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Evaluation of mango residues to produce hyaluronic acid by Streptococcus zooepidemicus

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Abstract

Mango processing generates significant amounts of residues (35–65%) that may represent environmental problems owed to improper disposal. The use of mango byproducts as substrates to produce hyaluronic acid (HA) is an attractive alternative to reduce the cost of substrate. In this study, we evaluated the potential of hydrolyzates from mango peels and seeds to produce HA by Streptococcus equi. subsp. zooepidemicus. The physicochemical characterization of mango residues showed that the seeds contain a higher amount of holocellulose (cellulose and hemicellulose), which amounts 54.2% (w/w) whereas it only represents 15.5% (w/w) in the peels. Mango peels, however, are composed mainly of hot water-extractives (62% w/w, that include sucrose, fructose, glucose and organic acids). A higher concentration of monosaccharides (39.8 g/L) was obtained from the enzymatic hydrolysis (with Macerex) of peels as compared to seeds (24.8 g/L with Celuzyme). From mango peels, hydrolyzates were obtained 0.6 g/L HA, while 0.9 g/L HA were obtained with hydrolyzates from mango seeds. These results demonstrate that mango byproducts have the potential to be used for production of HA.

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Availability of data and materials

The datasets generated during and/or analyzed during the current study are not publicly available but are available from the corresponding author upon request.

References

  • Ammar TY, Pereira TAP, Mistura SLL, Kuhn A, Saggin JI, Lopes Júnior OV (2015) Viscossuplementacão no tratamento da osteoartrose do joelho: uma revisão da literatura (Viscosupplementation in the treatment of knee osteoarthrosis: a review of the literature). Rev Brasil Ortop 50(5):489–494. https://doi.org/10.1016/j.rbo.2014.09.011

    Article  Google Scholar 

  • Arslan NP, Aydoğan MN (2021) Evaluation of sheep wool protein hydrolysate and molasses as low-cost fermentation substrates for hyaluronic acid production by Streptococcus zooepidemicus ATCC 35246. Waste Biomass Valorization 12:925–935. https://doi.org/10.1007/s12649-020-01062-w

    Article  CAS  Google Scholar 

  • Azaf Ferrari O, Conesa Domínguez C, Seguí Gil L (2016) Pretratamientos para la mejora de la hidrólisis enzimática del residuo de industrialización de la piña para la obtención de bioetanol. Efecto del pretratamiento con microondas en la producción de compuestos fenólicos inhibitorios de la fermentación. Instituto de Ingeniería de Alimentos. (Pretreatments for the improvement of enzymatic hydrolysis of piña industrialization residue for the production of bioethanol. Effect of microwave pretreatment on the production of fermentation-inhibiting phenolic compounds. Institute of Food Engineering). Universidat Politécnica de Valencia. https://riunet.upv.es/handle/10251/71808

  • Boeriu C, Springer J, Kooy F, Broek L, Eggink G (2013) Production Methods for Hyaluronan. Int J Carbohydr Chemi 14. https://doi.org/10.1155/2013/624967

  • Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane bagasse hydrolysate improves ethanol production by Candida shehatae NCIM 3501. Bioresour Technol 98(10):1947–1950. https://doi.org/10.1016/j.biortech.2006.07.047

    Article  CAS  PubMed  Google Scholar 

  • Chen SJ, Chen JL, Huang WC, Chen HL (2009) Fermentation process development for hyaluronic acid production by Streptococcus zooepidemicus ATCC 39920. Korean J Chem Eng 26:428–432

    Article  CAS  Google Scholar 

  • Chong BF, Blank LM, Mclaughlin R, Nielsen LK (2005) Microbial hyaluronic acid production. Appl Microbiol Biotechnol 66(4):341–351. https://doi.org/10.1007/s00253-004-1774-4

    Article  CAS  PubMed  Google Scholar 

  • Cross C, Bevan E (1907) Researches on Cellulose, 2nd ed. Longmans, green, and Co. London, UK, Volume 2

  • de Macedo AC, Santana MH (2012) Hyaluronic acid depolymerization by ascorbate-redox effects on solid state cultivation of Streptococcus zooepidemicus in cashew apple fruit bagasse. World J Microbiol Biotechnol 28(5):2213–2219. https://doi.org/10.1007/s11274-012-1028-z

