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Bacterial and Fungal Proteolytic Enzymes: Production, Catalysis and Potential Applications

Abstract

Submerged and solid-state bioprocesses have been extensively explored worldwide and employed in a number of important studies dealing with microbial cultivation for the production of enzymes. The development of these production technologies has facilitated the generation of new enzyme-based products with applications in pharmaceuticals, food, bioactive peptides, and basic research studies, among others. The applicability of microorganisms in biotechnology is potentiated because of their various advantages, including large-scale production, short time of cultivation, and ease of handling. Currently, several studies are being conducted to search for new microbial peptidases with peculiar biochemical properties for industrial applications. Bioprospecting, being an important prerequisite for research and biotechnological development, is based on exploring the microbial diversity for enzyme production. Limited information is available on the production of specific proteolytic enzymes from bacterial and fungal species, especially on the subgroups threonine and glutamic peptidases, and the seventh catalytic type, nonhydrolytic asparagine peptide lyase. This gap in information motivated the present study about these unique biocatalysts. In this study, the biochemical and biotechnological aspects of the seven catalytic types of proteolytic enzymes, namely aspartyl, cysteine, serine, metallo, glutamic, and threonine peptidase, and asparagine peptide lyase, are summarized, with an emphasis on new studies, production, catalysis, and application of these enzymes.

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References

  1. 1.

    Ward, O. P. (2011). Production of recombinant proteins by filamentous fungi. Biotechnology Advances, 30, 1119–1139. doi:10.1016/j.biotechadv.2011.09.012.

  2. 2.

    Jisha, V. N., Smitha, R. B., Pradeep, S., Sreedevi, S., Unni, K. N., Sajith, S., Priji, P., Josh, M. S., & Benjamin, S. (2013). Versatility of microbial proteases. Advances in Enzyme Research, 1, 39–51.

    Article  Google Scholar 

  3. 3.

    Silva, R. R., Ângelo, T., & Cabral, H. (2013). Comparative evaluation of peptidases produced by Penicillium corylophilum and Penicillium waksmanii in solid state fermentation using agro-industrial residues. Journal of Agricultural Science and Technology B, 3, 230–237.

  4. 4.

    Silva, R. R., Caetano, R. C., Okamoto, D. N., de Oliveira, L. C. G., Bertolin, T. C., Juliano, M. A., et al. (2014). The identification and biochemical properties of the catalytic specificity of a serine peptidase secreted by Aspergillus fumigatus Fresenius. Protein and Peptide Letters, 21, 663–671.

  5. 5.

    Joo, H-S., & Choi, J. W. (2012). Purification and characterization of a novel alkaline protease from Bacillus horikoshii. Journal of Microbiology and Biotechnology, 22, 58–68.

  6. 6.

    Hawksworth, D. L. (2001). The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research, 105, 1422–1432.

    Article  Google Scholar 

  7. 7.

    Chambergo, F. S., & Valencia, E. Y. (2016). Fungal biodiversity to biotechnology. Applied Microbiology and Biotechnology, 100, 2567–2577.

    CAS  Article  Google Scholar 

  8. 8.

    Halabi, N., Rivoire, O., Leibler, S., & Ranganathan, R. (2009). Protein sectors: evolutionary units of three-dimensional structure. Cell, 138, 774–786.

  9. 9.

    Krem, M. M., & Di Cera, E. (2001). Molecular markers of serine protease evolution. The EMBO Journal, 20, 3036–3045.

    CAS  Article  Google Scholar 

  10. 10.

    Souza, P. M., Bittencourt, M. L. A., Caprara, C. C., Freitas, M., Almeida, R. P. C., Silveira, D., Fonseca, Y. M., Filho, E. X. F., Junior, A. P., & Magalhães, P. O. (2015). A biotechnology perspective of fungal proteases. Brazilian Journal of Microbiology, 46, 337–346.

    Article  Google Scholar 

  11. 11.

    Schechter, I., & Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochemical and Biophysical Research Communications, 27, 157–162.

  12. 12.

    Rawlings, N. D. (2016). Peptidase specificity from the substrate cleavage collection in the MEROPS database and a tool to measure cleavage site conservation. Biochimie, 122, 5–30.

    CAS  Article  Google Scholar 

  13. 13.

