Ameliorating effects of chicken feathers in plant growth promotion activity by a keratinolytic strain of Bacillus subtilis PF1

Abstract

Background

Feathers are the major byproducts of poultry industry and considered as waste. Feathers (composed of protein keratin) are metabolized by a number of microorganisms as a source of carbon and nitrogen. Degradation of feathers results in production of amino acids and peptides, which can be employed as precursors for plant growth-promoting metabolites such as indole acetic acid, ammonia and HCN. The aim of the present investigation was to assess the influence of these metabolites (termed as feather protein hydrolysate) on plant growth promotion activity of keratinolytic bacterial strain Bacillus subtilis PF1.

Results

Strain PF1 exhibits potent keratinolytic activity and can efficiently degrade 10 g/l chicken feathers under submerged cultivation with 81.4 ± 4.40 U/ml keratinase activity. Different concentrations of feathers supported the production of indole acetic acid by strain PF1. Strain PF1 produces maximum indole acetic acid (46.2 ± 0.21 µg/ml) in the presence of 2.0 % feathers at 120 h of incubation. The indole acetic acid production was confirmed by thin-layer chromatography and Fourier transform infrared spectroscopic analysis. However, increased concentration of feathers exhibited negative effect on phosphate solubilization due to increased alkalinity. HCN production also exhibited positive correlation with concentration of feathers. Finally, plant growth of Vigna radiata in the presence of strain PF1 with chicken feathers in soil was investigated, which showed good plant growth promotion activity. Increased ratio of C/N in soil also supported the plant growth promotion activity of feathers.

Conclusion

Feather degradation property of B. subtilis PF1 could be efficiently utilized for feather waste management. The metabolites released by feather degradation along with strain PF1 could be successfully employed as an economic source of nitrogen fertilizers for plants.

Keywords

Bacillus subtilis PF1 / Chicken feather / Indole acetic acid production / Phosphate solubilization / HCN production

References

[1] Ahemad M, Kibret M. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci, 2014, 26: 1-20.

[2] Anbu P, Gopinath SCB, Hilda A, Lakshmipriya T, Annadurai G. Optimization of extracellular keratinase production by poultry farm isolates Scopulariopsis brevicaulis. Bioresour Technol, 2007, 98: 1298-1303.

[3] Anwar MS, Siddique MT, Verma A, Rao YR, Nailwal T, Ansari MW, Pande V. Multitrait plant growth promoting (PGP) rhizobacterial isolates from Brassica juncea rhizosphere. Commun Integr Biol, 2014, 7: 1-9.

[4] Castric PA. Hydrogen cyanide; a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol, 1974, 21: 613-618.

[5] Cheng X, Huang L, Tu X, Li K. Medium optimization for the feather degradation by Streptomyces fradiae Var S-221 using the response surface methodology. Biodegradation, 2010, 21: 117-122.

[6] Choi JM, Nelson PV. Developing a slow release nitrogen fertilizer from organic sources using poultry feathers. J Am Soc Hortic Sci, 1996, 121: 634-638.

[7] Correa APF, Daroit DJ, Brandelli A. Characterization of keratinase produced by Bacillus Sp. P7 isolated from an Amazonian environment. Int Biodeter Biodegr, 2010, 64: 1-6.

[8] Das R, Tiwary BN. Production of indole acetic acid by novel bacterial strain of Planomicrobium chinense isolated from diesel oil contaminated site and its impact on the growth of Vigna radiate. Eur J Soil Biol, 2014, 62: 92-100.

[9] Dastager SG, Deepa CK, Pandey A. Isolation and characterization of novel plant growth promoting Micrococcus sp NII-0909 and its interaction with cowpea. Plant Physiol Biochem, 2010, 48: 987-992.

[10] De Logu A, Uda P, Pellerano ML, Pouseda ML. Comparison of two rapid calorimetric methods for determining resistance of Mycobacterium tuberculosis to rifampin, isoniazid, streptomycin in liquid medium. Eur J Clin Microbiol, 2001, 20: 33-39.

[11] Eaton AD, Lenore SC, Greenberg AE. Standard methods for the examination of water and wastewater, 1995, 19, Washington DC: American Public Health Association.

[12] Francisco SS, Houdusse F, Zamarreno AM, Garnica M, Casanova E, Garcia-Mina JM. Effects of IAA and IAA precursors on the development, mineral nutrition, IAA content and free polyamine content of pepper plants cultivated in hydroponic conditions. Sci Hortic (Amsterdam), 2005, 106: 38-52.

[13] Goswami D, Dhandhukia P, Patel P, Thakkar JN. Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogia by Bacillus licheniformis A2. Microbiol Res, 2014, 169: 66-75.

[14] Hadas A, Kautsky L. Feather meal a semi slow release nitrogen fertilizers for organic farming. Fert Res, 1994, 38: 165-170.

[15] Jeong JH, Lee OM, Jeon YD, Kim JD, Lee NR, Lee CY, Son HJ. Production of keratinolytic enzyme by a newly isolated feather-degrading Stenotrophomonas maltophilia that produces plant growth-promoting activity. Process Biochem, 2010, 45: 1738-1745.

[16] Jeong JH, Jeon YD, Lee OM, Kim JD, Lee NR, Park GT, Son HJ. Characterization of a multifunctional feather-degrading Bacillus subtilis isolated from forest soil. Biodegradation, 2010, 21: 1029-1040.

