Skip to main content
Log in

Utilization of orange peel, a food industrial waste, in the production of exo-polygalacturonase by pellet forming Aspergillus sojae

  • Original Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

The production of exo-polygalacturonase (exo-PG) from orange peel (OP), a food industrial waste, using Aspergillus sojae was studied in submerged culture. A simple, low-cost, industrially significant medium formulation, composed of only OP and (NH4)2SO4 (AS) was developed. At an inoculum size of 2.8 × 103 spores/mL, growth was in the form of pellets, which provided better mixing of the culture broth and higher exo-PG activity. These pellets were successfully used as an inoculum for bioreactors and 173.0 U/mL exo-PG was produced. Fed-batch cultivation further enhanced the exo-PG activity to 244.0 U/mL in 127.5 h. The final morphology in the form of pellets is significant to industrial fermentation easing the subsequent downstream processing. Furthermore, the low pH trend obtained during this fermentation serves an advantage to fungal fermentations prone to contamination problems. As a result, an economical exo-PG production process was defined utilizing a food industrial by-product and producing high amount of enzyme.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Marin FR, Soler-Rivas C, Benavente-Garcia O, Castillo J, Perez-Alvarez JA (2007) By-products from different citrus processes as a source of customized functional fibres. Food Chem 100:736–741

    Article  CAS  Google Scholar 

  2. Lopez JAS, Li Q, Thompson IP (2010) Biorefinery of waste orange peel. Crit Rev Biotechnol 30:63–69

    Article  Google Scholar 

  3. Mamma D, Kourtoglou E, Christakopoulos P (2008) Fungal multienzyme production on industrial by-products of the citrus-processing industry. Bioresour Technol 99:2373–2383

    Article  CAS  Google Scholar 

  4. Giese EC, Dekker RFH, Barbosa AM (2008) Orange bagasse as substrate for the production of pectinase and laccase by Botryosphaeria rhodina MAMB-05 in submerged and solid state fermentation. Bioresources 3:335–345

    CAS  Google Scholar 

  5. El-Sheekh MM, Ismail AMS, El-Abd MA, Hegazy EM, El-Diwany AI (2009) Effective technological pectinases by Aspergillus carneus NRC1 utilizing the Egyptian orange juice industry scraps. Int Biodeterior Biodegrad 63:12–18

    Article  CAS  Google Scholar 

  6. Tao NG, Shi WQ, Liu YJ, Huang SR (2011) Production of feed enzymes from citrus processing waste by solid-state fermentation with Eupenicillium javanicum. Int J Food Sci Technol 46:1073–1079

    Article  CAS  Google Scholar 

  7. Heerd D, Yegin S, Tari C, Fernandez-Lahore M (2012) Pectinase enzyme-complex production by Aspergillus spp. in solid-state fermentation: a comparative study. Food Bioprod Process 90:102–110

    Article  CAS  Google Scholar 

  8. Buyukkileci AO, Tari C, Fernandez-Lahore M (2011) Enhanced production of exo-polygalacturonase from agro-based products by Aspergillus sojae. Bioresources 6:3452–3468

    CAS  Google Scholar 

  9. Oberoi HS, Vadlani PV, Nanjundaswamy A, Bansal S, Singh S, Kaur S, Babbar N (2011) Enhanced ethanol production from Kinnow mandarin (Citrus reticulata) waste via a statistically optimized simultaneous saccharification and fermentation process. Bioresour Technol 102:1593–1601

    Article  CAS  Google Scholar 

  10. Pourbafrani M, Forgacs G, Horvath IS, Niklasson C, Taherzadeh MJ (2010) Production of biofuels, limonene and pectin from citrus wastes. Bioresour Technol 101:4246–4250

    Article  CAS  Google Scholar 

  11. Wilkins MR, Widmer WW, Grohmann K (2007) Simultaneous saccharification and fermentation of citrus peel waste by Saccharomyces cerevisiae to produce ethanol. Process Biochem 42:1614–1619

    Article  CAS  Google Scholar 

  12. Wilkins MR, Widmer WW, Grohmann K, Cameron RG (2007) Hydrolysis of grapefruit peel waste with cellulase and pectinase enzymes. Bioresour Technol 98:1596–1601

    Article  CAS  Google Scholar 

  13. Fontana RC, Polidoro TA, da Silveira MM (2009) Comparison of stirred tank and airlift bioreactors in the production of polygalacturonases by Aspergillus oryzae. Bioresour Technol 100:4493–4498