    Merheb-Dini, C., Cabral, H., Leite, R. S. R., Zanphorlin, L. M., Okamoto, D. N., Rodriguez, G. O. B., et al. (2009). Biochemical and functional characterization of a metalloprotease from the thermophilic fungus Thermoascus aurantiacus. Journal of Agricultural and Food Chemistry, 57, 9210–9217.

  14. 14.

    Neto, Y. A., de Oliveira, L. C., de Oliveira, A. H., Rosa, J. C., Juliano, M. A., Juliano, L., Rodrigues, A., & Cabral, H. (2015). Determination of specificity and biochemical characteristics of neutral protease isolated from Myceliophthora thermophila. Protein and Peptide Letters, 22, 972–982.

    Article  Google Scholar 

  15. 15.

    Biaggio, R. T., Silva, R. R., da Rosa, N. G., Leite, R. S. R., Arantes, E. C., Cabral, T. P. F., et al. (2016). Purification and biochemical characterization of an extracellular serine peptidase from Aspergillus terreus. Preparative Biochemistry and Biotechnology, 46, 298–304.

  16. 16.

    Silva, R. R., Souto, T. B., Oliveira, T. B., Oliveira, L. C. G., Karcher, D., Juliano, M. A., et al. (2016). Evaluation of the catalytic specificity, biochemical properties, and milk clotting abilities of an aspartic peptidase from Rhizomucor miehei. Journal of Industrial Microbiology and Biotechnology, 43, 1059–1069.

  17. 17.

    Doron, L., Coppenhagen-Glazer, S., Ibrahim, Y., Eini, A., Naor, R., Rosen, G., & Bachrach, G. (2014). Identification and characterization of Fusolisin, the Fusobacterium nucleatum autotransporter serine protease. PloS One. doi:10.1371/journal.pone.0111329.

    Google Scholar 

  18. 18.

    Brannon, J. R., Thomassin, J-L., Gruenheid, S., & Moual, H. L. (2015). Antimicrobial peptide conformation as a structural determinant of omptin protease specificity. Journal of Bacteriology, 197, 3583–3591. doi:10.1128/JB.00469-15.

  19. 19.

    Alves, A. C. V., Rogana, E., Barbosa, C. F., & Ferreira-Alves, D. L. (2007). The correction of reaction rates in continuous fluorometric assays of enzymes. Journal of Biochemical and Biophysical Methods, 70, 471–479.

    CAS  Article  Google Scholar 

  20. 20.

    Yegin, S., Fernandez-Lahore, M., Salgado, A. J. G., Guvenc, U., Goksungur, Y., & Tari, C. (2011). Aspartic proteinases from Mucor spp. in cheese manufacturing. Applied Microbiology and Biotechnology, 89, 949–960.

    CAS  Article  Google Scholar 

  21. 21.

    Kumar, A., Grover, S., Sharma, J., & Batish, V. K. (2010). Chymosin and other milk coagulants: sources and biotechnological interventions. Critical Reviews in Biotechnology, 30, 243–258.

    CAS  Article  Google Scholar 

  22. 22.

    Hill, J., & Phylip, L. H. (1997). Bacterial asparatic proteinases. FEBS Letters, 409, 357–360.

    CAS  Article  Google Scholar 

  23. 23.

    Brocklehurst, K., & Philpott, M. P. (2013). Cysteine proteases: mode of action and role in epidermal differentiation. Cell and Tissue Research, 351, 237–244. doi:10.1007/s00441-013-1557-2.

    CAS  Article  Google Scholar 

  24. 24.

    Ward, O. P., Rao, M. B., & Kulkarni, A. (2009). Proteases, production. Elsevier, 495–511.

  25. 25.

    Datta, A. (1992). Purification and characterization of a novel protease from solid substrate cultures of Phanerochaete chrysosporium. The Journal of Biological Chemistry, 267, 728–736.

    CAS  Google Scholar 

  26. 26.

    Cabaleiro, D. R., Rodrıguez-Couto, S., Sanromán, A., & Longo, M. A. (2002). Comparison between the protease production ability of ligninolytic fungi cultivated in solid state media. Process Biochemistry, 37, 1017–1023.

    CAS  Article  Google Scholar 

  27. 27.

