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Enzymatic saccharification of banana peel and sequential fermentation of the reducing sugars to produce lactic acid

  • María Aurora Martínez-TrujilloEmail author
  • Karina Bautista-Rangel
  • Mayola García-Rivero
  • Abigail Martínez-Estrada
  • Martín R. Cruz-DíazEmail author
Research Paper
  • 24 Downloads

Abstract

An integral bioprocess to produce lactic acid (LA) from banana peel (BP) was studied. Oxidases produced by Trametes versicolor and hydrolases produced by Aspergillus flavipes and Aspergillus niger saccharified BP at optimal conditions: 230 rpm, 66 g/L BP, and 73.5% (v/v) of enzymatic crude extract (using equal quantities of the enzymatic extracts). At bioreactor scale (1 L), the joint action of oxidases and hydrolases released 18 g/L of reducing sugars (RS) after 24 h (60% corresponded to glucose), consuming the BP polysaccharides. Lactobacillus delbrueckii fermented the released RS, producing 10 g/L of LA; while in the sequential fermentation (inoculating L. delbrueckii after saccharification), 28 g/L of LA were produced, observing an apparent decrease in feedback inhibition of hydrolases below 1.5 g/L of RS. This process is susceptible for upscaling to produce high LA concentrations and represents a platform to utilize agroindustrial wastes to obtain value-added products.

