Abstract
Feathers, a waste product of poultry industries have highly recalcitrant structure and are a rich source of organic nitrogen. The use of keratinolytic microbes for bioconversion of feather waste to a value added hydrolysate is gaining the interest of researchers. Bacillus aerius NSMk2 has been reported as a potential keratinolytic strain that converts chicken feather waste into a hydrolysate rich in proteins, small peptides and amino acids. In the present study, biostimulating potential of chicken feather waste-derived protein hydrolysate (PH) generated by biocatalytic action of Bacillus aerius NSMk2 has been evaluated for the growth of mung beans (Vigna radiata), under potted conditions. Soil treated with PH, unhydrolyzed feathers (UF) or diammonium phosphate (DAP) was transferred to different pots, and seeds of mung beans were transplanted. PH treated groups showed superior germination frequency and early growth of pods. The highest number of pods with highest weight of seeds was observed in test groups as compared to control. Higher weight of roots was observed in plants treated with PH, and content of deoxyribonucleic acid (DNA), ribonucleic acid (RNA) and total protein was found to be high. The content of phosphate, potassium and carbon:nitrogen ratio (C:N) was substantially high in soil after application of hydrolysate. Appreciable count of free living nitrogen fixers and phosphate solubilizers was also observed in PH treated groups. The present study shows improved plant performance, yield and soil fertility after application of Bacillus aerius NSMk2 derived protein hydrolysate, and therefore indicates its application as a potential biostimulant in agroindustry.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- PH:
-
Protein hydrolysate
- UF:
-
Unhydrolyzed feathers
- DAP:
-
Diammonium phosphate
- DNA:
-
Deoxyribonucleic acid
- RNA:
-
Ribonucleic acid
- IAA:
-
Indole-3-acetic acid
- EBIC:
-
European Biostimulants Industry Council
- MSM:
-
Minimal salt medium
- CTAB:
-
Hexadecyltrimethyl-ammonium bromide
- EDTA:
-
Ethylenediamine tetraacetic acid
- PSB:
-
Phosphate solubilizing bacteria
References
Abdel-Mawgoud A, Hausmann R, Lepine F, Muller MM (2011) Rhamnolipids: diversity of microbial structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336. https://doi.org/10.1007/s00253-010-2498-2
Abou Chehade L, Al Chami Z, De Pascali SA, Cavoski I, Fanizzi FP (2018) Biostimulants from food processing by-products: agronomic, quality and metabolic impacts on organic tomato (Solanum lycopersicum L.). J Sci Food Agric 98:1426–1436. https://doi.org/10.1002/jsfa.8610
Adetunji CO, Makanjuola OR, Arowora KA, Afolayan SS, Adetunji JB (2012) Production and application of keratin-based organic fertilizer from microbially hydrolyzed feathers to cowpea (Vigna unguiculata). Int J Sci Eng Res 3:164–172
Asad SA, Bano A, Faroo M, Aslam M, Afzal A (2004) Comparative study of the effects of biofertilizers on nodulation and yield characteristics of mung bean (Phaseolus vulgaris L.). Int J Agric Biol 6:837–843
Bahadur L, Tiwari DD (2014) Nutrient management in mung bean (Vigna radiata L.) through sulfur and biofertilizers. Legum Res 37:180–187
Bhange K, Chaturvedi V, Bhatt R (2016) Ameliorating effects of chicken feathers in plant growth promotion activity by a keratinolytic strain of Bacillus subtilis PF1. Bioresour Bioprocess 3:13–23. https://doi.org/10.1186/s40643-016-0091-y
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 Report 3:224–230. https://doi.org/10.1016/j.biteb.2018.07.015