    Dubey, V. K., Pande, M., Singh, B. K., & Jagannadham, M. V. (2007). Papain-like proteases: applications of their inhibitors. African Journal of Biotechnology, 6, 1077–1086.

    CAS  Google Scholar 

  28. 28.

    Rozs, M., Manczinger, L., Vágvölgyi, C., & Kevei, F. (2001). Secretion of a trypsin-like thiol protease by a new keratinolytic strain of Bacillus licheniformis. FEMS Microbiology Letters, 205, 221–224.

    CAS  Article  Google Scholar 

  29. 29.

    Silva, R. R., Cabral, T. P. F., Rodrigues, A., & Cabral, H. (2013). Production and partial characterization of serine and metallo peptidases secreted by Aspergillus fumigatus Fresenius in submerged and solid state fermentation. Brazilian Journal of Microbiology, 44, 235–243.

    Article  Google Scholar 

  30. 30.

    Graminho, E. R., Silva, R. R., Cabral, T. P. F., Arantes, E. C., Da Rosa, N. G., Juliano, L., Okamoto, D. N., Oliveira, L. C. G., Kondo, M. Y., Juliano, M. A., & Cabral, H. (2013). Purification, characterization, and specificity determination of a new serine protease secreted by Penicillium waksmanii. Applied Biochemistry and Biotechnology, 169, 201–214.

    CAS  Article  Google Scholar 

  31. 31.

    Ida, E. L., Silva, R. R., de Oliveira, T. B., Souto, T. B., Leite, J. A., Rodrigues, A., et al. (2016). Biochemical properties and evaluation of washing performance in commercial detergent compatibility of two collagenolytic serine peptidases secreted by Aspergillus fischeri and Penicillium citrinum. Preparative Biochemistry and Biotechnology. doi:10.1080/10826068.2016.1224247.

  32. 32.

    Iqbal, I., Aftab, M. N., Afzal, M., Ur-Rehman, A., Aftab, S., Zafar, A., et al. (2015). Purification and characterization of cloned alkaline protease gene of Geobacillus stearothermophilus. Journal of Basic Microbiology, 55, 160–171.

  33. 33.

    Joshi, S., & Satyanarayana, T. (2013). Characteristics and applications of a recombinant alkaline serine protease from a novel bacterium Bacillus lehensis. Bioresource Technology, 131, 76–85.

    CAS  Article  Google Scholar 

  34. 34.

    Lv, L.-X., Sim, M.-H., Li, Y.-D., Min, J., Feng, W.-H., Guan, W.-J., & Li, Y.-Q. (2010). Production, characterization and application of a keratinase from Chryseobacterium L99 sp. nov. Process Biochemistry, 45, 1236–1244.

    CAS  Article  Google Scholar 

  35. 35.

    Prakash, P., Jayalakshmi, S. K., & Sreeramulu, K. (2010). Purification and characterization of extreme alkaline, thermostable keratinase, and keratin disulfide reductase produced by Bacillus halodurans PPKS-2. Applied Microbiology and Biotechnology, 87, 625–633.

    CAS  Article  Google Scholar 

  36. 36.

    Fernández, D., Russi, S., Vendrell, J., Monod, M., & Pallares, I. (2013). A functional and structural study of the major metalloprotease secreted by the pathogenic fungus Aspergillus fumigatus. A cta Crystallographica Section D, 69, 1946–1957. doi:10.1107/S0907444913017642.

  37. 37.

    Neto, Y. A. A. H., Motta, C. M. S., & Cabral, H. (2013). Optimization of metalloprotease production by Eupenicillium javanicum in both solid state and submerged bioprocesses. African Journal of Biochemistry Research, 7, 146–157.

  38. 38.

    Jashni, M. K., Dols, I. H. M., Iida, Y., Boeren, S., Beenen, H. G., Mehrabi, R., Collemare, J., & de Wit, P. J. G. M. (2015). Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Molecular Plant-Microbe Interactions, 28, 996–1008.

    CAS  Article  Google Scholar 

  39. 39.

    Ruf, A., Stihle, M., Benz, J., Schmidt, M., & Sobek, H. (2013). Structure of gentlyase, the neutral metalloprotease of Paenibacillus polymyxa. Acta Crystallographica. Section D, Biological Crystallography, 69, 24–31.

    CAS  Article  Google Scholar 

  40. 40.