Keywords

Agricultural wastes Oxidases Hydrolases Optimization Lactic acid fermentation 

Notes

Acknowledgements

KBR thanks CONACYT for the scholarship. Authors want to thank Tecnológico Nacional de México, for the support to develop this work (projects 657.18-PD and 665.18-PD). M. Cruz-Díaz thanks CONACYT for the support given to the project 256787 (Design of a biorefinery for the production of polylactic acid through a sustainable energy route). Also to project PIAPI1814 FESC, UNAM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. 1.
    Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production. In: Biofuels. Springer, Berlin Heidelberg, pp. 41–65. doi: 10.1007/978-3-540-73651-6 (108: 41-65).Google Scholar
  2. 2.
    Guerrero AB, Ballesteros I, Ballesteros M (2018) The potential of agricultural banana waste for bioethanol production. Fuel 213:176–185.  https://doi.org/10.1016/j.fuel.2017.10.105 CrossRefGoogle Scholar
  3. 3.
  4. 4.
    Saraiva AB, Pacheco EBAV, Visconte LLY, Pereira E (2012) Potentials for utilization of post-fiber extraction waste from tropical fruit production in Brazil—the example of banana pseudo-stem. Int J Environ Bioenergy 4(2):101–119Google Scholar
  5. 5.
    Kumar P, Barrett DM, Delwiche MJ, Stroeve P (2009) Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind Eng Chem Res 48(8):3713–3729.  https://doi.org/10.1021/ie801542g CrossRefGoogle Scholar
  6. 6.
    Harinder SO, Praveen VV, Lavudi S, Sunil B, Joshua DH (2011) Ethanol production from banana peels using statistically optimized simultaneous saccharification and fermentation process. Waste Manage 31:1576–1584.  https://doi.org/10.1016/j.wasman.2011.02.007 CrossRefGoogle Scholar
  7. 7.
    Rehman S, Aslam H, Ahmad A, Khan SA, Sohail M (2014) Production of plant cell wall degrading enzymes by monoculture and co-culture of Aspergillus niger and Aspergillus terreus under SSF of banana peels. Braz J Microbiol 45(4):1485–1492.  https://doi.org/10.1590/S1517-83822014000400045 CrossRefPubMedGoogle Scholar
  8. 8.
    Mufidah E, Asep A, Prihanto WM (2017) Optimization of l-lactic acid production from banana peel by multiple parallel fermentation with Bacillus licheniformis and Aspergillus awamori. Food Sci Technol Res 23(1):137–143.  https://doi.org/10.3136/fstr.23.137 CrossRefGoogle Scholar
  9. 9.
    Davidi L, Moraïs S, Artzi L, Knop D, Hadar Y, Arfi Y, Bayer EA (2016) Toward combined delignification and saccharification of wheat straw by a laccase-containing designer cellulosome. P Natl Acad Sci 113(39):10854–10859.  https://doi.org/10.1073/pnas.1608012113 CrossRefGoogle Scholar
  10. 10.
    Talebnia F, Karakashev D, Angelidaki I (2010) Production of bioethanol from wheat straw: an overview on pretreatment, hydrolysis, and fermentation. Bioresour Technol 101(13):4744–4753.  https://doi.org/10.1016/j.biortech.2009.11.080 CrossRefPubMedGoogle Scholar
  11. 11.
    Wolf MVE, García GE, García RM, Aguilar-Osorio G, Martínez-Trujillo MA (2015) Batch and pulsed fed-batch cultures of Aspergillus flavipes FP-500 growing on lemon peel at stirred tank reactor. Appl Biochem Biotechnol 177:1201–1215.  https://doi.org/10.1007/s12010-015-1807-8 CrossRefGoogle Scholar
  12. 12.
    Ponce-Noyola T, De la Torre M (1995) Isolation of a high-specific-growth-rate mutant of Cellulomonas flavigena on sugar cane bagasse. Appl Microbiol Biotechnol 42(5):709–712.  https://doi.org/10.1007/BF00171949 CrossRefGoogle Scholar
  13. 13.
    Chen C (2003) Evaluation of air oven moisture content determination methods for rough rice. Biosyst Eng 86(4):447–457CrossRefGoogle Scholar
  14. 14.
    Uppdegraff C (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424.  https://doi.org/10.1016/S0003-2697(69)80009-6 CrossRefGoogle Scholar
  15. 15.
    Hatfield R (1994) A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures. J Sci Food Agr 65:51–58.  https://doi.org/10.1002/jsfa.2740650109 CrossRefGoogle Scholar