    Article  CAS  PubMed  Google Scholar 

  • El-Kady T, Abd El-Rahman M, Toliba AO, Abo El-maty S (2017) Evaluation of mango seed kernel extract as natural occurring phenolic rich antioxidant compound. Bull Natl Nutr Inst 48:1–30

    Article  Google Scholar 

  • Fallacara A, Baldini E, Manfredini S, Vertuani S (2018) Hyaluronic acid in the third millennium. Polymers 10(7):701. https://doi.org/10.3390/polym10070701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores-Méndez DA, Ramos-Ibarra JR, Toriz G, Arriola-Guevara E, Guatemala-Morales G, Corona-González RI (2021) Bored coffee beans for production of hyaluronic acid by Streptococcus zooepidemicus. Ferment 7(3):121. https://doi.org/10.3390/fermentation7030121

    Article  CAS  Google Scholar 

  • Flores-Méndez DA, Pelayo-Ortiz C, Martínez-Gómez A, Guatemala-Morales GM, Corona-González RI (2023) Evaluation of Agave tequilana by-products for microbial production of hyaluronic acid. Bioresour Technol Rep 21:101366. https://doi.org/10.1016/j.biteb.2023.101366

    Article  CAS  Google Scholar 

  • García-Magaña ML, García HS, Bello-Pérez LA, Sáyago-Ayerdi SG, De Oca MM (2013) Functional properties and dietary fiber characterization of mango processing by-products (Mangifera indica L., cv Ataulfo and Tommy Atkins). Plant Foods for Human Nutrition (Dordrecht, Netherlands) 68:254–258. https://doi.org/10.1007/s11130-013-0364-y

    Article  CAS  PubMed  Google Scholar 

  • García-Mahecha M, Soto-Valdez H, Carvajal-Millan E, Madera-Santana TJ, Lomelí-Ramírez MG, Colín-Chávez C (2023) Bioactive compounds in extracts from the agro-industrial waste of mango. Molecules 8(1):458. https://doi.org/10.3390/molecules28010458

    Article  CAS  Google Scholar 

  • Gummadi S, Panda T (2003) Purification and biochemical properties of microbial pectinases - a review. Process Biochem 38(7):987–996. https://doi.org/10.1016/S0032-9592(02)00203-0

    Article  CAS  Google Scholar 

  • Guzmán O, Lemus C, Bugarin J, Bonilla J, Ly J (2013) Composición y características químicas de mangos (Mangifera indica l) destinados a la alimentación animal en Nayarit. México. Rev Cubana Ciencia Agrícola 47(3):273–277

    Google Scholar 

  • Liu L, Liu Y, Li J, Du G, Chen J (2011) Microbial production of hyaluronic acid: current state, challenges, and perspectives. Microb Cell Factories 10:99. https://doi.org/10.1186/1475-2859-10-99

    Article  CAS  Google Scholar 

  • Nelson DL, Cox MM (2017) Lehninger principles of biochemistry. 7th ed. W. H. Freeman. New York, USA, pp. 1–1328.

  • Oliveira AH, Ogrodowski CC, De Macedo AC, Santana MH, Gonçalves LR (2013) Cashew apple juice as microbial cultivation medium for non-immunogenic hyaluronic acid production. Brazil J Microbiol 44(4):1097–1104. https://doi.org/10.1590/S1517-83822014005000017

    Article  Google Scholar 

  • Pan N, Vignoli J, Baldo C, Pereira H, Silva RSSF, Celligoi M (2015) Agroindustrial byproducts for the production of hyaluronic acid by Streptococcus zooepidemicus ATCC 39920. Int J Sci Technol Res 4:114–118

    Google Scholar 

  • Quintero CV, Giraldo GG, Lucas AJ, Vasco LJ (2013) Caracterización fisicoquímica del mango común (Mangifera indica l.) durante su proceso de maduración. Biotecnología en el Sector Agropecuario y Agroindustrial (Physicochemical characterization of the common mango (Mangifera indica l.) during its ripening process. Biotechnology in the Agricultural and Agroindustrial Sector 11(1):10–18

  • Rohit SG, Jyoti PK, Subbi RRT, Naresh M, Senthilkumar S (2018) Kinetic modeling of hyaluronic acid production in palmyra palm (Borassus flabellifer) based medium by Streptococcus zooepidemicus MTCC 3523. Biochem Engineer J 137:284–293. https://doi.org/10.1016/j.bej.2018.06.011

    Article  CAS  Google Scholar 

  • Rosalie R, Joas J, Mertz C, Dufossé L, Léchaudel M (2022) Impact of water supply reduction and cold storage on phenolic compounds from mango (Mangifera indica L. cv. Cogshall) pulp peel plants 11(22):3038. https://doi.org/10.3390/plants11223038.