[17] Jeong JH, Park KH, Oh DJ, Hwang DY, Kim HS, Lee CY, Son HJ. Keratinolytic enzyme-mediated biodegradation of recalcitrant feather by a newly isolated Xanthomonas sp. P5. Polym Degrad Stab, 2010, 95: 1969-1977.

[18] Kaur G, Reddy MS. Solubilizing bacteria on crop yield and soil fertility at multilocational site. Eur J Soil Biol, 2014, 61: 35-40.

[19] Kim JM, Lim WJ, Suh HJ. Feather degrading Bacillus species from poultry waste. Process Biochem, 2001, 37: 287-291.

[20] Kochar M, Upadhyay A, Srivastava S. Indole-3-acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res Microbiol, 2011, 162: 426-435.

[21] Kumar P, Dubey RC, Maheshwari DK. Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res, 2012, 167(2012): 493-499.

[22] Lasekan A, Abu Bakar F, Hashim D. Potential of chicken by-products as sources of useful biological resources. Waste Manage, 2013, 33: 552-556.

[23] Lateef A, Oloke JK, Gueguim EB, Sobowale BO, Ajao SO, Bello BY. Keratinolytic activities of a new feather- degrading isolate of Bacillus cereus LAU 08 isolated from Nigerian soil. Int Biodeter Biodegr, 2010, 64: 162-165.

[24] Mehta S, Nautiyal CS. An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol, 2001, 43: 51-56.

[25] Nilegaonkar SS, Zambare VP, Kanekar PP, Dhakephalkar PK, Sarnaik SS. Production and Partial characterization of dehairing protease from Bacillus cereus MCM B-326. Bioresour Technol, 2007, 98: 1238-1245.

[26] Nustorova M, Braikova D, Gousterova A, Vasileva-Tonkova E, Nedkov P. Chemical, microbiological and plant analysis of soil fertilized with alkaline hydrolysate of sheep’s wool waste, world. J Microbiol Biotechnol, 2006, 22: 383-390.

[27] Olsen SR, Sommers LE. Pageetal AL. Phosphorus. Methods of soil analysis, part 2 Agron Mongr 9, 1982, 2, Madison: ASA and SSSA, 416-418.

[28] Park GT, Son HJ. Keratinolytic activity of Bacillus megaterium F7–1 a feather- degrading mesophilic bacterium. Microbiol Res, 2009, 164: 478-485.

[29] Paul T, Haldar SK, Das A, Bera S, Maity C, Mandal A, Das PS, Das Mohapatra PKD, Pati BR, Mondal KC. Exploitation of chicken feather waste as a plant growth promoting agent using keratinase producing novel isolate Paenibacillus woosongensis TKB2. Biocatal Agric Biotechnol, 2013, 2: 50-57.

[30] Perez-Montano F, Alias-Vilegas C, Bellogin RA, Del Cerro P, Espunny MR, Jimenez- Guerrero I, Lopez Baena FJ, Ollero J, Cubo T. Plant growth promotion in cereal and plant: from microorganism capabilities to crop production. Microbiol Res, 2014, 169(5–6): 325-336.

[31] Sachdev DP, Chaudhari HG, Kasture VM, Dhavale DD, Chopade BA. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian J Exp Biol, 2009, 47: 993-1000.

[32] Sadasivam S, Mannikkam A. Biochemical methods for agricultural sciences, 1992, New Delhi: Wiley Estern Ltd. 246

[33] Senthilkumar M, Swarnlakshmi K, Govindasamy V, Lee YK, Annapurna K. Biocontrol potential of soybean bacterial endophytes against charcoal rot fungus Rhizoctonia bataticola. Curr Microbiol, 2009, 58: 288-293.

[34] Silva LR, Pereira MJ, Rui JA, Gonçalves F, Valentão P, Guedes de Pinho P, Andrade PB. Glycine max (L.) Merr. Vigna radiata L. and Medicago sativa L. sprouts: a natural source of bioactive compounds. Food Res Int, 2013, 50: 127-175.

[35] Sunar K, Dey P, Chakraborty U, Chakraborty B. Biocontrol efficacy and plant growth promoting activity of Bacillus altitudinis isolated from Darjeeling hills. India J Basic Microbiol, 2013, 55: 91-104.

[36] Tatineni R, Doddapaneni KK, Potumarthi RC, Vellanki RN, Kandathil MT, Kolli N, Mangamoori LN. Purification and characterization of an alkaline keratinase from Streptomyces sp. Bioresour Technol, 2008, 99: 1596-1602.

[37] Tiwary E, Gupta R. 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, 2010, 101: 6103-6110.

[38] Trivedi P, Pandy A, Palni LM. In vitro evaluation of antagonistic properties of Pseudomonas corrugate. Microbiol Res, 2008, 163: 329-336.

[39] Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y, Tudzynski B, Sharon A. Identification and functional characterization of indole-3-acetamide mediated IAA biosynthesis in plant associated Fusarium species. Fungal Genet Biolol, 2012, 49: 48-57.

[40] Verma JP, Yadav J, Tiwary KN, Jaiswal DK. Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum) in India. Soil Biol Biochem, 2013, 70: 33-37.

[41] Vessey JK. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 2003, 255: 571-586.