  16. 16.
    Southgate DAT (1991) Determination of food carbohydrates, 2nd edn. Elsevier Applied Science, New YorkGoogle Scholar
  17. 17.
    Nielsen S (1998) Food analysis, 2nd edn. An Aspen Publication, GaithersburgGoogle Scholar
  18. 18.
    Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428.  https://doi.org/10.1021/ac60147a030 CrossRefGoogle Scholar
  19. 19.
    Kjeldahl J (1883) Determination of protein nitrogen in food products. Encycl Food Sci 1883:439–441Google Scholar
  20. 20.
    Onyeike EN, Acheru GN (2002) Chemical composition of selected Nigerian oil seeds and physicochemical properties of the oil extracts. Food Chem 77:431–437CrossRefGoogle Scholar
  21. 21.
    Durán-Hinojosa U, Soto-Vázquez L, García Rivero M, Zafra Jiménez G, Vigueras Carmona S E, Martínez-Trujillo M A (2017) Solid-state culture for lignocellulases production in fermentation process. Angela Faustino Jozala ed. Intechopen. 255–269.Google Scholar
  22. 22.
    Trejo-Aguilar BA, Visser J, Aguilar-Osorio G (1996) Pectinase secretion by Aspergillus FP-180 and Aspergillus niger N-402 growing under stress induced by the pH of culture medium. Pr Biotechnol 14:915–920.  https://doi.org/10.1016/S0921-0423(96)80334-0 CrossRefGoogle Scholar
  23. 23.
    Montgomery (2001) Design and analysis of experiments. 5th Edn. Wiley, HobokenGoogle Scholar
  24. 24.
    Rogosa M, Mitchell JA, Wiseman RF (1951) A selective medium for the isolation and enumeration of oral and fecal lactobacilli. J Bacteriol 62:132–133.  https://doi.org/10.1177/00220345510300051201 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Wee Y J, Ryu H W (2009) Lactic acid production by Lactobacillus sp. RKY2 in a cell-recycle continuous fermentation using lignocellulosic hydrolyzates as inexpensive raw materials. Bioresour Technol 100(18), 4262–4270. DOI: 10.1016/j.biortech.2009.03.074.CrossRefPubMedGoogle Scholar
  26. 26.
    Tibolla H, Pelissari FM, Rodrigues IM, Menegalli CF (2017) Cellulose nanofibers produced from banana peel by enzymatic treatment: Study of process conditions. Ind crops prod 95:664–674.  https://doi.org/10.1016/j.indcrop.2016.11.035 CrossRefGoogle Scholar
  27. 27.
    Mosier NS, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch MR (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673–686.  https://doi.org/10.1016/j.biortech.2004.06.025 CrossRefPubMedGoogle Scholar
  28. 28.
    Inoue H, Yano S, Endo T, Sakaki T, Sawayama S (2008) Combining hot-compressed water and ball milling pretreatments to improve the efficiency of the enzymatic hydrolysis of eucalyptus. Biotechnol Biofuels 1(2):1–9.  https://doi.org/10.1186/1754-6834-1-2 CrossRefGoogle Scholar
  29. 29.
    Culleton H, McKie V, de Vries RP (2013) Physiological and molecular aspects of degradation of plant polysaccharides by fungi: what have we learned from Aspergillus? Biotechnol J 8(8):884–894.  https://doi.org/10.1002/biot.201200382 CrossRefPubMedGoogle Scholar
  30. 30.
    Martínez-Trujillo A, Arreguín-Rangel L, García-Rivero M, Aguilar-Osorio G (2011) Use of fruit residues for pectinase production by Aspergillus flavipes FP-500 and Aspergillus terreus FP-370. Lett Appl Microbiol 53(2):202–209.  https://doi.org/10.1111/j.1472-765X.2011.03096.x CrossRefPubMedGoogle Scholar
  31. 31.
    Torres-Barajas LR, Aguilar-Osorio G (2013) Xylanolytic system proteins desorption from Aspergillus flavipes FP-500 cultures with agrowastes. Revista Mexicana de Ingeniería Química 12(3):513–525Google Scholar
  32. 32.
    Fernandez-Aulis F, Hernandez-Vazquez L, Aguilar-Osorio G, Arrieta-Baez D, Navarro-Ocaña A (2019) Extraction and identification of anthocyanins in corn cob and corn husk from Cacahuacintle Maize. J Food Sci 84(5):954–962.  https://doi.org/10.1111/1750-3841.14589 CrossRefPubMedGoogle Scholar
  33. 33.
