Abstract
This study proposed a novel and cost-effective approach to enhance and optimize the exo-polygalacturonase from P. indica, a root endophytic fungus. In the current investigation, the impact of ammonium sulfate, sugar beet pulp (SBP), and glucose as variables on induction of exo-polygalacturonase from P. indica was optimized using the central composite design (CCD) of response surface methodology (RSM) under submerged fermentation (SmF). Additionally, determination of the exo-polygalacturonase molecular weight and in situ analysis was performed. The optimal reaction conditions, which resulted in the highest enzyme activity, were observed in the following conditions: ammonium sulfate (4 g/L), SBP (20 g/L), and glucose (60 g/L). Under the optimized condition, the maximum enzyme activity reached 19.4 U/ml (127 U/mg), which increased by 5.84 times compared to non-optimized conditions. The exo-polygalacturonase molecular weight was estimated at 60 KDa. In line with the bioinformatic analysis, the exo-polygalacturonase sequence of P. indica showed similarity with Rhizoctonia solani’s and Thanateporus cucumeris. These results indicated that SBP acts as a cheap and suitable inducer of exo-polygalacturonase production by P. indica in submerged cultivation. The outcome of this study will be useful for industries to decrease environmental pollution with cost-effective approaches.
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References
Aguilar G, Huitrón C (1990) Constitutive exo-pectinase produced by Aspergillus sp. CH-Y-1043 on different carbon source. Biotechnol Lett 12:655–660. https://doi.org/10.1007/BF01088189
Ahmed I, Zia MA, Hussain MA, Akram Z, Naveed MT, Nowrouzi A (2016) Bioprocessing of citrus waste peel for induced pectinase production by Aspergillus niger; its purification and characterization. J Rad Res Appl Sci 9:148–154. https://doi.org/10.1016/j.jrras.2015.11.003
Amin F, Arooj T, Nazli Z-i-H, Bhatti HN, Bilal M (2021) Exo-polygalacturonase production from agro-waste by Penicillium fellutanum and insight into thermodynamic, kinetic, and fruit juice clarification. Biomass Convers Biorefin 1–11. https://doi.org/10.1007/s13399-021-01902-2
Bai Z, Zhang H, Qi H, Peng X, Li B (2004) Pectinase production by Aspergillus niger using wastewater in solid state fermentation for eliciting plant disease resistance. Bioresour Technol 95:49–52. https://doi.org/10.1016/j.biortech.2003.06.006
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 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Chen Y, Sun D, Zhou Y, Liu L, Han W, Zheng B, Wang Z, Zhang Z (2014) Cloning, expression and characterization of a novel thermophilic polygalacturonase from Caldicellulosiruptor bescii DSM 6725. Int J Mol Sci 15:5717–5729. https://doi.org/10.3390/ijms15045717
Fawole O, Odunfa S (2003) Some factors affecting production of pectic enzymes by Aspergillus niger. Int Biodeterior Biodegrad 52:223–227. https://doi.org/10.1016/S0964-8305(03)00094-5
Fontana RC, Salvador S, Silveira MMd (2005) Influence of pectin and glucose on growth and polygalacturonase production by Aspergillus niger in solid-state cultivation. J Ind Microbiol Biotechnol 32:371–377. https://doi.org/10.1007/s10295-005-0004-0
Gupta N, Mahur BK, Izrayeel AMD, Ahuja A, Rastogi VK (2022) Biomass conversion of agricultural waste residues for different applications: a comprehensive review. Environ Sci and Pollut Res 29:73622–73647. https://doi.org/10.1007/s11356-022-22802-6
Heerd D, Diercks-Horn S, Fernández-Lahore M (2014) Efficient polygalacturonase production from agricultural and agro-industrial residues by solid-state culture of Aspergillus sojae under optimized conditions. Springerplus 3:1–14. https://doi.org/10.1186/2193-1801-3-742
Heidarizadeh M, Rezaei PF, Shahabivand S (2018) Novel pectinase from Piriformospora indica, optimization of growth parameters and enzyme production in submerged culture condition. Turkish J Biochem 43:289–295. https://doi.org/10.1515/tjb-2017-0192
Hutnan M, Drtil M, Mrafkova L (2000) Anaerobic biodegradation of sugar beet pulp. Biodegradation 11:203–211. https://doi.org/10.1023/A:1011139621329
Jacob N (2009) Biotechnology for Agro-Industrial Residues Utilisation: Utilisation of Agro-Residues. In: Singh nee P, Pandey A (ed) Pectinolytic enzymes. Springer, Dordrecht, pp 383–396. https://doi.org/10.1007/978-1-4020-9942-7_21
John J, Kaimal KS, Smith ML, Rahman PK, Chellam PV (2020) Advances in upstream and downstream strategies of pectinase bioprocessing: a review. Int J Biol Macromol 162:1086–1099. https://doi.org/10.1016/j.ijbiomac.2020.06.224
