The keratinolytic bacteria Bacillus cytotoxicus as a source of novel proteases and feather protein hydrolysates with antioxidant activities

Avdiyuk KV, Varvanets A (2019) Keratinolytic enzymes: producers, physical and chemical properties. Application for biotechnology. Biotechnol Acta 12:27–45 Verma A, Singh H, Anwar S, Chattopadhyay A, Tiwari KK, Kaur S, Dhilon GS (2017) Microbial keratinases: industrial enzymes with waste management potential. Crit Rev Biotechnol 37(4):476–491. https://doi.org/10.1080/07388551.2016.1185388 Callegaro K, Brandelli A, Daroit DJ (2019) Beyond plucking: feathers bioprocessing into valuable protein hydrolysates. Waste Manag 95:399–415. https://doi.org/10.1016/j.wasman.2019.06.040 Friedrich AB, Antranikian G (1996) Keratin degradation by Fervidobacterium pennovorans, a novel thermophilic anaerobic species of the order Thermotogales. Appl Environ Microbiol 62(8):2875–2882. https://doi.org/10.1128/aem.62.8.2875-2882.1996 Nam GW, Lee DW, Lee HS, Lee NJ, Kim BC, Choe EA, Hwang JK, Suhartono MT, Pyun YR (2002) Native feather degradation by Fervidobacterium islandicum AW-1, a newly isolated keratinase-producing thermophilic anaerobe. Arch Microbiol 178(6):538–547. https://doi.org/10.1007/s00203-002-0489-0 Riessen S, Antranikian G (2001) Isolation of Thermoanaerobacter keratinophilus sp. nov.; a novel thermophilic, anaerobic bacterium with keratinolytic activity. Extremophiles 5(6):399–408. https://doi.org/10.1007/s007920100209 Kublanov I, Perevalova A, Slobodkina G, Lebedinsky A, Bidzhieva S, Kolganova T, Kaliberda E, Rumsh L, Haertle T, Bonch-Osmolovskaya E (2009) Biodiversity of thermophilic prokaryotes with hidrolytic activities in hot springs of Uzon Caldera, Kamchatka (Russia). Appl Environ Microbiol 75(1):286–291. https://doi.org/10.1128/AEM.00607-08 Ionata E, Canganella F, Bianconi G, Benno Y, Sakamoto M, Capasso A, Rossi M, La Cara F (2008) A novel keratinase from Clostridium sporogenes bv. pennavorans bv. nov., a thermotolerant organism isolated from solfataric muds. Microbiol Res 163(1):105–112. https://doi.org/10.1016/j.micres.2006.08.001 Matsui T, Yamada Y, Mitsuya H, Shigeri Y, Yoshida Y, Saito Y, Matsui H, Watanabe K (2009) Sustainable and practical degradation of intact chicken feathers by cultivating a newly isolated thermophilic Meiothermus ruber H328. Appl Microbiol Biotechnol 82(5):941–950. https://doi.org/10.1007/s00253-009-1880-4 Guinebretiere MH, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of Bacillus cereus Group occasionally associated with food poisoning. Int J Syst Evol Microbiol 63(Pt_1):31–40. https://doi.org/10.1099/ijs.0.030627-0 Cavello I, Urbieta MS, Cavalitto SF, Donati E (2020) Bacillus cytotoxicus isolated from a pristine natural geothermal area reveals high keratinolytic activity. Microorganisms 8:1–13. https://www.mdpi.com/2076-2607/8/6/796 Cavello I, Cavalitto S, Hours R (2012) Biodegradation of a keratin waste and the concomitant production of detergent stable serine proteases from Paecilomyces lilacinus. Appl Biochem Biotechnol 167(5):945–958. https://doi.org/10.1007/s12010-012-9650-7 Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3 García-Carreño FL, Dimes LE, Haard NF (1993) Substrate-gel electrophoresis for composition and molecular weight of proteinases or proteinaceous proteinase inhibitors. Anal Biochem 214(1):65–69. https://doi.org/10.1006/abio.1993.1457 Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685. https://doi.org/10.1038/227680a0 Dyballa N, Metzger S (2009) Fast and sensitive colloidal coomassie G-250 staining for proteins in polyacrylamide gels. J Vis Exp (30):e1431. https://doi.org/10.3791/1431 Yildirim A, Mavi A, Oktay M, Kara A, Algur O, Bilaloglu V (2000) Comparison of antioxidant and antimicrobial activities of tilia (Tilia argentea Desf ex