    Article  CAS  Google Scholar 

  14. Kashyap DR, Vohra PK, Chopra S, Tewari R (2001) Applications of pectinases in the commercial sector: a review. Bioresour Technol 77:215–227

    Article  CAS  Google Scholar 

  15. Ribeiro DS, Henrique SMB, Oliveira LS, Macedo GA, Fleuri LF (2010) Enzymes in juice processing: a review. Int J Food Sci Tech 45:635–641

    Article  CAS  Google Scholar 

  16. Jayani RS, Saxena S, Gupta R (2005) Microbial pectinolytic enzymes: a review. Process Biochem 40:2931–2944

    Article  CAS  Google Scholar 

  17. Favela-Torres E, Volke-Sepulveda T, Viniegra-Gonzalez G (2006) Production of hydrolytic depolymerising pectinases. Food Technol Biotechnol 44:221–227

    CAS  Google Scholar 

  18. Zeni J, Cence K, Grando CE, Tiggermann L, Colet R, Lerin LA, Cansian RL, Toniazzo G, de Oliveira D, Valduga E (2011) Screening of pectinase-producing microorganisms with polygalacturonase activity. Appl Biochem Biotechnol 163:383–392

    Article  CAS  Google Scholar 

  19. Gogus N, Tari C, Oncu S, Unluturk S, Tokatli F (2006) Relationship between morphology, rheology and polygalacturonase production by Aspergillus sojae ATCC 20235 in submerged cultures. Biochem Eng J 32:171–178

    Article  Google Scholar 

  20. Tari C, Gögus N, Tokatli F (2007) Optimization of biomass, pellet size and polygalacturonase production by Aspergillus sojae ATCC 20235 using response surface methodology. Enzyme Microb Technol 40:1108–1116

    Article  CAS  Google Scholar 

  21. Ustok FI, Tari C, Gogus N (2007) Solid-state production of polygalacturonase by Aspergillus sojae ATCC 20235. J Biotechnol 127:322–334

    Article  CAS  Google Scholar 

  22. Pazouki M, Panda T (2000) Understanding the morphology of fungi. Bioprocess Eng 22:127–143

    Article  CAS  Google Scholar 

  23. Paul GC, Priede MA, Thomas CR (1999) Relationship between morphology and citric acid production in submerged Aspergillus niger fermentations. Biochem Eng J 3:121–129

    Article  CAS  Google Scholar 

  24. Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259

    Article  CAS  Google Scholar 

  25. Amanullah A, Christensen LH, Hansen K, Nienow AW, Thomas CR (2002) Dependence of morphology on agitation intensity in fed-batch cultures of Aspergillus oryzae and its implications for recombinant protein production. Biotechnol Bioeng 77:815–826

    Article  CAS  Google Scholar 

  26. Grimm LH, Kelly S, Krull R, Hempel DC (2005) Morphology and productivity of filamentous fungi. Appl Microbiol Biotechnol 69:375–384

    Article  CAS  Google Scholar 

  27. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  28. Panda T, Naidu GSN, Sinha J (1999) Multiresponse analysis of microbiological parameters affecting the production of pectolytic enzymes by Aspergillus niger: a statistical view. Process Biochem 35:187–195

    Article  CAS  Google Scholar 

  29. Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  30. Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23

    CAS  Google Scholar 

  31. Gogus N, Taze BH, Demir H, Tari C, Unluturk S, Lahore MF (2014) Evaluation of orange peel, an industrial waste, for the production of Aspergillus sojae polygalacturonase considering both morphology and rheology effects. Turk J Biol 38:537–548

    Article  Google Scholar 

  32. Oncul S, Tari C, Unluturk S (2007) Effect of various process parameters on morphology, rheology, and polygalacturonase production by Aspergillus sojae in a batch bioreactor. Biotechnol Prog 23:836–845

    Article  Google Scholar 

  33. Nighojkar S, Phanse Y, Sinha D, Nighojkar A, Kumar A (2006) Production of polygalacturonase by immobilized cells of Aspergillus niger using orange peel as inducer. Process Biochem 41:1136–1140

    Article  CAS  Google Scholar 

  34. Teixeira MFS, Lima JL, Duran N (2000) Carbon sources effect on pectinase production from Aspergillus japonicus 586. Braz J Microbiol 31:286–290

    Article  CAS  Google Scholar 

  35. Galiotou-Panayotou M, Rodis P, Kapantai M (1993) Enhanced polygalacturonase production by Aspergillus niger NRRL-364 grown on supplemented citrus pectin. Lett Appl Microbiol 17:145–148