Bhari R, Kaur M, Singh RS (2019) Thermostable and halotolerant keratinase from Bacillus aerius NSMk2 with remarkable dehairing and laundary applications. J Basic Microbiol 59:555–568. https://doi.org/10.1002/jobm.201900001
Bhari R, Kaur M, Singh RS (2020) Nutritional enhancement of chicken feather waste by Bacillus aerius NSMk2. Indian J Microbiol 60:518–525. https://doi.org/10.1007/s12088-020-00897-0
Biernath C, Fischer H, Kuzyakov Y (2008) Root uptake of N-containing and N-free low molecular weight organic substances by maize: a 14C/15N tracer study. Soil Biol Biochem 40:2237–2245. https://doi.org/10.1016/j.soilbio.2008.04.019
Bose A, Pathan S, Pathak K, Keharia H (2013) Keratinolytic protease production by Bacillus amyloliquefaciens 6B using feather meal as substrate and application of feather hydrolysate as substrate and application of feather hydrolysate as organic nitrogen input for agricultural soil. Waste Biomass Valori 5:595–605. https://doi.org/10.1007/s12649-013-9272-5
Bremner JM (1996) Total nitrogen. In: Sparks DL (ed) Methods of soil analysis: chemical methods. Soil Science Society of America, Madison, pp 1085–1086
Bryndina L, Ilyina N, Baklanova O, Moiseyeva E (2019) Comparative evaluation of biostimulator efficiency on corn seeds germination: keratin protein and preparation Ribav extra. Earth Environ Sci 392:012068. https://doi.org/10.1088/1755-1315/392/1/012068
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8
Campos P, Borie F, Cornejo P, Lopez-Raez JA, Lopez-Garcia A, Sequel A (2018) Phosphorus acquisition efficiency related to root trails: is mycorrhizal symbiosis a key factor to wheat and barley crop**? Front Plant Sci 9:752. https://doi.org/10.3389/fpls.2018.00752
Canellas LP, Olivares FL, Okorokova-Facanha AL, Facanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957. https://doi.org/10.1104/pp.007088
Choi JM, Nelson PV (1996) Develo** a slow-release nitrogen fertilizer from organic sources: using poultry feathers. J Am Soc Hortic Sci 121:634–638
Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, Rouphael Y (2015) Protein hydrolysates as biostimulants in horticulture. Sci Hortic 196:28–38. https://doi.org/10.1016/j.scienta.2015.08.037
Colla G, Hoagland L, Ruzzi M, Cardarelli M, Bonini P, Canaguier R, Rouphael Y (2017) Biostimulant action of protein hydrolysates: unraveling their effects on plant physiology and microbiome. Front Plant Sci 8:1–14. https://doi.org/10.3389/fpls.2017.02202
Dubey RC, Maheshwari DK (2002) Practical microbiology 2nd (eds.). Chand S & Co. Pvt. Ltd., New Delhi, p 413
El Habbasha SF, Hozayn M, Khalafallah MA (2007) Integration effect between phosphorus levels and biofertilizers on quality and quantity yield of faba bean (Vicia faba L.) in newly cultivated sandy soils. Res J Agric Biol Sci 3:966–971
El-Ghamery AA, El-Nahas AI, Mansour MM (2000) The action of atrazine herbicide as an inhibitor of cell division on chromosomes and nucleic acids content in root meristems of Allium cepa and Vicia faba. Cytologia 65:277–287. https://doi.org/10.1508/cytologia.65.277
Ertani A, Cavani L, Pizzeghello D, Brandellero E, Altissimo A, Ciavatta C, Nardi S (2009) Biostimulant activity of two protein hydrolysates in the growth and nitrogen metabolism of maize seedlings. J Plant Nutr Soil Sci 172:237–244
Ertani A, Pizzeghello D, Baglieri A, Cadili V, Tambone F, Gennari M, Nardi S (2012) Agro-industrial residues and their biological activity on maize (Zea mays L.) metabolism. J Geochem Explor 129:103–111