DC), sage (Salvia triloba l.), and black tea (Camellia sinensis) extracts. J Agric Food Chem 48(10):5030–5034. https://doi.org/10.1021/jf000590k Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9-10):1231–1237. https://doi.org/10.1016/S0891-5849(98)00315-3 Chiacchiarini P, Lavalle L, Giaveno A, Donati E (2010) First assessment of acidophilic microorganisms from geothermal Copahue-Caviahue system. Hydrometallurgy 104(3-4):334–341. https://doi.org/10.1016/j.hydromet.2010.02.020 Urbieta MS, González Toril E, Giaveno MA, Aguilera Bazán A, Donati E (2014) Archeal and bacterial diversity in five different hydrothermal ponds in the Copahue region in Argentina. Syst Appl Microbiol 37(6):429–441. https://doi.org/10.1016/j.syapm.2014.05.012 Urbieta MS, González-Toril E, Bazán ÁA, Giaveno MA, Donati E (2015) Comparison of the microbial communities of hot springs waters and the microbial biofilms in the acidic geothermal area of Copahue (Neuqu+®n, Argentina). Extremophiles 19(2):437–450. https://doi.org/10.1007/s00792-015-0729-2 Cavello I, Urbieta MS, Segretin AB, Giaveno A, Cavalitto S, Donati ER (2018) Assessment of keratinase and other hydrolytic enzymes in thermophilic bacteria isolated from geothermal areas in Patagonia Argentina. Geomicrobiol J 35(2):156–165. https://doi.org/10.1080/01490451.2017.1339144 Lima MA, Urbieta MS, Donati E (2019) Arsenic-tolerant microbial consortia from sediments of Copahue geothermal system with potential applications in bioremediation. J Basic Microbiol 59(7):680–691. https://doi.org/10.1002/jobm.201800628 Williams CM, Richter CS, Mackenzie JM, Shih JC (1990) Isolation, identification and characterization of a feather-degrading bacterium. Appl Environ Microbiol 56(6):1509–1515. https://doi.org/10.1128/aem.56.6.1509-1515.1990 Manczinger L, Rozs M, Vavolgyi C, Kevei F (2003) Isolation and characterization of a new keratinolytic Bacillus licheniformis strain. World J Microbiol Biotechnol 19(1):35–39. https://doi.org/10.1023/A:1022576826372 Rai SK, Konwarh R, Mukherjee AK (2009) Purification, characterization and biotechnological application of an alkaline β-keratinase produced by Bacillus subtilis RM-01 in solid-state fermentation using chicken-feather as substrate. Biochem Eng J 45(3):218–225. https://doi.org/10.1016/j.bej.2009.04.001 Bihari Z, Vidéki E, Mihalik A, Szvetnik Z, Szabó M, Kesseru P, Kiss I (2010) Degradation of native feathers by a novel keratinase-producing, thermophilic Iisolate, Brevibacillus thermoruber T1E. Z Naturforsch C 65(1-2):134–140. https://doi.org/10.1515/znc-2010-1-221 Shrinivas D, Naik GR (2011) Characterization of alkaline thermostable keratinolytic protease from thermoalkalophilic Bacillus halodurans JB 99 exhibiting dehairing activity. Int Biodeterior Biodegradation 65(1):29–35. https://doi.org/10.1016/j.ibiod.2010.04.013 Bouacem K, Bouanane-Darenfed A, Zarai Jaouadi N, Joseph M, Hacene H, Ollivier B, Fardeau ML, Bejar S, Jaouadi B (2016) Novel serine keratinase from Caldicoprobacter algeriensis exhibiting outstanding hide dehairing abilities. Int J Biol Macromol 86:321–328. https://doi.org/10.1016/j.ijbiomac.2016.01.074 Sivakumar T, Shankar T, Thangapandian V, Ramasubramanian V (2013) Optimization of cultural condition for keratinase production using Bacillus cereus TS1. Insight Microbiol 3(1):1–8. https://doi.org/10.5567/IMICRO-IK.2013.1.8 Lateef A, Oloke JK, Gueguim Kana EB, Sobowale BO, Ajao SO, Bello BY (2010) Keratinolytic activities of a new feather-degrading isolate of Bacillus cereus LAU 08 isolated from Nigerian soil. Int Biodeterior Biodegradation 64(2):162–165. https://doi.org/10.1016/j.ibiod.2009.12.007 Fakhfakh-Zouari N, Haddar A, Hmidet N, Frikha F, Nasri M (2010) Application of statistical experimental design for optimization of keratinases production by Bacillus pumilus A1 