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Selective biodegradation of recalcitrant black chicken feathers by a newly isolated thermotolerant bacterium Pseudochrobactrum sp. IY-BUK1 for enhanced production of keratinase and protein-rich hydrolysates

  • Ibrahim YusufEmail author
  • Lawal Garba
  • Mustapha Ahmad Shehu
  • Aminat Musa Oyiza
  • Muhammad Rabiu Kabir
  • Musa Haruna
Original Article
  • 16 Downloads

Abstract

Black chicken feathers generated in large amount from poultry and slaughter houses are highly recalcitrant to microbial degradation due to their tough structural nature. A novel keratinolytic bacterium that possessed high affinity for black feather was isolated from chicken manure and identified as Pseudochrobactrum sp. IY-BUK1. Keratinase and feather soluble protein were effectively produced by the free living cells of the bacterium in media containing only black feathers and a mixture of equal amount of black-, brown- and white-coloured feathers. Complete degradation of 5 g/L of black feathers was completed in 3 days following optimisation of physico-chemical conditions. However, the bacterium selectively completed the degradation of black feather in a medium containing mixture of feathers in 144 h leaving behind approximately 33% and 45% of brown and white feathers in the medium respectively. Gellan gum-immobilised cells of strain IY-BUK1 enhanced the keratinase production by about 150% and were used repeatedly for ten cycles to degrade 5 g/L of black feather in a semi continuous fermentation of 18 h per cycle with enhanced and stable production of soluble protein. The study demonstrated the potential use of Pseudochrobactrum sp. IY-BUK1 not only in biodegradation of highly recalcitrant black feathers, but also in producing keratinase enzymes and valuable soluble proteins for possible industrial usage.

Keywords

Pseudochrobactrum sp. IY-BUK1 Feather degradation Keratinase Melanised feathers Immobilisation Gellan gum 

Notes

Acknowledgements

The authors wish to acknowledge the heads of Microbiology, Biochemistry and Centre for Biotechnology research for providing the facilities to carry out the work.