Faust F, Schubert S (2016) Protein synthesis is the most sensitive process when potassium is substituted by sodium in the nutrition of sugar beet (Beta vulgaris). Plant Physiol Biochem 107:237–247. https://doi.org/10.1016/j.plaphy.2016.06.009
Gammon NJR (1951) Determination of total potassium and sodium in sandy soils by the flame photometer. Soil Sci 71:211–214
Gao C, El-Sawah AM, Ali DFI, Hamoud YA, Shaghaleh H, Sheteiwy MS (2020) The integration of bio and organic fertilizers improve plant growth, grain yield, quality and metabolism of hybrid maize (Zea mays L.). Agronomy 10:1–25. https://doi.org/10.3390/agronomy10030319
Gupta R, Rajput R, Sharma R, Gupta N (2013) Biotechnological applications and prospective market of microbial keratinases. Appl Microbiol Biotechnol 97:9931–9940. https://doi.org/10.1007/s00253-013-5292-0
Hardy RW, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207. https://doi.org/10.1104/pp.43.8.1185
Hasanuzzaman M, Nahar K, Rahman A, Al Muhamed J, Alharby HF, Fujita M (2018) Exogenous glutathionine attenuates lead-induced oxidative stress in wheat by improving antioxidant defence and physiological mechanisms. J Plant Interact 13:203–212. https://doi.org/10.1080/17429145.2018.1458913
Htwe AZ, Moh SM, Soe KM, Moe K (2019) Effects of biofertilizer produced from Bradyrhizobium and Streptomyces griseoflavus on plant growth, nodulation, nitrogen fixation, nutrient uptake, and seed yield of mung bean, cowpea, and soybean. Agronomy 9:77. https://doi.org/10.3390/agronomy9020077
Ibrahim ME, Bekheta MA, El-Mousari A, Gafar NA (2010) Improvement of growth and seed yield quality of Vicia faba L plants as affected by application of some bioregulators. Aust J Basic Appl Sci 1:657–666
Jeong JH, Lee OM, Jeon YD, Kim JD, Lee NR, Lee CY, Son HJ (2010) Production of keratinolytic enzyme by a newly isolated feather-degrading Stenotrophomonas maltophilia that produces plant growth-promoting activity. Process Biochem 45:1738–1745. https://doi.org/10.1016/j.procbio.2010.07.020
Joardar JC, Rahman MM (2018) Poultry feather waste management and effects on plant growth. Int J Recyc Org Waste Agri 7:183–188. https://doi.org/10.1007/s40093-018-0204-z
Khan S, Qureshi MI, Alam T, Abdin MZ (2007) Protocol for isolation of genomic DNA from dry and fresh roots of medicinal plants suitable for RAPD and restriction digestion. Afr J Biotechnol 6:175–178
Kolomaznik K, Pecha J, Matusu V, Janacova D (2012) Diffusion of biostimulators into plant tissues. Heat Mass Transf 48:1505–1512. https://doi.org/10.1007/s00231-012-0998-6
Kumar A, Shahbaz M, Koirala M, Blagodatskaya E, Seidel SJ, Kuzyakov Y, Pausch J (2019) Root trait plasticity and plant nutrient acquistion in phosphorus limited soil. J Plant Nutr Soil Sci 182:945–952
Lasekan A, Bakar A, 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
Lowry OH, Roserbrough NH, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Biochem 193:265–275
Lukatkin AS, Mokshin EV, da Silva JAT (2017) Use of alternative plant growth regulators and carbon sources to manipulate Dianthus caryophyllus L. shoot induction in vitro. Rend Lincei Sci Fis Nat 28:583–588. https://doi.org/10.1007/s12210-017-0623-1
Manna MC, Swarup A, Wanjari RH, Mishra B, Shahi DK (2007) Long-term fertilization: manure and liming effects on soil organic matter and crop yields. Soil Tillage Res 2:397–409. https://doi.org/10.1016/j.still.2006.08.013
Mishra A, Prasad K, Geeta R (2010) Effect of bio-fertilizer inoculations on growth and yield of dwarf pea (Pisum sativum L.) in conjunction with different doses of chemical fertilizers. J Agron 9:163–168. https://doi.org/10.3923/ja.2010.163.168