  • Serna Cock L, Torres León C (2015) Potencial agroindustrial de cáscaras de mango (Mangifera indica) variedades Keitt y Tommy Atkins. Acta Agron 64(2):110–115

    Article  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Sogi DS, Siddiq M, Greiby I, Dolan KD (2013) Total phenolics, antioxidant activity, and functional properties of ‘Tommy Atkins’ mango peel and kernel as affected by drying methods. Food Chem 141(3):2649–2655. https://doi.org/10.1016/j.foodchem.2013.05.053

    Article  CAS  PubMed  Google Scholar 

  • Suárez-Hernández LA, Camacho-Ruíz RM, Arriola-Guevara E, Padilla-Camberos E, Kirchmayr MR, Corona-González RI, Guatemala-Morales GM (2021) Validation of an analytical method for the simultaneous determination of hyaluronic acid concentration and molar mass by size-exclusion chromatography. Molecules 26(17):5360. https://doi.org/10.3390/molecules26175360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • TAPPI TAOTPAPI (1997) Preparation of wood for chemical analysis. T 264 cm-97. Fibrous materials and pulp testing. TAPPI Test methods. Atlanta, GA, USA

  • TAPPI TAOTPAPI (2002) Ash in wood, pulp, paper and paperboard: combustion at 525 °C. T 211 om-02. Fibrous materials and pulp testing. TAPPI Test methods. TAPPI Press: Atlanta, GA, USA 

  • TAPPI TAOTPAPI (2006) Acid-insoluble lignin in wood and pulp. T 222 om-02; Fibrous materials and pulp testing, TAPPI Test methods, TAPPI Press: Atlanta, GA, USA

  • TAPPI TAOTPAPI (2007) Solvent extractives of wood and pulp. T 204 cm-97; Fibrous materials and pulp testing, TAPPI Test methods, TAPPI Press: Atlanta, GA, USA

  • TAPPI TAOTPAPIT (1999) Water solubility of wood and pulp. T 207 cm-99; Fibrous materials and pulp testing, TAPPI Test methods TAPPI Press: Atlanta, GA, USA

  • Vázquez JA, Pastrana L, Piñeiro C, Teixeira JA, Pérez-Martín RI, Amado IR (2015) Production of Hyaluronic Acid by Streptococcus zooepidemicus on Protein Substrates Obtained from Scyliorhinus canicula Discards. Mar Drugs 13(10):6537–6549. https://doi.org/10.3390/md13106537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise L, Murphy M, D’Addieco A (1946) Chlorite holocellulose, its fractionation and bearing on summative wood analysis and on the hemicellulose. Pap Trade J 122:35–43

    CAS  Google Scholar 

Download references

Acknowledgements

JCM would like to thank Consejo Nacional de Ciencia y Tecnología (CONACYT) for scholarship CVU: 853236.

Funding

This work was supported by Fondo Institucional de Fomento Regional para el Desarrollo Científico, Tecnológico y de Innovación (FORDECYT) CONACYT, México (Project no. 2017-10-292747), Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C., and Universidad de Guadalajara (UDG).

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RICG: conceptualization, methodology, resources, validation supervision, funding acquisition, writing, and review and editing; JCM: investigation, methodology, and writing original draft; GGM: conceptualization, funding acquisition, resources, and writing original draft; GT: conceptualization, analyzed data, writing, and review and editing; EAG: data analysis, writing, and review and editing; LASH: methodology, visualization, writing, and review and editing. All authors contributed in the conception, study design, results interpretation, reviewing and editing the final version of manuscript. All authors read and approved the final manuscript. The first draft of the manuscript was written by RICG and JCM, and all the coauthors commented previous versions of this manuscript.

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Correspondence to Rosa Isela Corona-González.

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Contreras Mendoza, J., Arriola Guevara, E., Suarez Hernández, L.A. et al. Evaluation of mango residues to produce hyaluronic acid by Streptococcus zooepidemicus. Folia Microbiol 69, 847–856 (2024). https://doi.org/10.1007/s12223-023-01123-2

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