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Evaluation of Sheep Wool Protein Hydrolysate and Molasses as Low-Cost Fermentation Substrates for Hyaluronic Acid Production by Streptococcus zooepidemicus ATCC 35246

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Abstract

Peptones are widely used as complex fermentation substrate for hyaluronic acid (HA) production; however, use of peptones in HA production reduces commercial competitiveness due to their high price. The present study was conducted to test the feasibility of sheep wool peptone (SWP) (mainly organic nitrogen source) and molasses (mainly carbon source) as cheap substrates for HA production from Streptococcus zooepidemicus ATCC 35246. Six peptones (SWP I–VI) were prepared from sheep wool using different chemical hydrolysis methods. Among them, SWP-VI was determined to be more fovarable for HA production. SWP-VI was compared with commercial tryptone peptone (TP) and protease peptone (PP) in order to evaluate its effectiveness in production of HA, lactic acid (LA) and cell biomass (CB). The protein contents of SWP-VI, TP and PP were determined as 70.6, 83.1 and 83.8 g/100 g, respectively. The best peptone for HA and CB production was SWP-VI, whereas PP was found to be more favourable for LA production. Maximum HA concentrations in SWP-VI, TP and PP media were determined as 3.54, 2.58 and 2.47 g/L, respectively.

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References

  1. Vázquez, J.A., Pastrana, L., Piñeiro, C., Teixeira, J.A., Pérez-Martín, R., Amado, I.R.: Production of hyaluronic acid by Streptococcus zooepidemicus on protein substrates obtained from Scyliorhinus canicula discards. Mar. Drugs 13, 6537–6549 (2015)

    Google Scholar 

  2. Kogan, G., Soltes, L., Stern, R., Gemeiner, P.: Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol. Lett. 29, 17–25 (2007)

    Google Scholar 

  3. Manasa, M., Sridevi, V., Chandana Lakshmi, M.V., Dedeepya, J.: A review on hyaluronic acid. Int. J. Res. Chem. Environ. 2, 6–11 (2012)

    Google Scholar 

  4. Chong, B.F., Blank, L.M., Mclaughlin, R., Nielsen, L.K.: Microbial hyaluronic acid production. Appl. Microbiol. Biotechnol. 66, 341–351 (2005)

    Google Scholar 

  5. Averbeck, M., Gebhardt, C.A., Voigt, S., et al.: Differential regulation of hyaluronan metabolism in the epidermal and dermal compartments of human skin by UVB irradiation. J. Invest. Derm. 127, 687–697 (2007)

    Google Scholar 

  6. Balazs, E.A., Sweeney, D.B.: The injection of hyaluronic acid and reconstituted vitreous into the vitreous cavity. In: McPherson, A. (ed.) New and Controversial Aspects of Retinal Detachment, pp. 371–376. Harper and Row, New York (1968)

    Google Scholar 

  7. Liu, L., Liu, Y., Li, J., Du, G., Chen, J.: Microbial production of hyaluronic acid: current state, challenges, and perspectives. Microb. Cell Fact. 10, 99 (2011)

    Google Scholar 

  8. Chien, L.J., Lee, C.K.: Hyaluronic acid production by recombinant Lactococcus lactis. Appl. Microbiol. Biotechnol. 77, 339–342 (2007)

    Google Scholar 

  9. Armstrong, D.C., Cooney, M.J., Johns, M.R.: Growth and amino-acids requirements of hyaluronic-acid-producing Streptococcus zooepidemicus. Appl. Microbiol. Biotechnol. 47, 309–312 (1997)

    Google Scholar 

  10. Kim, S.J., Park, S.Y., Kin, C.W.: A novel approach to the production of hyaluronic acid by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 16, 1849–1855 (2006)

    Google Scholar 

  11. Amado, I.R., Vázquez, J.A., Pastrana, L., Teixeira, J.A.: Microbial production of hyaluronic acid from agro-industrial by-products: molasses and corn steep liquor. Biochem. Eng. J. 117, 181–187 (2017)

    Google Scholar 

  12. Duan, X.J., Yang, L., Zhang, X., Tan, W.S.: Effect of oxygen and shear stress on molecular weight of hyaluronic acid produced by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 18, 718–724 (2008)

    Google Scholar 

  13. Liu, L., Du, G., Chen, J., Zhu, Y., Wang, M., Sun, J.: Microbial production of low molecular weight hyaluronic acid by adding hydrogen peroxide and ascorbate in batch culture of Streptococcus zooepidemicus. Bioresour. Technol. 100, 362–367 (2009)

    Google Scholar 

  14. Patil, K.P., Chaudhari, B.L., Chincholkar, S.B.: Screening for pharmaceutically important exopolysaccharide producing Streptococci and partial optimization for EPS production. Curr. Trends Biotechnol. Pharm. 3, 329–340 (2009)