Funding information

The project was partially supported financially by Bayero University Kano, Nigeria.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adinarayana K, Jyothi B, Ellaiah P (2005) Production of alkaline protease with immobilized cells of Bacillus subtilis PE-11 in various matrices by entrapment technique. AAPS PharmSciTech 6:E391–E397.  https://doi.org/10.1208/pt060348 CrossRefGoogle Scholar
  2. Ahmad S, Shamaan N, Arif N (2012) Enhanced phenol degradation by immobilized Acinetobacter sp. strain AQ5NOL 1. World J Microbiol Biotechnol 28:347–352CrossRefGoogle Scholar
  3. Barrowclough G, Sibley F (1980) Feather pigmentation and abrasion: test of a hypothesis. Auk 881–883Google Scholar
  4. Bhange K, Chaturvedi V, Bhatt R (2016) Feather degradation potential of Stenotrophomonas maltophilia KB13 and feather protein hydrolysate (FPH) mediated reduction of hexavalent chromium. 3 Biotech 6:42.  https://doi.org/10.1007/s13205-016-0370-5 CrossRefGoogle Scholar
  5. Bhari R, Kaur M, Singh RS, Pandey A, Larroche C (2018) Bioconversion of chicken feathers by Bacillus aerius NSMk2: a potential approach in poultry waste management. Bioresour Technol Rep 3:224–230.  https://doi.org/10.1016/J.BITEB.2018.07.015 CrossRefGoogle Scholar
  6. Brenner DJ, Krieg N, Garrity G, Staley J (2005) The proteobacteria, part B: the gammaproteobacteria. In: Bergey’s Manual of Systematic Bacteriology, vol 2. Springer, p 323e376Google Scholar
  7. Burtt EH Jr, Schroeder MR, Smith LA, Sroka JE, McGraw KJ (2011) Colourful parrot feathers resist bacterial degradation. Biol Lett 7:214–216.  https://doi.org/10.1098/rsbl.2010.0716 CrossRefGoogle Scholar
  8. Butler M (2004) Are melanized feather barbs stronger? J Exp Biol 207:285–293.  https://doi.org/10.1242/jeb.00746 CrossRefGoogle Scholar
  9. Călin M, Constantinescu-Aruxandei D, Alexandrescu E, Răut I, Doni MB, Arsene ML, Oancea F, Jecu L, Lazăr V (2017) Degradation of keratin substrates by keratinolytic fungi. Electron J Biotechnol 28:101–112.  https://doi.org/10.1016/J.EJBT.2017.05.007 CrossRefGoogle Scholar
  10. Cao ZJ, Zhang Q, Wei D-K, Chen L, Wang J, Zhang XQ, Zhou MH (2009) Characterization of a novel Stenotrophomonas isolate with high keratinase activity and purification of the enzyme. J Ind Microbiol Biotechnol 36:181–188.  https://doi.org/10.1007/s10295-008-0469-8 CrossRefGoogle Scholar
  11. Cappuccino J.G. Sherman N (1996) Microbiology-A laboratory manual (Vol. 9). Benjamin Cummings Science Publishing, Carlifonia. p 471Google Scholar
  12. Chaturvedi V, Bhange K, Bhatt R, Verma P (2014) Production of kertinases using chicken feathers as substrate by a novel multifunctional strain of Pseudomonas stutzeri and its dehairing application. Biocatal Agric Biotechnol 3:167–174.  https://doi.org/10.1016/j.bcab.2013.08.005 CrossRefGoogle Scholar
  13. Chaudhari PN, Chaudhari BL, Chincholkar SB (2013) Iron containing keratinolytic metallo-protease produced by Chryseobacterium gleum. Process Biochem 48:144–151.  https://doi.org/10.1016/j.procbio.2012.11.009 CrossRefGoogle Scholar
  14. Corrêa APF, Daroit DJ, Brandelli A (2010) Characterization of a keratinase produced by Bacillus sp. P7 isolated from an Amazonian environment. Int Biodeterior Biodegradation 64:1–6.  https://doi.org/10.1016/j.ibiod.2009.06.015 CrossRefGoogle Scholar
  15. Dahloum L, Yakubu A, Halbouche M (2018) Effects of housing system and plumage colour on egg quality characteristics of indigenous naked-neck chickens. Livest Res Rural Dev 30:206 Retrieved from http://www.lrrd.org/lrrd30/12/abdul30206.html. Accessed 11 Apr 2019
  16. de Oliveira CT, Pellenz L, Pereira JQ, Brandelli A, Daroit DJ (2016) Screening of bacteria for protease production and feather degradation. Waste Biomass Valoriz 7:447–453.  https://doi.org/10.1007/s12649-015-9464-2 CrossRefGoogle Scholar