Nustorova M, Braikova D, Gousterova A, Vasileva-Tonkova E, Nedkov P (2006) Chemical, microbiological and plant analysis of soil fertilized with alkaline hydrolysate of sheep’s wool waste. World J Microbiol Biotechnol 22:383–390. https://doi.org/10.1007/s11274-005-9045-9
Olsen SR, Sommers LE (1982) Phosphorus. In: Miller AL, Keeney LH (eds) Methods of soil analysis: chemical and microbiological properties. American Society of Agronomy, Madison, pp 403–430
Pati BR, Sengupta S, Chandra AK (1995) Impact of selected phyllospheric diazotrophs on the growth of wheat seedlings and assay of the growth substances produced by the diazotrops. Microbiol Res 150:121–127. https://doi.org/10.1016/S0944-5013(11)80046-7
Paul T, Halder SK, Das A, Bera S, Maity C, Mandal A, Mondal KC (2013) Exploitation of chicken feather waste as a plant growth promoting agent using keratinase producing novel isolate Paenibacillus woosongensis TKB2. Biocatal Agric Biotechnol 2:50–57. https://doi.org/10.1016/j.bcab.2012.10.001
Ragel P, Raddatz N, Leidi EO, Quintero FJ, Pardo JM (2019) Regulation of K+ nutrition in plants. Front Plant Sci 10:1–21. https://doi.org/10.3389/fpls.2019.00281
Sadej W, Przekwas K (2008) Fluctuations of nitrogen levels in soil profile under conditions of long-term fertilization experiment. Plant Soil Environ 54:197–203
Sholikhah F (2016) Provision of biofertilizer dilution formulation (1:15) with dosage and frequency variations of growth and productivity of green nut (Vigna radiate L.). thesis, Airlangga University
Tamreihao K, Devi LJ, Khunjamayum R, Mukherjee S, Ashem RS, Ningthoujam DS (2017) Biofertilizing potential of feather hydrolyzate produced by indigenous keratinolytic Amycolatopsis sp. MBRL 40 for rice cultivation under field conditions. Biocatal Agric Biotechnol 10:317–320. https://doi.org/10.1016/j.bcab.2017.04.010
Tamreihao K, Mukherjee S, Khunjamayum R, Jaya Devi L, Asem RS, Ningthoujam DS (2018) Feather degradation by keratinolytic bacteria and biofertilizing potential for sustainable agricultural production. J Basic Microbiol 5:1–10. https://doi.org/10.1016/j.bcab.2017.04.010
Trevisan S, Pizzeghello D, Ruperti B, Francioso O, Sassi A, Palme K, Quaggiotti S, Nardi S (2009) Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element in Arabidopsis. Plant Biol 12:604–614. https://doi.org/10.1111/j.1438-8677.2009.00248.x
Verma A, Singh H, Anwar MS, Kumar S, Ansari MW, Agrawal S (2016) Production of thermostable organic solvent tolerant keratinolytic protease from Thermoactinomycetes sp. RM4: IAA production and plant growth promotion. Front Microbiol 7:1–13. https://doi.org/10.3389/Ffmicb.2016.01189
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. https://doi.org/10.1023/A:1026037216893
Wang X, Shen J, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179:302–306. https://doi.org/10.1016/j.plantsci.2010.06.007
Yin X, Schapendonk HCM, Struik PC (2018) Exploring the optimum nitrogen partitioning to predict the acclimation of C3 leaf photosynthesis to varying growth conditions. J Exp Bot 70:2435–2244. https://doi.org/10.1093/jxb/ery277
Acknowledgments
The financial assistance received from Science and Engineering Research Board (SERB), Government of India, New Delhi in the form a major research project (ECR/2015/000156) is duly acknowledged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kaur, M., Bhari, R. & Singh, R.S. Chicken feather waste-derived protein hydrolysate as a potential biostimulant for cultivation of mung beans. Biologia 76, 1807–1815 (2021). https://doi.org/10.1007/s11756-021-00724-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00724-x