    Article  CAS  Google Scholar 

  36. Grohmann K, Cameron RG, Buslig BS (1995) Fractionation and pretreatment of orange peel by dilute acid hydrolysis. Bioresour Technol 54:129–141

    Article  CAS  Google Scholar 

  37. Talebnia F, Pourbafrani M, Lundin M, Taherzadeh MJ (2008) Optimization study of citrus waste saccharification by dilute-acid hydrolysis. Bioresources 3:108–122

    CAS  Google Scholar 

  38. Widmer W, Zhou WY, Grohmann K (2010) Pretreatment effects on orange processing waste for making ethanol by simultaneous saccharification and fermentation. Bioresour Technol 101:5242–5249

    Article  CAS  Google Scholar 

  39. Buyukkileci AO, Hamamci H, Yucel M (2006) Lactate and ethanol productions by Rhizopus oryzae ATCC 9363 and activities of related pyruvate branch point enzymes. J Biosci Bioeng 102:464–466

    Article  CAS  Google Scholar 

  40. Papagianni M, Moo-Young M (2002) Protease secretion in glucoamylase producer Aspergillus niger cultures: fungal morphology and inoculum effects. Process Biochem 37:1271–1278

    Article  CAS  Google Scholar 

  41. Friedrich J, Cimerman A, Steiner W (1990) Production of pectolytic enzymes by Aspergillus niger—effect of inoculum size and potassium hexacyanoferrate II-trihydrate. Appl Microbiol Biotechnol 33:377–381

    CAS  Google Scholar 

  42. Hermersdorfer H, Leuchtenberger A, Wardsack C, Ruttloff H (1987) Influence of culture conditions on mycelial structure and polygalacturonase synthesis of Aspergillus niger. J Basic Microbiol 27:309–315

    Article  CAS  Google Scholar 

  43. Couri S, Pinto GAS, de Senna LF, Martelli HL (2003) Influence of metal ions on pellet morphology and polygalacturonase synthesis by Aspergillus niger 3T5B8. Braz J Microbiol 34:16–21

    Article  CAS  Google Scholar 

  44. Malvessi E, da Silveira MM (2004) Influence of medium composition and pH on the production of polygalacturonases by Aspergillus oryzae. Braz Arch Biol Tecn 47:693–702

    Article  CAS  Google Scholar 

  45. Beg QK, Bhushan B, Kapoor M, Hoondal GS (2000) Effect of amino acids on production of xylanase and pectinase from Streptomyces sp QG-11-3. World J Microbiol Biotechnol 16:211–213

    Article  CAS  Google Scholar 

  46. Hadj-Taieb N, Ayadi M, Trigui S, Bouabdallah F, Gargouri A (2002) Hyperproduction of pectinase activities by a fully constitutive mutant (CT1) of Penicillium occitanis. Enzyme Microb Technol 30:662–666

    Article  CAS  Google Scholar 

  47. Villas-Boas SG, Esposito E, de Mendonca MM (2002) Novel lignocellulolytic ability of Candida utilis during solid-substrate cultivation on apple pomace. World J Microbiol Biotechnol 18:541–545

    Article  CAS  Google Scholar 

  48. Nakkeeran E, Gowthaman MK, Umesh-Kumar S, Subramanian R (2012) Techno-economic analysis of processes for Aspergillus carbonarius polygalacturonase production. J Biosci Bioeng 113:634–640

    Article  CAS  Google Scholar 

  49. Rangarajan V, Rajasekharan M, Ravichandran R, Sriganesh K, Vaitheeswaran V (2010) Pectinase production from orange peel extract and dried orange peel solid as substrates using Aspergillus niger. Int J Biotechnol Biochem 6:445–453

    Google Scholar 

  50. Pedrolli D, Gomes E, Monti R, Carmona E (2008) Studies on productivity and characterization of polygalacturonase from Aspergillus giganteus submerged culture using citrus pectin and orange waste. Appl Biochem Biotechnol 144:191–200

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by TÜBITAK (Turkey) and BMBF (Germany) through the Intensified Cooperation Project of IntenC 107O602 and EUROTRANSBIO, PGSYS/ETB-2008-44.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Canan Tari.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buyukkileci, A.O., Lahore, M.F. & Tari, C. Utilization of orange peel, a food industrial waste, in the production of exo-polygalacturonase by pellet forming Aspergillus sojae . Bioprocess Biosyst Eng 38, 749–760 (2015). https://doi.org/10.1007/s00449-014-1315-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-014-1315-1

Keywords

Navigation