    Membrillo Venegas I, Fuentes-Hernández J, García-Rivero M, Martínez-Trujillo A (2013) Characteristics of Aspergillus niger xylanases produced on rice husk and wheat bran in submerged culture and solid-state fermentation for an applicability proposal. Int J of Food Sci Technol 48(9):1798–1807.  https://doi.org/10.1111/ijfs.12153 CrossRefGoogle Scholar
  34. 34.
    Chaturvedi V, Verma P (2013) An overview of key pretreatment processes employed for bioconversion of lignocellulosic biomass into biofuels and value-added products. 3 Biotech 3(5):415–431.  https://doi.org/10.1007/s13205-013-0167-8 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Gupta VK, Kubicek CP, Berrin JG, Wilson DW, Couturier M, Berlin A, Ezeji T (2016) Fungal enzymes for bio-products from sustainable and waste biomass. Trends Biochem Sci 41(7):633–645.  https://doi.org/10.1016/j.tibs.2016.04.006 CrossRefPubMedGoogle Scholar
  36. 36.
    Ping X, Mei L (2012) Xylose production, consumption and health benefits. Biochemistry Research Trends. Published by Nova science publishers, Inc., New York, pp 1–14Google Scholar
  37. 37.
    Gutiérrez-Rojas I, Moreno-Sarmiento N, Montoya D (2014) Mechanisms and regulation of enzymatic hydrolysis of cellulose in filamentous fungi: classical cases and new models. Revista Iberoamericana de Mycologia 32(1):1–12.  https://doi.org/10.1016/j.riam.2013.10.009 CrossRefGoogle Scholar
  38. 38.
    Roda A, De Faveri DM, Dordoni R, Lambri M (2014) Vinegar production from pineapple wastes—preliminary saccharification trials. Chem Eng Trans 37:607–612.  https://doi.org/10.3303/CET1437102 CrossRefGoogle Scholar
  39. 39.
    Ciolacu D. E (2018) Biochemical modification of lignocellulosic biomass. In: Popa VI, Volf I (eds) Biomass as renewable raw material to obtain bioproducts of high-tech value. Elsevier: Amsterdam, pp b315–350. https://doi.org/10.1016/B978-0-444-63774-1.00009-0 CrossRefGoogle Scholar
  40. 40.
    Hatakka A (2005) Biodegradation of lignin. In: Alexander S (eds) Biopolymers online. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany. https://doi.org/10.1002/3527600035.bpol1005
  41. 41.
    Moreno AD, Tomás-Pejó E, Ibarra D, Ballesteros M, Olsson L (2013) In situ laccase treatment enhances the fermentability of steam-exploded wheat straw in SSCF processes at high dry matter consistencies. Bioresource Technol 143:337–343.  https://doi.org/10.1016/j.biortech.2013.06.011 CrossRefGoogle Scholar
  42. 42.
    dos Santos AC, Ximenes E, Kim Y, Ladisch MR (2018) Lignin–enzyme interactions in the hydrolysis of lignocellulosic biomass. Trends Biotechnol 37(5):518–531.  https://doi.org/10.1016/j.tibtech.2018.10.010 CrossRefPubMedGoogle Scholar
  43. 43.
    Daou M, Faulds CB (2017) Glyoxal oxidases: their nature and properties. World J Microbiol Biotechnol 33(5):87.  https://doi.org/10.1007/s11274-017-2254-1 CrossRefPubMedGoogle Scholar
  44. 44.
    Peciulyte A, Samuelsson L, Olsson L, McFarland KC, Frickmann J, Østergård L, Halvorsen R, Scott BR, Johansen KS (2018) Redox processes acidify and decarboxylate steam-pretreated lignocellulosic biomass and are modulated by LPMO and catalase. Biotechnol Biofuels 11(1):165.  https://doi.org/10.1186/s13068-018-1159-z CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    López CA, Rojo PG, Echevarria CA, Gallon AM (2007) Desarrollo de materiales compuestos a partir de fibras de plátano modificadas con enzimas ligninolíticas. Scientia et Technica. 10(22517/23447214):5105Google Scholar
  46. 46.
    Mena-Espino X, Barahona-Pérez F, Alzate-Gaviria L, Rodríguez-Vázquez R, Tzec-Simá M, Domínguez-Maldonado J, Canto-Canché BB (2011) Saccharification with Phanerochaete chrysosporium and Pleurotus ostreatus enzymatic extracts of pretreated banana waste. Afr J Biotechnol 10(19):3824–3834Google Scholar
  47. 47.
    Harinder SO, Simranjeet KS, Praveen VV (2012) Statistical optimization of hydrolysis process for banana peels using cellulolytic and pectinolytic enzymes. Food Bioprod Process 90(2):257–265.  https://doi.org/10.1016/j.fbp.2011.05.002 CrossRefGoogle Scholar