Kumar S, Sharma H, Sarkar B (2011) Effect of substrate and fermentation conditions on pectinase and cellulase production by Aspergillus niger NCIM 548 in submerged (SmF) and solid state fermentation (SSF). Food Sci Biotechnol 20:1289–1298. https://doi.org/10.1007/s10068-011-0178-3
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547. https://doi.org/10.1093/molbev/msy096
Kumar V, Sahai V, Bisaria V (2012) Production of amylase and chlamydospores by Piriformospora indica, a root endophytic fungus. Biocatal Agricu Biotechnol 1:124–128. https://doi.org/10.1016/j.bcab.2012.02.002
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Merril CR, Goldman D, Sedman SA, Ebert MH (1981) Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science 211:1437–1438. https://doi.org/10.1126/science.6162199
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Nair S, Panda T (1997) Statistical optimization of medium components for improved synthesis of pectinase by Aspergillus niger. Bioproc Biosyst Eng 16:169–173. https://doi.org/10.1007/s004490050305
Olsson L, Christensen TM, Hansen KP, Palmqvist EA (2003) Influence of the carbon source on production of cellulases, hemicellulases and pectinases by Trichoderma reesei Rut C-30. Enzyme Microb Technol 33:612–619. https://doi.org/10.1016/S0141-0229(03)00181-9
Oyede M A (1998) Studies on cell wall degrading enzymes associated with degradation of cassava (Manihot esculenta) tubers by some phytopathogenic fungi. Dissertation. Obafemi Awolowo University
Patidar MK, Nighojkar S, Kumar A, Nighojkar A (2018) Pectinolytic enzymes-solid state fermentation, assay methods and applications in fruit juice industries: a review. 3 Biotech 8:1–24. https://doi.org/10.1007/s13205-018-1220-4
Patil SR, Dayanand A (2006) Production of pectinase from deseeded sunflower head by Aspergillus niger in submerged and solid-state conditions. Bioresour Technol 97:2054–2058. https://doi.org/10.1016/j.biortech.2005.09.015
Ramos AM, Gally M, García MC, Levin L (2010) Pectinolytic enzyme production by Colletotrichum truncatum, causal agent of soybean anthracnose. Rev Iberoma Micol 27:186–190. https://doi.org/10.1016/j.riam.2010.06.002
Satapathy S, Rout JR, Kerry RG, Thatoi H, Sahoo SL (2020) Biochemical prospects of various microbial pectinase and pectin: an approachable concept in pharmaceutical bioprocessing. Fron Nutr 7:117. https://doi.org/10.3389/fnut.2020.00117
Tepe O, Dursun AY (2014) Exo-pectinase production by Bacillus pumilus using different agricultural wastes and optimizing of medium components using response surface methodology. Environ Sci Pollut Res Int 21:9911–9920. https://doi.org/10.1007/s11356-014-2833-8
Thakur A, Pahwa R, Singh S, Gupta R (2010) Production, purification, and characterization of polygalacturonase from Mucor circinelloides ITCC 6025. Enzyme Res 2010:1–7. https://doi.org/10.4061/2010/170549
Verma S, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903. https://doi.org/10.1080/00275514.1998.12026983
Viayaraghavan P, Jeba Kumar S, Valan Arasu M, Al-Dhabi NA (2019) Simultaneous production of commercial enzymes using agro industrial residues by statistical approach. J Sci Food Agric 99:2685–2696. https://doi.org/10.1002/jsfa.9436
Acknowledgements
We wish to acknowledge the Management of Research and Technology and the Central laboratory of University of Maragheh for their help in running the experiments.
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Partial financial support was received from University of Maragheh. The funding code is 3567.
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Conceptualization, formal analysis, writing—review and editing, project administration, and supervision were carried out by Parisa Fathi Rezaei. Material preparation, data collection and analysis, and writing original draft preparation were performed by Somayyeh Kiani. Bioinformatic analysis was done by Sina Jamalzadegan. All authors read and approved the final manuscript.
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Kiani, S., Fathi Rezaei, P. & Jamalzadegan, S. Exo-polygalacturonase production enhancement by Piriformospora indica from sugar beet pulp under submerged fermentation using the response surface methodology. Environ Sci Pollut Res 30, 45815–45826 (2023). https://doi.org/10.1007/s11356-023-25488-6
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DOI: https://doi.org/10.1007/s11356-023-25488-6