grown on chicken feather and some biochemical properties. Process Biochem 45(5):617–626. https://doi.org/10.1016/j.procbio.2009.12.007 Sahoo DK, Das A, Thatoi H, Mondal KC, Mohapatra PKD (2012) Keratinase production and biodegradation of whole chicken feather keratin by a newly isolated bacterium under submerged fermentation. Appl Biochem Biotechnol 167(5):1040–1051. https://doi.org/10.1007/s12010-011-9527-1 Cg C, Js C, Jj Q, Yin Y, Zheng X (2008) Purification and characterization of keratinase from a new Bacillus subtilis strain. J Zhejiang Univ Sci B 9:713–720 Abdel-Naby MA, El-Refai HA, Ibrahim MHA (2017) Structural characterization, catalytic, kinetic and thermodynamic properties of Keratinase from Bacillus pumilus FH9. Int J Biol Macromol 105(Pt 1):973–980. https://doi.org/10.1016/j.ijbiomac.2017.07.118 Hamiche S, Mechri S, Khelouia L, Annane R, El Hattab M, Badis A, Jaouadi B (2019) Purification and biochemical characterization of two keratinases from Bacillus amyloliquefaciens S13 isolated from marine brown alga Zonaria tournefortii with potential keratin-biodegradation and hide-unhairing activities. Int J Biol Macromol 122:758–769. https://doi.org/10.1016/j.ijbiomac.2018.10.174 Emran MA, Ismail SA, Hashem AM (2020) Production of detergent stable thermophilic alkaline protease by Bacillus licheniformis ALW1. Biocatal Agric Biotechnol 26:101631 Jaouadi B, Abdelmalek B, Fodil D, Ferradji FZ, Rekik H, Zara N, Bejar S (2010) Purification and characterization of a thermostable keratinolytic serine alkaline proteinase from Streptomyces sp. strain AB1 with high stability in organic solvents. Bioresour Technol 101(21):8361–8369. https://doi.org/10.1016/j.biortech.2010.05.066 Habbeche A, Saoudi B, Jaouadi B, Haberra S, Kerouaz B, Boudelaa M, Badis A, Ladjama A (2014) Purification and biochemical characterization of a detergent-stable keratinase from a newly thermophilic actinomycete Actinomadura keratinilytica strain Cpt29 isolated from poultry compost. J Biosci Bioeng 117(4):413–421. https://doi.org/10.1016/j.jbiosc.2013.09.006 Abdel-Fattah AM, El-Gamal MS, Ismail SA, Emran MA, Hashem AM (2018) Biodegradation of feather waste by keratinase produced from newly isolated Bacillus licheniformis ALW1. J Genet Eng Biotechnol 16(2):311–318. https://doi.org/10.1016/j.jgeb.2018.05.005 Daroit DJ, Correa AP, Brandelli A (2011) Production of keratinolytic proteases through bioconversion of feather meal by the Amazonian bacterium Bacillus sp. P45. Int Biodeterior Biodegradation 65(1):45–51. https://doi.org/10.1016/j.ibiod.2010.04.014 Bhari R, Kaur M, Singh RS (2019) Thermostable and halotolerant keratinase from Bacillus aerius NSMk2 with remarkable dehairing and laundary applications. J Basic Microbiol 59(6):555–568. https://doi.org/10.1002/jobm.201900001 Tork SE, Shahein YE, El-Hakim AE, Abdel-Aty AM, Aly MM (2013) Production and characterization of thermostable metallo-keratinase from newly isolated Bacillus subtilis NRC 3. Int J Biol Macromol 55:169–175. https://doi.org/10.1016/j.ijbiomac.2013.01.002 Collins T, Meuwis MA, Gerday C, Feller G (2003) Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J Mol Biol 328(2):419–428. https://doi.org/10.1016/S0022-2836(03)00287-0 Hashem AM, Abdel-Fattah A, Ismail S, El-Gamal M, Esawy M, Emran MA (2018) Optimization, characterization and thermodynamic studies on B. licheniformis ALW1 keratinase. Egypt J Chem 61:591–607 Hammami A, Fakhfakh N, Abdelhedi O, Nasri M, Bayoudh A (2018) Proteolytic and amylolytic enzymes from a newly isolated Bacillus mojavensis SA: characterization and applications as laundry detergent additive and in leather processing. Int J Biol Macromol 108:56–68. https://doi.org/10.1016/j.ijbiomac.2017.11.148 Ferrareze PAG, Correa APF, Brandelli A (2016) Purification and characterization of a keratinolytic