    Wang, F., Ning, Z., Lan, D., Liu, Y., Yang, B., & Wang, Y. (2012). Biochemical properties of recombinant leucine aminopeptidase II from Bacillus stearothermophilus and potential applications in the hydrolysis of Chinese anchovy (Engraulis japonicus) proteins. Journal of Agricultural and Food Chemistry, 60, 165–172.

    CAS  Article  Google Scholar 

  41. 41.

    Riffel, A., Brandelli, A., Bellato, C. M., Souza, G. H., Eberlin, M. N., & Tavares, F. C. (2007). Purification and characterization of a keratinolytic metalloprotease from Chryseobacterium sp. kr6. Journal of Biotechnology, 128, 693–703.

    CAS  Article  Google Scholar 

  42. 42.

    Tyndall, J. D. A., Nall, T., & Fairlie, D. P. (2005). Proteases universally recognize beta strands in their active sites. Chemical Reviews, 105, 973–999.

    CAS  Article  Google Scholar 

  43. 43.

    Kisselev, A. F., Songyang, Z., & Goldberg, A. L. (2000). Why does threonine, and not serine, function as the active site nucleophile in proteasomes? The Journal of Biological Chemistry, 275, 14831–14837.

    CAS  Article  Google Scholar 

  44. 44.

    Rawlings, N. D., Barret, A. J., & Bateman, A. (2011). Asparagine peptide lyases: a seventh catalytic type of proteolytic enzymes. The Journal of Biological Chemistry, 286, 38321–38328.

  45. 45.

    Baird Jr, T. T., Wright, W. D., & Craik, C. S. (2006). Conversion of trypsin to a functional threonine protease. Protein Science, 15, 1229–1238.

  46. 46.

    Kataoka, Y., Takada, K., Oyama, H., Tsunemi, M., James, M. N. G., & Oda, K. (2005). Catalytic residues and substrate specificity of scytalidoglutamic peptidase, the first member of the eqolisin in family (G1) of peptidases. FEBS Letters, 579, 2991–2994.

    CAS  Article  Google Scholar 

  47. 47.

    Pillai, B., Cherney, M. M., Hiraga, K., Takada, K., Oda, K., & James, M. N. G. (2007). Crystal structure of scytalidoglutamic peptidase with its first potent inhibitor provides insights into substrate specificity and catalysis. Journal of Molecular Biology, 365, 343–361.

    CAS  Article  Google Scholar 

  48. 48.

    Yabuki, Y., Kubota, K., Kojima, M., Inoue, H., & Takahashi, K. (2004). Identification of a glutamine residue essential for catalytic activity of aspergilloglutamic peptidase by site-directed mutagenesis. FEBS Letters, 569, 161–164.

    CAS  Article  Google Scholar 

  49. 49.

    Jensen, K., Østergaard, P. R., Wilting, R., & Lassen, S. F. (2010). Identification and characterization of a bacterial glutamic peptidase. BMC Biochemistry, 11, 1–12.

    Article  Google Scholar 

  50. 50.

    Hidalgo, M. E., Daroit, D. J., Corrêa, A. P. F., Pieniz, S., Brandelli, A., & Risso, P. H. (2012). Physicochemical and antioxidant properties of bovine caseinate hydrolysates obtained through microbial protease treatment. International Journal of Dairy Technology, 65, 342–352.

    CAS  Article  Google Scholar 

  51. 51.

    Carrasco-Castilla, J., Hernández-Álvarez, A. J., Jiménez-Martínez, C., Gutiérrez-López, G. F., & Dávila-Ortiz, G. (2012). Use of proteomics and peptidomics methods in food bioactive peptide science and engineering. Food Engineering Reviews, 4, 224–243.

    CAS  Article  Google Scholar 

  52. 52.

    Bhat, Z. F., Kumar, S., & Bhat, H. F. (2015). Bioactive peptides from egg: a review. Nutrition & Food Science, 45, 190–212.

  53. 53.

    De Castro, R. J. S., & Sato, H. H. (2014). Antioxidant activities and functional properties of soy protein isolate hydrolysates obtained using microbial proteases. International Journal of Food Science and Technology, 49, 317–328.

  54. 54.