  48. 48.
    Nuttiya C, Jirasak K (2013) Pretreatment methods for banana peel as a substrate for the bioproduction of ethanol in SHF and SSF. Int J Comput Internet Manag 21(2):15–19Google Scholar
  49. 49.
    Martín C (2002) Comparison of the fermentability of enzymatic hydrolysates of sugarcane bagasse pretreated by steam explosion using different impregnating agents. Appl Biochem Biotechnol 98(100):699–716.  https://doi.org/10.1007/978-1-4612-0119-9_57 CrossRefPubMedGoogle Scholar
  50. 50.
    Sheehan JS, Himmel ME (2001) Outlook for bioethanol production from lignocellulosic feedstocks: technology hurtles. Agro Food Ind Hi-Tech 12:54–57Google Scholar
  51. 51.
    Öhgren K, Bura R, Lesnicki G, Saddler J, Zacchi G (2007) A comparison between simultaneous saccharification and fermentation and separate hydrolysis and fermentation using steam-pretreated corn stover. Process Biochem 42:834–839.  https://doi.org/10.1016/j.procbio.2007.02.003 CrossRefGoogle Scholar
  52. 52.
    Chen M, Zhao J, Xia L (2008) Enzymatic hydrolysis of maize straw polysaccharides for the production of reducing sugars. Carbohydr Polym 71:411–415.  https://doi.org/10.1016/j.carbpol.2007.06.011 CrossRefGoogle Scholar
  53. 53.
    Wang Y, Tashiro Y, Sonomoto K (2015) Fermentative production of lactic acid from renewable materials: recent achievements, prospects, and limits. J Biosc Bioeng 119(1):10–18.  https://doi.org/10.1016/j.jbiosc.2014.06.003 CrossRefGoogle Scholar
  54. 54.
    Caspeta L, Caro-Bermúdez MA, Ponce-Noyola T, Martínez A (2014) Enzymatic hydrolysis at high-solids loadings for the conversion of agave bagasse to fuel ethanol. Appl Energy 113:277–286.  https://doi.org/10.1016/j.apenergy.2013.07.036 CrossRefGoogle Scholar
  55. 55.
    Zhang X, Xu C, Wang H (2007) Pretreatment of bamboo residues with Coriolus versicolor for enzymatic hydrolysis. J Biosci Bioeng 104(2):149–151.  https://doi.org/10.1263/jbb.104.149 CrossRefPubMedGoogle Scholar
  56. 56.
    Abdel-Rahman MA, Tashiro Y, Sonomoto K (2011) Lactic acid production from lignocellulose-derived sugars using lactic acid bacteria: overview and limits. J Biotechnol 156(4):286–301.  https://doi.org/10.1016/j.jbiotec.2011.06.017 CrossRefPubMedGoogle Scholar
  57. 57.
    Tanaka T, Hoshina M, Tanabe S, Sakai K, Ohtsubo S, Taniguchi M (2006) Production of D-lactic acid from defatted rice bran by simultaneous saccharification and fermentation. Bioresour Technol 97:211–217.  https://doi.org/10.1016/j.biortech.2005.02.025 CrossRefPubMedGoogle Scholar
  58. 58.
    John RP, Nampoothiri KM, Pandey A (2006) Solid state fermentation for L-lactic acid production from agro-wastes using Lactobacillus delbrueckii. Proc Biochem 41:759–763.  https://doi.org/10.1016/j.procbio.2005.09.013 CrossRefGoogle Scholar
  59. 59.
    Sasaki C, Okumura R, Asakawa A, Asada C, Nakamura Y (2012) Production of d-lactic acid from sugarcane bagasse using steam explosion. J Phys Conf Ser 352(1):12054.  https://doi.org/10.1088/1742-6596/352/1/012054 CrossRefGoogle Scholar
  60. 60.
    Chookieatwatana K (2014) Lactic acid production from simultaneous saccharification and fermentation of Cassava Starch by Lactobacillus plantarum MSUL 903. APCBEE Procedia 8:156–160.  https://doi.org/10.1016/j.apcbee.2014.03.019 CrossRefGoogle Scholar
  61. 61.
    Mufidah E, Wakayama M (2016) Optimization of D-lactic acid production using unutilized biomass as substrates by multiple parallel fermentation. 3 Biotech 6(2):186.  https://doi.org/10.1007/s13205-016-0499-2 CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.División de Ingeniería Química Y Bioquímica, Tecnológico de Estudios Superiores de EcatepecTecnológico Nacional de MéxicoEcatepec de MorelosMexico
  2. 2.Departamento de Ingeniería Y Tecnología, Facultad de Estudios Superiores CuautitlánUNAMCuautitlán IzcalliMexico

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