    Google Scholar 

  15. Amado, I.R., Vázquez, J.A., Pastrana, L., Teixeira, J.A.: Cheese whey: a cost-effective alternative for hyaluronic acid production by Streptococcus zooepidemicus. Food Chem. 198, 54–61 (2016)

    Google Scholar 

  16. Wang, K., Li, R., Ma, J.H., Jian, Y.K., Che, J.N.: Extracting keratin from wool by using L-cysteine. Green Chem. 18, 476–481 (2016)

    Google Scholar 

  17. Mokrejs, P., Krejci, O., Svoboda, P.: Producing keratin hydrolysates from sheep wool. Orient. J. Chem. 27, 1303–1309 (2011)

    Google Scholar 

  18. Zhang, H., Deb-Choudhury, S., Plowman, J., Dyer, J.: The Effect of wool surface and interior modification on subsequent photostability. J. Appl. Polym. Sci. 127(5), 3435–3440 (2013)

    Google Scholar 

  19. Lewis, D.M., Rippon, J.A.: The Coloration of Wool and Other Keratin Fibres. Wiley, New York (2013)

    Google Scholar 

  20. Gousterova, A., Nustorova, M., Goshev, I., Christov, P., Braikova, D., Tishinov, K., Haertle, T., Nedkov, P.: Alkaline hydrolysate of waste sheep wool aimed as fertilizer. Biotechnol. Biotechnol. Equip. 17, 140–145 (2003)

    Google Scholar 

  21. Gousterova, A., Braikova, D., Goshev, I., Christov, P., Tishinov, K., Vasileva-Tonkova, E., Haertle, T., Nedkov, P.: Degradation of keratin and collagen containing wastes by newly isolated thermoactinomycetes or by alkaline hydrolysis. Lett. Appl. Microbiol. 40, 335–340 (2005)

    Google Scholar 

  22. Nustorova, M., Braikova, D., Gousterova, A., Vasileva-Tonkova, E., Nedkov, P.: Chemical, microbiological and plant analysis of soil fertilized with alkaline hydrolysate of sheep’s wool waste. World J. Microbiol. Biotechnol. 22, 383–390 (2006)

    Google Scholar 

  23. Eslahi, N., Dadashian, F., Nejad, N.H.: Optimization of enzymatic hydrolysis of wool fibers for nanoparticles production using response surface methodology. Adv. Powder Technol. 24, 416–426 (2013)

    Google Scholar 

  24. Taskin, M., Unver, Y., Firat, A., Ortucu, S., Yildiz, M.: Sheep wool protein hydrolysate: a new peptone source for microorganisms. J. Chem. Technol. Biotechnol. 91, 1675–1680 (2016)

    Google Scholar 

  25. Kalogiannis, S., Iakovidou, G., Liakopoulou-Kyriakides, M., Kyriakidis, D.A., Skaracis, G.N.: Optimization of xanthan gum production by Xanthomonas campestris grown in molasses. Process Biochem. 39, 249–256 (2003)

    Google Scholar 

  26. Survase, S.A., Saudagar, P.S., Singhal, R.S.: Use of complex media for the production of scleroglucan by Sclerotium rolfsii MTCC 2156. Bioresour. Technol. 98, 1509–1512 (2007)

    Google Scholar 

  27. Akhtar, T., Hashmi, A.S., Tayyab, M., Anjum, A.A., Saeed, S., Ali, S.: Bioconversion of agricultural waste to butyric acid through solid state fermentation by Clostridium tyrobutyricum. Waste Biomass Valoriz. 1–7 (2018)

  28. Kurcz, A., Błażejak, S., Kot, A.M., Bzducha-Wróbel, A., Kieliszek, M.: Application of industrial wastes for the production of microbial single-cell protein by fodder yeast Candida utilis. Waste Biomass Valoriz. 9, 57–64 (2018)

    Google Scholar 

  29. Lazaro, C.Z., Bosio, M., dos Santos Ferreira, J., Varesche, M.B.A., Silva, E.L.: The biological hydrogen production potential of agroindustrial residues. Waste Biomass Valoriz. 6, 273–280 (2015)

    Google Scholar 

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

    Google Scholar 

  31. Pan, C.N., Pereira, B.C.H., da Silva, C.L.M., Vasconcelos, D.F.A., Celligoi, C.P.A.M.: Improvement production of hyaluronic acid by Streptococcus zooepidemicus in sugarcane molasses. Appl. Biochem. Biotechol. 182, 276–293 (2017)

    Google Scholar 

  32. Yadav, S., Chandra, R.: Biodegradation of organic compounds of molasses melanoidin (MM) from biomethanated distillery spent wash (BMDS) during the decolourisation by a potential bacterial consortium. Biodegradation 23, 609–620 (2012)

    Google Scholar 

  33. Taskin, M., Ortucu, S., Unver, Y., Tasar, O.C., Ozdemir, M., Kaymak, H.C.: Invertase production and molasses decolourization by cold-adapted filamentous fungus Cladosporium herbarum ER-25 in non-sterile molasses medium. Process Saf. Environ. Prot. 103, 136–143 (2016)