  17. Ferrareze P, Correa A, Brandelli A (2016) Purification and characterization of a keratinolytic protease produced by probiotic Bacillus subtilis. Biocatal Agric Biotechnol 7:102–109CrossRefGoogle Scholar
  18. Gessesse A, Hatti-Kaul R, Gashe BA, Mattiasson B (2003) Novel alkaline proteases from alkaliphilic bacteria grown on chicken feather. Enzym Microb Technol 32:519–524.  https://doi.org/10.1016/S0141-0229(02)00324-1 CrossRefGoogle Scholar
  19. Ghaffar I, Imtiaz A, Hussain A, Javid A, Jabeen F, Akmal M, Qazi JI (2018) Microbial production and industrial applications of keratinases: an overview. Int Microbiol 21:163–174.  https://doi.org/10.1007/s10123-018-0022-1 CrossRefGoogle Scholar
  20. Goldstein G, Flory K, Browne B, Majid S (2004) Bacterial degradation of black and white feathers. Auk 121:656–659CrossRefGoogle Scholar
  21. Grande JM, Negro JJ, Torres MJ (2004) The evolution of bird plumage colouration: a role for feather-degradation bacteria? Ardeola 51:375–383Google Scholar
  22. Gunderson A, Frame A (2008) Resistance of melanized feathers to bacterial degradation: is it really so black and white? J Avian Biol 39:539–545CrossRefGoogle Scholar
  23. Gurav RG, Tang J, Jadhav JP (2016) Sulfitolytic and keratinolytic potential of Chryseobacterium sp. RBT revealed hydrolysis of melanin containing feathers. 3 Biotech 6:145.  https://doi.org/10.1007/s13205-016-0464-0 CrossRefGoogle Scholar
  24. Jacob S, Colmas L, Parthuisot N, Heeb P (2014) Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits. Naturwissenschaften 101:929–938.  https://doi.org/10.1007/s00114-014-1234-7 CrossRefGoogle Scholar
  25. Jeong J-H, Jeon Y-D, Lee OM, Kim JD, Lee NR, Park GT, Son HJ (2010a) Characterization of a multifunctional feather-degrading Bacillus subtilis isolated from forest soil. Biodegradation 21:1029–1040.  https://doi.org/10.1007/s10532-010-9363-y CrossRefGoogle Scholar
  26. Jeong J-H, Oh D-J, Hwang D-Y, Kim H-S, Park K-H, Lee C-Y, Son H-J (2010b) Keratinolytic enzyme-mediated biodegradation of recalcitrant feather by a newly isolated Xanthomonas sp. P5. Polym Degrad Stab 95:1969–1977CrossRefGoogle Scholar
  27. Joshi S, Tejashwini M, Revati N (2007) Isolation, identification and characterization of a feather degrading bacterium. Int J Poult Sci 6:689–693CrossRefGoogle Scholar
  28. Justyn NM, Peteya JA, D’Alba L, Shawkey MD (2017) Preferential attachment and colonization of the keratinolytic bacterium Bacillus licheniformis on black- and white-striped feathers. Auk 134:466–473.  https://doi.org/10.1642/AUK-16-245.1 CrossRefGoogle Scholar
  29. Korkmaz H, Hür H, Di S (2004) Characterization of alkaline keratinase of Bacillus licheniformis strain HK-1 from poultry waste. Ann Microbiol 54:201–211Google Scholar
  30. Kshetri P, Roy SS, Sharma SK, Singh TS, Ansari MA, Prakash N, Ngachan SV (2017) Transforming chicken feather waste into feather protein hydrolysate using a newly isolated multifaceted keratinolytic bacterium Chryseobacterium sediminis RCM-SSR-7. Waste Biomass Valoriz 10:1–11.  https://doi.org/10.1007/s12649-017-0037-4 CrossRefGoogle Scholar
  31. Kumar EV, Vijay M, Srijana K, Chaitanya Y, Reddy HK, Reddy G (2011a) Biodegradation of poultry feathers by a novel bacterial isolate Bacillus altitudinis GVC11. Indian J Biotechnol 10:502–507Google Scholar
  32. Kumar E, Srijana M, Kumar K (2011b) A novel serine alkaline protease from Bacillus altitudinis GVC11 and its application as a dehairing agent. Bioprocess Biosyst Eng 34:403–409CrossRefGoogle Scholar
  33. Łaba W, Żarowska B, Chorążyk D, Pudło A, Piegza M, Kancelista A, Kopeć W (2018) New keratinolytic bacteria in valorization of chicken feather waste. AMB Express 8:9.  https://doi.org/10.1186/s13568-018-0538-y CrossRefGoogle Scholar