    Coda, R., Rizzello, C. G., Pinto, D., & Gobbetti, M. (2012). Selected lactic acid bacteria synthesize antioxidant peptides during sourdough fermentation of cereal flours. Applied and Environmental Microbiology, 78, 1087–1096.

  55. 55.

    Corrêa, A. P. F., Daroit, D. J., Coelho, J., Meira, S. M. M., Lopes, F. C., Segalin, J., Risso, P. H., & Brandelli, A. (2011). Antioxidant, antihypertensive and antimicrobial properties of ovine milk caseinate hydrolyzed with a microbial protease. Journal of the Science of Food and Agriculture, 91, 2247–2254.

    Google Scholar 

  56. 56.

    Cheong, S. H., Kim, E.-K., Hwang, J-W., Kim, Y-S., Lee, J-S., Moon, S-H., et al. (2013). Purification of a novel peptide derived from a shellfish, Crassostrea gigas, and evaluation of its anticancer property. Journal of Agricultural and Food Chemistry, 61, 11442–11446.

  57. 57.

    Moraes, H. Á., Silvestre, M. P. C., Amorin, L. L., Silva, V. D. M., Silva, M. R., Simões e Silva, A. C., & Silveira, J. N. (2014). Use of different proteases to obtain whey protein concentrate hydrolysates with inhibitory activity toward angiotensin-converting enzyme. Journal of Food Biochemistry, 38, 102–109.

    Article  Google Scholar 

  58. 58.

    Lafarga, T., & Hayes, M. (2014). Bioactive peptides from meat muscle and by-products: generation functionality and application as functional ingredients. Meat Science, 98, 227–239.

  59. 59.

    Li-Chian, E. C. Y. (2015). Bioactive peptides and protein hydrolysates: research trends and challenges for application as nutraceuticals and functional food ingredients. Current Opinion in Food Science, 1, 28–37.

    Article  Google Scholar 

  60. 60.

    Dorado, J., Field, J. A., Almendros, G., & Sierra-Alvarez, R. (2001). Nitrogen-removal with protease as a method to improve the selective delignification of hemp stemwood by the white-rot fungus Bjerkandera sp. strain BOS55. Applied Microbiology and Biotechnology, 57, 205–211.

    CAS  Article  Google Scholar 

  61. 61.

    Ramirez-Bribiesca, J. E., Soto-Sanchiez, A., Hernandez-Calva, L. M., Salinas-Chavira, J., Galaviz-Rodriguez, J. R., Cruz-Monterrosa, R. G., et al. (2010). Influence of Pleurotus ostreatus spent corn straw on performance and carcass characteristics of feedlot Pelibuey lambs. Indian Journal of Animal Sciences, 80, 754–757.

  62. 62.

    Raghuwanshi, S., Misra, S., & Saxena, R. K. (2014). Treatment of wheat straw using tannase and white-rot fungus to improve feed utilization by ruminants. Journal of Animal Science and Biotechnology, 5, 1–8.

    Article  Google Scholar 

  63. 63.

    Staszczak, M., Zdunek, E., & Leonowicz, A. (2000). Studies on the role of proteases in the white-rot fungus Trametes versicolor: effect of PMSF and chloroquine on ligninolytic enzymes activity. Journal of Basic Microbiology, 40, 51–63.

    CAS  Article  Google Scholar 

  64. 64.

    Gupta, R., Beg, Q. K., & Lorenz, P. (2002). Bacterial alkaline proteases: molecular approaches and industrial application. Applied Microbiology and Biotechnology, 59, 15–32.

    CAS  Article  Google Scholar 

  65. 65.

    Sinha, R., Radha, C., Prakash, J., & Kaul, P. (2007). Whey protein hydrolysate: functional properties, nutritional quality and utilization in beverage formulation. Food Chemistry, 101, 1484–1491.

    CAS  Article  Google Scholar 

  66. 66.

    Fitzgerald, R. J., & O’Cuinn, G. (2006). Enzymatic debittering of food protein hydrolysates. Biotechnology Advances, 24, 234–237.

    CAS  Article  Google Scholar 

  67. 67.

    Hmidet, N., Ali, N. E.-H., Haddar, A., Kanoun, S., Kaomoun, S., & Nasri, M. (2009). Alkaline proteases and thermostable α-amylase co-produced by Bacillus licheniformis NH1: characterization and potential application as detergent additive. Biochemical Engineering Journal, 47, 71–79.

