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

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.

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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

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ahmad S, Shamaan N, Arif N (2012) Enhanced phenol degradation by immobilized Acinetobacter sp. strain AQ5NOL 1. World J Microbiol Biotechnol 28:347–352

    CAS  Article  Google Scholar 

  3. Barrowclough G, Sibley F (1980) Feather pigmentation and abrasion: test of a hypothesis. Auk 881–883

  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

    Article  PubMed  PubMed Central  Google 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

    Article  Google 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 323e376

  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

    Article  PubMed  Google Scholar 

  8. Butler M (2004) Are melanized feather barbs stronger? J Exp Biol 207:285–293. https://doi.org/10.1242/jeb.00746

    Article  PubMed  Google 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

    Article  Google 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

    CAS  Article  PubMed  Google Scholar 

  11. Cappuccino J.G. Sherman N (1996) Microbiology-A laboratory manual (Vol. 9). Benjamin Cummings Science Publishing, Carlifonia. p 471

  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

    Article  Google 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

    CAS  Article  Google 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

    CAS  Article  Google 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

    CAS  Article  Google Scholar 

  17. Ferrareze P, Correa A, Brandelli A (2016) Purification and characterization of a keratinolytic protease produced by probiotic Bacillus subtilis. Biocatal Agric Biotechnol 7:102–109

    Article  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google Scholar 

  20. Goldstein G, Flory K, Browne B, Majid S (2004) Bacterial degradation of black and white feathers. Auk 121:656–659

    Article  Google Scholar 

  21. Grande JM, Negro JJ, Torres MJ (2004) The evolution of bird plumage colouration: a role for feather-degradation bacteria? Ardeola 51:375–383

    Google Scholar 

  22. Gunderson A, Frame A (2008) Resistance of melanized feathers to bacterial degradation: is it really so black and white? J Avian Biol 39:539–545

    Article  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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 95:1969–1977

    CAS  Article  Google Scholar 

  27. Joshi S, Tejashwini M, Revati N (2007) Isolation, identification and characterization of a feather degrading bacterium. Int J Poult Sci 6:689–693

    Article  Google 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

    Article  Google Scholar 

  29. Korkmaz H, Hür H, Di S (2004) Characterization of alkaline keratinase of Bacillus licheniformis strain HK-1 from poultry waste. Ann Microbiol 54:201–211

    CAS  Google 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

    CAS  Article  Google 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 10:502–507

    CAS  Google 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 34:403–409

    Article  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google Scholar 

  35. Lowry OC, Rosebrough N (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265

    CAS  Google 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

    CAS  Article  Google 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 7:1018–1024

    Google Scholar 

  38. McGraw K (2006) Mechanics of uncommon colors: pterins, porphyrins, and psittacofulvins. Bird Color 1:354–398

    Google 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

    Article  Google 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

    CAS  Article  Google Scholar 

  41. Ningthoujam SD, Tamreihao K, Mukherjee S, et al (2018) Keratinaceous wastes and their valorization through keratinolytic microorganisms in keratin. IntechOpen

  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

    CAS  Article  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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 39:93–98

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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 2:38–41

    Google 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 183:182–195

    CAS  Article  Google 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

    Article  Google 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

    CAS  Article  PubMed  Google Scholar 

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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.

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

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Correspondence to Ibrahim Yusuf.

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Yusuf, I., Garba, L., Shehu, M.A. et al. 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. Int Microbiol 23, 189–200 (2020). https://doi.org/10.1007/s10123-019-00090-4

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Keywords

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