  34. Lasekan A, Abu F, Hashim D (2013) Potential of chicken by-products as sources of useful biological resources. Waste Manag 33:552–565.  https://doi.org/10.1016/j.wasman.2012.08.001 CrossRefGoogle Scholar
  35. Lowry OC, Rosebrough N (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265Google Scholar
  36. Lv LX, Sim MH, Li YD, Min J, Feng WH, Guan WJ, Li YQ (2010) Production, characterization and application of a keratinase from Chryseobacterium L99 sp. nov. Process Biochem 45:1236–1244.  https://doi.org/10.1016/j.procbio.2010.03.011 CrossRefGoogle Scholar
  37. Mariyammal A, Ezhilarasu A, Karthy ES, Menaga D (2018) Purification and characterization of novel extracellular keratinase enzyme from poultry feather waste. Int J Curr Res Life Sci 7:1018–1024Google Scholar
  38. McGraw K (2006) Mechanics of uncommon colors: pterins, porphyrins, and psittacofulvins. Bird Color 1:354–398Google Scholar
  39. Moslemy P, Neufeld RJ, Millette D, Guiot SR (2003) Transport of gellan gum microbeads through sand: an experimental evaluation for encapsulated cell bioaugmentation. J Environ Manag 69:249–259.  https://doi.org/10.1016/j.jenvman.2003.09.003 CrossRefGoogle Scholar
  40. Nagarajan S, Eswaran P, Masilamani RP, Natarajan H (2017) Chicken feather compost to promote the plant growth activity by using keratinolytic bacteria. Waste Biomass Valoriz 9:531–538.  https://doi.org/10.1007/s12649-017-0004-0 CrossRefGoogle Scholar
  41. Ningthoujam SD, Tamreihao K, Mukherjee S, et al (2018) Keratinaceous wastes and their valorization through keratinolytic microorganisms in keratin. IntechOpenGoogle Scholar
  42. Nwogu S (2017) Local farmers produce 30% of Nigeria’s poultry demand. Punch Newspaper, Published September 1, 2017. https://punchng.com/local-farmers-produce-30-of-nigerias-poultry-demand/. Accessed on 3/4/2019
  43. Okoroma EA, Garelick H, Abiola OO, Purchase D (2012) Identification and characterisation of a Bacillus licheniformis strain with profound keratinase activity for degradation of melanised feather. Int Biodeterior Biodegradation 74:54–60.  https://doi.org/10.1016/j.ibiod.2012.07.013 CrossRefGoogle Scholar
  44. Peng Z, Zhang J, Du G, Chen J (2019) Keratin waste recycling based on microbial degradation: mechanisms and prospects. ACS Sustain Chem Eng 7:9727–9736.  https://doi.org/10.1021/acssuschemeng.9b01527 CrossRefGoogle Scholar
  45. Prakash P, Jayalakshmi SK, Sreeramulu K (2010) Production of keratinase by free and immobilized cells of Bacillus halodurans strain PPKS-2: partial characterization and its application in feather degradation and dehairing of the goat skin. Appl Biochem Biotechnol 160:1909–1920.  https://doi.org/10.1007/s12010-009-8702-0 CrossRefGoogle Scholar
  46. Ramarosandratana A, Harvengt L, Bouvet A, Calvayrac R, Pâques M (2001) Effects of carbohydrate source, polyethylene glycol and gellan gum concentration on embryonal-suspensor mass (ESM) proliferation and maturation of maritime pine somatic embryos. Vitr Cell Dev Biol Plant 37:29–34.  https://doi.org/10.1007/s11627-001-0006-1 CrossRefGoogle Scholar
  47. Ramnani P, Gupta R (2004) Optimization of medium composition for keratinase production on feather by Bacillus licheniformis RG1 using statistical methods involving response surface methodology. Biotechnol Appl Biochem 40:191–196.  https://doi.org/10.1042/BA20030228 CrossRefGoogle Scholar
  48. Ramnani P, Singh R, Gupta R (2005) Keratinolytic potential of Bacillus licheniformis RG1: structural and biochemical mechanism of feather degradation. Can J Microbiol 51:191–196.  https://doi.org/10.1139/w04-123 CrossRefGoogle Scholar
  49. Riffel A, Brandelli A (2006) Keratinolytic bacteria isolated from feather waste. Braz J Microbiol 37:395–399.  https://doi.org/10.1590/S1517-83822006000300036 CrossRefGoogle Scholar