    CAS  Article  Google Scholar 

  68. 68.

    Rao, M. B., Tanksale, A. M., Ghatge, M. S., & Deshpande, V. V. (1998). Molecular and biotechnological aspects of microbial proteases. Microbiology and Molecular Biology Reviews, 62, 597–635.

  69. 69.

    Bonugli-Santos, R. C., Vasconcelos, M. R. S., Passarini, M. R. Z., Vieira, G. A. L., Lopes, V. C. P., Mainardi, P. H., Santos, J. Á., Duarte, L. A., Otero, I. V. R., Yoshida, M. A. S., Feitosa, V. A., Pessoa Jr., A., & Sette, L. D. (2015). Marine-derived fungi: diversity of enzymes and biotechnological applications. Frontiers in Microbiology, 6, 1–15.

    Article  Google Scholar 

  70. 70.

    Pandey, A. (2003). Solid-state fermentation. Biochemical Engineering Journal, 13, 81–84.

    CAS  Article  Google Scholar 

  71. 71.

    Muthulakshmi, C., Gomathi, D., Kumar, D. G., Ravikumar, G., Kalaiselvi, M., & Uma, C. (2011). Production, purification and characterization of protease by Aspergillus flavus under solid state fermentation. Jordan Journal of Biological Sciences, 4, 137–148.

    Google Scholar 

  72. 72.

    Sandhya, C., Sumantha, A., Szakacs, G., & Pandey, A. (2005). Comparative evaluation of neutral protease production by Aspergillus oryzae in submerged and solid-state fermentation. Process Biochemistry, 40, 2689–2694.

    CAS  Article  Google Scholar 

  73. 73.

    Kaur, S., Vohra, R. M., Kapoor, M., Beg, Q. K., & Hoondal, G. S. (2001). Enhanced production and characterization of a highly thermostable alkaline protease from Bacillus sp. P-2. World Journal of Microbiology and Biotechnology, 17, 125–129.

    CAS  Article  Google Scholar 

  74. 74.

    Prakasham, R. S., Rao, C. S., & Sarma, P. N. (2006). Green gram husk—an inexpensive substrate for alkaline protease production by Bacillus sp. in solid-state fermentation. Bioresource Technology, 97, 1449–1454.

    CAS  Article  Google Scholar 

  75. 75.

    Mahanta, N., Gupta, A., & Khare, S. K. (2008). Production of protease and lipase by solvent tolerant Pseudomonas aeruginosa PseA in solid-state fermentation using Jatropha curcas seed cake as substrate. Bioresource Technology, 99, 1729–1735.

    CAS  Article  Google Scholar 

  76. 76.

    Wu, F.-C., Chang, C.-W., & Shih, I.-L. (2013). Optimization of the production and characterization of milk clotting enzymes by Bacillus subtilis natto. Springer Plus, 2, 1–10.

    Article  Google Scholar 

  77. 77.

    Imdakim, M. M., Hassan, Z., Aween, M. M., Elshaafi, B. M., & Muhialdin, B. J. (2015). Milk clotting and proteolytic activity of enzyme preparation from Pediococcus acidilactici SH for dairy products. African Journal of Biotechnology, 14, 133–142.

    CAS  Article  Google Scholar 

  78. 78.

    Ahmetoglu, N., Bekler, F. M., Acer, O., Guven, R. G., & Guven, K. (2015). Production, purification and characterisation of thermostable metallo-protease from newly isolated Bacillus sp. KG5. Eurasian Journal of Biosciences. doi:10.5053/ejobios.2015.9.0.1.

  79. 79.

    Lakshmi, G., & Prasad, N. N. (2015). Purification and characterization of alkaline protease from a mutant Bacillus licheniformis Bl8. Advances in Biological Research, 9, 15–23.

    Google Scholar 

  80. 80.

    Tunga, R., Shrivastava, B., & Banerjee, R. (2003). Purification and characterization of a protease from solid state culture of Aspergillus parasiticus. Process Biochemistry, 38, 1553–1558.

    CAS  Article  Google Scholar 

  81. 81.

