904. Steiner, R.J., Kellems, R.O., and Church, D.C. 1983. Feather and hair meals for ruminants. IV. Effects of chemical treatments of feathers and processing time on digestibility. J. Anim. Sci. 57: 495-502.
48. Szabo, I., Benedek, A., Mihaly-Szabo, I., and Barabas, Gy. 2000. Feather degradation with a thermotolerant Streptomyces grami- nofaciens strain. World J. Microbiol. Biotechnol. 16: 253-255. doi:10.1023/A:1008950032017.
49. Takami, H., Nakamura, S., Aono, R., and Horikoshi, K. 1992. Degradation of human hair by a thermostable alkaline protease from alkaliphilic Bacillus sp. No. AH-101. Biosci. Biotechnol. Biochem. 56: 1667-1669.
50. Takami, H., Nogi, Y., and Horikoshi, K. 1999. Reidentification of the keratinase-producing facultatively alkaliphilic bacillus sp. AH-101 as Bacillus halodurans. Extremophiles, 3: 293-296. doi:10.1007/s007920050130. PMID:10591021.
51. Takiuchi, I., Higuchi, D., Sei, Y., and Koga, M. 1982. Isolation of an extracellular proteinase (keratinase) from Microsporum canis. Sabouraudia, 20: 281-288. PMID:6186036.
52. Thanikaivelan, P., Rao, J.R., Nair, B.U., and Ramasami, T. 2004. Progress and recent trends in biotechnological methods for leather processing. Trends Biotechnol. 22: 181-188. doi:10. 1016/j.tibtech.2004.02.008. PMID:15038923.
53. Thys, R.C.S., Lucas, F.S., Riffel, A., Heeb, P., and Brandelli, A. 2004. Characterization of a protease of a feather-degrading Mi- crobacterium species. Lett. Appl. Microbiol. 39: 181-186. doi:10.1111/j.1472-765X. 2004.01558.x. PMID:15242459.
54. Vidal, L., Christen, P., and Coello, M.N. 2000. Feather degradation by Kocuria rosea in submerged culture. World J. Microbiol. Biotechnol. 16: 551-554. doi:10.1023/A:1008976802181.
55. Wang, J.J., and Shih, J.C.H. 1999. Fermentation production of ker- atinase from Bacillus licheniformis PWD-1 and a recombinant B. subtilis FDB-29. J. Ind. Microbiol. Biotechnol. 22: 608-616. doi:10.1038/sj.jim.2900667. PMID:10455487. Williams, C.M., Richter, C.S., Mackenzie, J.M., and Shih, J.C.H. 1990. Isolation, identification, and characterization of a feather- degrading bacterium. Appl. Environ. Microbiol. 56: 1509-1515. PMID:16348199
56. Williams, C.M., Lee, C.G., Garlich, J.D., and Shih, J.C.H. 1991. Evaluation of a bacterial feather fermentation product, feather- lysate as a feed protein. Poult. Sci. 70: 85-94.
57. Yamamura, S., Morita, Y., Hasan, Q., Yokohama, K., and Tamiya, E. 2002. Keratin degradation: a cooperative action of two enzymes from Stenotrophomonas sp. Biochem. Biophys. Res. Commun. 294: 1138-1143. doi:10.1016/S0006-291X(02)00580-6. PMID:12074595.
58. Yamauchi, K., Yamauchi, A., Kusunoki, T., Cohda, A., and Ko- nishi, Y. 1996. Preparation of stable aqueous solution of keratins, and physicochemical and biodegradational properties of films. J. Biomed. Mater. Res. 31: 439-444. doi:10.1002/(SICI) 1097-4636(199608)31:4<439::AID-JBM1>3.0.CO;2- M. PMID:8836838.
59. Yoshioka, M., Miwa, T., Horii, H., Takata, M., Yokoyama, T., Nishizawa, K., et al. 2007. Characterization of a proteolytic enzyme derived from a Bacillus strain that effectively degrades prion protein. J. Appl. Microbiol. 102: 509-515. doi:10.1111/j. 1365-2672.2006.03080.x. PMID:17241357.