  50. 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 167:1040–1051.  https://doi.org/10.1007/s12010-011-9527-1 CrossRefGoogle Scholar
  51. Shrinivas D, Kumar R, Naik G (2012) Enhanced production of alkaline thermostable keratinolytic protease from calcium alginate immobilized cells of thermoalkalophilic Bacillus halodurans JB 99. J Ind Microbiol Biotechnol 39:93–98CrossRefGoogle Scholar
  52. Sun W, Griffiths MW (2000) Survival of bifidobacteria in yogurt and simulated gastric juice following immobilization in gellan–xanthan beads. Int J Food Microbiol 61:17–25.  https://doi.org/10.1016/S0168-1605(00)00327-5 CrossRefGoogle Scholar
  53. Tatineni R, Doddapaneni K, Potumarthi R, Mangamoori L (2007) Optimization of keratinase production and enzyme activity using response surface methodology with Streptomyces sp. 7. Appl Biochem Biotechnol 141:187–201.  https://doi.org/10.1007/BF02729061 CrossRefGoogle Scholar
  54. Tiwary E, Gupta R (2010) Medium optimization for a novel 58 kDa dimeric keratinase from Bacillus licheniformis ER-15: biochemical characterization and application in feather degradation and dehairing of hides. Bioresour Technol 101:6103–6110.  https://doi.org/10.1016/j.biortech.2010.02.090 CrossRefGoogle Scholar
  55. Tuna A, Okumuş Y, Çelebi H, Seyhan AT (2015) Thermochemical conversion of poultry chicken feather fibers of different colors into microporous fibers. J Anal Appl Pyrolysis 115:112–124.  https://doi.org/10.1016/j.jaap.2015.07.008 CrossRefGoogle Scholar
  56. Vuillemard J-C, Terré S, Benoit S, Amiot J (1988) Protease production by immobilized growing cells of Serratia marcescens and Myxococcus xanthus in calcium alginate gel beads. Appl Microbiol Biotechnol 27:423–431.  https://doi.org/10.1007/BF00451607 CrossRefGoogle Scholar
  57. Wang T, Liang C, Sun Y, Gao W, Luo X, Gao Q, Li R, Fu S, Xu H, He T, Yuan H (2018) Strategical isolation of efficient chicken feather–degrading bacterial strains from tea plantation soil sample. Int Microbiol 22:227–237.  https://doi.org/10.1007/s10123-018-00042-4 CrossRefGoogle Scholar
  58. Yusuf I, Shukor MY, Yee PL et al (2014) Biodegradation of chicken feather wastes in submerged fermentation containing high concentrations of heavy metals by Bacillus sp. khayat. J Environ Bioremed Toxicol 2:38–41Google Scholar
  59. Yusuf I, Ahmad S, Phang L, Syed M (2016) Keratinase production and biodegradation of polluted secondary chicken feather wastes by a newly isolated multi heavy metal tolerant bacterium-Alcaligenes sp. J Environ Manag 183:182–195CrossRefGoogle Scholar
  60. Yusuf I, Aqlima S, Phang LY, Yasid NA, Shukor MY (2019) Effective production of keratinase by gellan gum-immobilised Alcaligenes sp . AQ05-001 using heavy metal-free and polluted feather wastes as substrates. 3 Biotech 9:04–12.  https://doi.org/10.1007/s13205-018-1555-x CrossRefGoogle Scholar
  61. Zhang RX, Gong JS, Su C, Zhang DD, Tian H, Dou WF, Li H, Shi JS, Xu ZH (2016) Biochemical characterization of a novel surfactant-stable serine keratinase with no collagenase activity from Brevibacillus parabrevis CGMCC 10798. Int J Biol Macromol 93:843–851.  https://doi.org/10.1016/j.ijbiomac.2016.09.063 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ibrahim Yusuf
    • 1
    Email author
  • Lawal Garba
    • 2
  • Mustapha Ahmad Shehu
    • 1
  • Aminat Musa Oyiza
    • 1
  • Muhammad Rabiu Kabir
    • 1
  • Musa Haruna
    • 3
  1. 1.Department of Microbiology, Faculty of Life Sciences, College of Natural and Pharmaceutical SciencesBayero University, KanoKanoNigeria
  2. 2.Department of MicrobiologyGombe State UniversityGombeNigeria
  3. 3.Department of BiologyKano University of Science and TechnologyWudilNigeria

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