    Kumar, S., Sharma, N. S., Saharan, M. R., & Singh, R. (2005). Extracellular acid protease from Rhizopus oryzae: purification and characterization. Process Biochemistry, 40, 1701–1705.

    CAS  Article  Google Scholar 

  82. 82.

    Neto, Y. A. B. H., Freitas, L. A. P., & Cabral, H. (2014). Multivariate analysis of the stability of spray-dried Eupenicillium javanicum peptidases. Drying Technology, 32, 614–621.

    Article  Google Scholar 

  83. 83.

    Neto, A. A. H. N., Coitinho, L. B., Freitas, L. A. P., & Cabral, H. (2016). Box-Behnken analysis and storage of spray-dried collagenolytic proteases from Myceliophthora thermophila submerged bioprocess. Preparative Biochemistry and Biotechnology.

  84. 84.

    Ibrahim, A. S. S., Al-Salamah, A. A., El-Toni, A. M., Almaary, K. S., El-Tayeb, M. A., Elbadawi, Y. B., & Antranikian, G. (2016). Enhancement of alkaline protease activity and stability via covalent immobilization onto hollow core-mesoporous Shell silica nanospheres. International Journal of Molecular Sciences, 17, 184. doi:10.3390/ijms17020184.

    Article  Google Scholar 

  85. 85.

    Tanksale, A., Chandra, P. M., Rao, M., & Deshpande, V. (2001). Immobilization of alkaline protease from Conidiobolus macrosporus for reuse and improved thermal stability. Biotechnology Letters, 23, 51–54.

  86. 86.

    Nirmal, N. P., & Laxman, R. S. (2014). Enhanced thermostability of a fungal alkaline protease by different additives. Enzyme Research, 1–8. doi:10.1155/2014/109303.

  87. 87.

    Spahn, C., & Minteer, S. D. (2008). Enzyme immobilization in biotechnology. Recent Patents on Engineering, 2, 195–200.

    CAS  Article  Google Scholar 

  88. 88.

    Zhu, X., Zhou, T., Wu, X., Cai, Y., Yao, D., Xie, X., & Liu, D. (2011). Covalent immobilization of enzymes within micro-aqueous organic medium. Journal of Molecular Catalysis B: Enzymatic, 72, 145–149.

    CAS  Article  Google Scholar 

  89. 89.

    Li, W. F., Zhou, X. X., & Lu, P. (2005). Structural features of thermozymes. Biotechnology Advances, 23, 271–281.

    CAS  Article  Google Scholar 

  90. 90.

    Roca, M., Liu, H., Messer, B., & Warshel, A. (2007). On the relationship between thermal stability and catalytic power of enzymes. Biochemistry, 46, 15076–15088.

  91. 91.

    Gomes, E., Guez, M. A. U., Martin, N., & Da Silva, R. (2007). Enzimas termoestáveis: Fontes, Produção e Aplicação Industrial. Quimica Nova, 30, 136–145.

    CAS  Article  Google Scholar 

  92. 92.

    Panda, M. K., Sahu, M. K., & Tayung, K. (2013). Isolation and characterization of a thermophilic Bacillus sp. with protease activity isolated from hot spring of Tarabalo, Odisha, India. Iranian Journal of Microbiology, 5, 159–165.

  93. 93.

    Toplak, A., Wu, B., Fusetti, F., Quaedflieg, P. J. L. M., & Janssen, D. B. (2013). Proteolysin, a novel highly thermostable and cosolvent-compatible protease from the thermophilic bacterium Coprothermobacter proteolyticus. Applied and Environmental Microbiology, 79, 5625–5632.

    CAS  Article  Google Scholar 

  94. 94.

    Wilson, P., & Remigio, Z. (2012). Production and characterisation of protease enzyme produced by a novel moderate thermophilic bacterium (EP1001) isolated from an alkaline hot spring, Zimbabwe. African Journal of Microbiology Research, 6(27), 5542–5551.

  95. 95.

    Zanphorlin, L. M., Cabral, H., Arantes, E., Assis, D., Juliano, L., Juliano, M. A., Da Silva, R., Gomes, E., & Bonilla-Rodriguez, G. O. (2011). Purification and characterization of a new alkaline protease from the thermophilic fungus Myceliophthora sp. Process Biochemistry, 46, 2137–2143.

    CAS  Article  Google Scholar 

  96. 96.