protease produced by probiotic Bacillus subtilis. Biocatal Agric Biotechnol 7:102–109. https://doi.org/10.1016/j.bcab.2016.05.009 Gegeckas A, Simkute A, Gudiukaité R, Citavicius DJ (2018) Characterization and application of keratinolytic paptidases from Bacillus spp. Int J Biol Macromol 113:1206–1213. https://doi.org/10.1016/j.ijbiomac.2018.03.046 Thys RCS, Brandelli A (2006) Purification and properties of a keratinolytic metalloprotease from Microbacterium sp. J Appl Microbiol 101(6):1259–1268. https://doi.org/10.1111/j.1365-2672.2006.03050.x Lee H, Suh DB, Hwang JH, Suh HJ (2002) Characterization of a kerationlytic metalloprotease from Bacillus sp. SCB-3. Appl Biochem Biotechnol 97(2):123–133. https://doi.org/10.1385/ABAB:97:2:123 Balaji S, Senthil Kumar M, Karthikeyan R, Kumar R, Kirubanandan S, Sridhar R, Sehgal PK (2008) Purification and characterization of an extracellular keratinase from a hornmeal-degrading Bacillus subtilis MTCC (9102). World J Microbiol Biotechnol 24(11):2741–2745. https://doi.org/10.1007/s11274-008-9782-7 Laba W, Rodziewicz A (2010) Keratinolytic potential of feather-degrading Bacillus polymyxa and Bacillus cereus. Pol J Environ Stud 19:371–378 Nnolim NE, Nwodo UU (2020) Bacillus sp. CSK2 produced thermostable alkaline keratinase using agro-wastes: keratinolytic enzyme characterization. BMC Biotechnol 20:65 Mhamdi S, Bkhairia I, Nasri R, Mechichi T, Nasri M, Kamoun AS (2017) Evaluation of the biotechnological potential of a novel purified protease BS1 from Bacillus safensis S406 on the chitin extraction and detergent formulation. Int J Biol Macromol 104(Pt A):739–747. https://doi.org/10.1016/j.ijbiomac.2017.06.062 Rahman RNZRA, Mahamad S, Salleh AB, Basri M (2007) A new organic solvent tolerant protease from Bacillus pumilus 115b. J Ind Microbiol Biotechnol 34(7):509–517. https://doi.org/10.1007/s10295-007-0222-8 Brandelli A, Daroit DJ, Riffel A (2010) Biochemical features of microbial keratinases and their production and applications. Appl Microbiol Biotechnol 85(6):1735–1750. https://doi.org/10.1007/s00253-009-2398-5 More S, Prakash S, Umashankar S, Vishwakarma J (2013) Purification and properties of a novel fungal alkaline keratinase from Cunninghamella echinulata. Turkish J Biochem 38(1):68–74. https://doi.org/10.5505/tjb.2013.37928 Wang L, Qian Y, Cao Y, Huang Y, Chang Z, Huang H (2017) Production and characterization of keratinolytic proteases by a chicken feather-degrading thermophilic strain, Thermoactinomyces sp. YT06. J Microbiol Biotechnol 27(12):2190–2198. https://doi.org/10.4014/jmb.1705.05082 Paul T, Das A, Mandal A, Halder SK, Jana A, Maity C, DasMohapatra PK, Pati BR, Mondal KC (2014) An efficient cloth cleaning properties of a crude keratinase combined with detergent: towards industrial viewpoint. J Clean Prod 66:672–684. https://doi.org/10.1016/j.jclepro.2013.10.054 Ramakrishna Reddy M, Sathi Reddy K, Ranjita Chouhan Y, Bee H, Reddy G (2017) Effective feather degradation and keratinase production by Bacillus pumilus GRK for its application as bio-detergent additive. Bioresour Technol 243:254–263. https://doi.org/10.1016/j.biortech.2017.06.067 Callegaro K, Welter N, Daroit DJ (2018) Feathers as bioresource: microbial conversion into bioactive protein hydrolysates. Process Biochem 75:1–9. https://doi.org/10.1016/j.procbio.2018.09.002 Fontoura R, Daroit DJ, Correa APF, Meira SMM, Mosquera M, Brandelli A (2014) Production of feather hydrolysates with antioxidant, angiotensin-I converting enzyme- and dipeptidyl peptidase-IV-inhibitory activities. New Biotechnol 31(5):506–513. https://doi.org/10.1016/j.nbt.2014.07.002 Fagerlund A, Brillard J, First R, Guinebretiere MH, Granum PE (2007) Toxin production in a rare and genetically remote cluster of strains of the Bacillus cereus group. BMC Microbiol 7:43