    Hsiao, N-W., Chen, Y., Kuan, Y-C., Lee, Y-C., Lee, S-K., Chan, H-H., et al. (2014). Purification and characterization of an aspartic protease from the Rhizopus oryzae protease extract, peptidase R. Electronic Journal of Biotechnology, 17, 89–94.

  97. 97.

    Merheb-Dini, C., Gomes, E., Boscolo, M., & Da Silva, R. (2010). Production and characterization of a milk-clotting protease in the crude enzymatic extract from the newly isolated Thermomucor indicae-seudaticae N31 (milk-clotting protease from the newly isolated Thermomucor indicae-seudaticae N31). Food Chemistry, 120, 87–93.

    CAS  Article  Google Scholar 

  98. 98.

    Merheb-Dini, C., Garcia, G. A. C., Penna, A. L. B., Gomes, E., & Da Silva, R. (2012). Use of a new milk-clotting from Thermomucor indicae-seudaticae N31 as coagulant and changes during ripening of Prato cheese. Food Chemistry, 130, 859–865.

    CAS  Article  Google Scholar 

  99. 99.

    Merheb-Dini, C., Chaves, K. S., Gomes, E., Da Silva, R., & Gigante, M. L. (2016). Coalho cheese made with protease from Thermomucor indicae-seudaticae N31: technological potential of the new coagulant for the production of high-cooked cheese. Journal of Food Science. doi:10.1111/1750-3841.13217.

  100. 100.

    Maurer, K.-H. (2004). Detergent proteases. Current Opinion in Biotechnology, 15, 330–334.

    CAS  Article  Google Scholar 

  101. 101.

    Aoki, K., Matsubara, S., Umeda, M., Tachibanac, S., Doi, M., & Takenaka, S. (2013). Aspartic protease from Aspergillus (Eurotium) repens strain MK82 is involved in the hydrolysis and decolourisation of dried bonito (Katsuobushi). Journal of the Science of Food and Agriculture, 93, 1349–1355.

    CAS  Article  Google Scholar 

  102. 102.

    Kondo, M. Y., Okamoto, D. N., Santos, J. A. N., Juliano, M. A., Oda, K., Pillai, B., James, M. N. G., Juliano, L., & Gouvea, I. E. (2010). Studies on the catalytic mechanism of a glutamic peptidase. The Journal of Biological Chemistry, 285, 21437–21445.

    CAS  Article  Google Scholar 

  103. 103.

    Oliveira, C. F., Coletto, D., Correa, A. P. F., Daroit, D. J., Toniolo, R., Cladera-Olivera, F., & Brandelli, A. (2014). Antioxidant activity and inhibition of meat lipid oxidation by soy protein hydrolysates obtained with a microbial protease. International Food Research Journal, 21, 775–781.

    Google Scholar 

  104. 104.

    Fontoura, R., Daroit, D. J., Correa, A. P. F., Meira, S. M. M., Mosquera, M., & Brandelli, A. (2014). Production of feather hydrolysates with antioxidant, angiotensin-I converting enzyme and dipeptidyl peptidase-IV-inhibitory activities. New Biotechnology, 31, 506–513.

    CAS  Article  Google Scholar 

  105. 105.

    Elfahri, K. R., Donkor, O. N., & Vasiljevic, T. (2014). Potencial of novel Lactobacillus helveticus strains and their cell wall bound proteases to release physiologically active peptides from milk proteins. International Dairy Journal, 38, 37–46.

    CAS  Article  Google Scholar 

  106. 106.

    Chaves-López, C., Serio, A., Paparella, A., Martuscelli, M., Corsetti, A., Tofalo, R., & Suzzi, G. (2014). Impact of microbial cultures on proteolysis and release of bioactive peptides in fermented milk. Food Microbiology, 42, 117–121.

    Article  Google Scholar 

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Correspondence to Ronivaldo Rodrigues da Silva.

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da Silva, R.R. Bacterial and Fungal Proteolytic Enzymes: Production, Catalysis and Potential Applications. Appl Biochem Biotechnol 183, 1–19 (2017). https://doi.org/10.1007/s12010-017-2427-2

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Keywords

  • Bacteria
  • Bioprocess
  • Biotechnology
  • Fungi
  • Lyases
  • Proteolytic enzymes