    Google Scholar 

  34. Orak, T., Caglar, O., Ortucu, S., Ozkan, H., Taskin, M.: Chicken feather peptone: a new alternative nitrogen source for pigment production by Monascus purpureus. J. Biotechnol. 271, 56–62 (2018)

    Google Scholar 

  35. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356 (1956)

    Google Scholar 

  36. Fong, C.B., Nielsen, L.K.: Aerobic cultivation of Streptococcus zooepidemicus and the role of NADH oxidase. Biochem. Eng. J. 16, 153–162 (2003)

    Google Scholar 

  37. Oliveira, A.H., Ogrodowski, C.C., de Macedo, A.C., Santana, M.H.A., Gonçalves, L.R.B.: Cashew apple juice as microbial cultivation medium for non-immunogenic hyaluronic acid production. Braz. J. Microbiol. 44, 1097–1104 (2013)

    Google Scholar 

  38. Kosakai, M., Yosizawa, Z.: A partial modification of the carbazole method of bitter and muir for quantitation of hexuronic acids. Anal. Biochem. 93, 295–298 (1979)

    Google Scholar 

  39. Oueslati, N., Leblanc, P., Harscoat-Schiavo, C., Rondags, E., Meunier, S., Kapel, R., Marc, I.: CTAB turbidimetric method for assaying hyaluronic acid in complex environments and under cross-linked form. Carbohydr. Polym. 112, 102–108 (2014)

    Google Scholar 

  40. Hikima, T., Nonomura, Y.: Powderization of wool keratin by alkali hydrolysis in higher alcohol/water binary systems. Chem. Lett. 37, 338–339 (2008)

    Google Scholar 

  41. Aroskar, V.J., Kamat, S.D., Kamat, D.V.: Effect of various nutritional supplements on hyaluronic acid production. IIOAB 2, 1 (2012)

    Google Scholar 

  42. Takara, K., Ushijima, K., Wada, K., Iwasaki, H., Yamashita, M.: Phenolic compounds from sugarcane molasses possessing antibacterial activity against cariogenic bacteria. J. Oleo Sci. 56, 611–614 (2007)

    Google Scholar 

  43. Liu, L., Du, G., Chen, J., Wang, M., Sun, J.: Enhanced hyaluronic acid production by a two-stage culture strategy based on the modelling of batch and fed-batch cultivation of Streptococcus zooepidemicus. Bioresour. Technol. 99, 8532–8536 (2008)

    Google Scholar 

  44. Jagannath, S., Ramachandran, K.B.: Influence of competing metabolic processes on the molecular weight of hyaluronic acid synthesized by Streptococcus zooepidemicus. Biochem. Eng. J. 48, 148–158 (2010)

    Google Scholar 

  45. Klompong, V., Benjakul, S., Kantachote, D., Shahidi, F.: Characteristics and use of yellow stripe trevally hydrolysate as culture media. J. Food Sci. 74, 219–225 (2009)

    Google Scholar 

  46. Chen, S.J., Chen, J.L., Huang, W.C., Chen, H.L.: Fermentation process development for hyaluronic acid production by Streptococcus zooepidemicus ATCC 39920. Korean J. Chem. Eng. 26, 428–432 (2009)

    Google Scholar 

  47. Im, J.H., Song, J.M., Kang, J.H., Kang, D.J.: Optimization of medium components for high-molecular-weight hyaluronic acid production by Streptococcus sp. ID9102 via a statistical approach. J. Ind. Microbiol Biotechnol. 36, 1337 (2009)

    Google Scholar 

  48. Linder, L., Holme, T., Frostell, G.: Hyaluronidase and aminopeptidase activity in cultures of Streptococcus mitis ATCC 903. Acta. Pathol. Microbiol. Scand. B 82, 521–526 (1974)

    Google Scholar 

  49. Hynes, W.L., Walton, S.L.: Hyaluronidases of gram-positive bacteria. FEMS Microbial. Lett. 183, 201–207 (2000)

    Google Scholar 

  50. Pourzardosht, N., Rasaee, M.J.: Improved yield of high molecular weight hyaluronic acid production in a stable strain of Streptococcus zooepidemicus via the elimination of the hyaluronidase-encoding gene. Mol. Biotechnol. 59, 192–199 (2017)

    Google Scholar 

  51. Hu, G., Sandham, H.J.: Streptococcal utilization of lactic acid and its effect on pH. Arch. Oral Biol. 17, 729–743 (1972)

    Google Scholar 

  52. Gudina, E., Rodrigues, A., Alves, E., Domingues, M., Teixeira, J., Rodrigues, L.: Bioconversion of agro-industrial by-products in rhamnolipids toward applications in enhanced oil recovery and bioremediation. Bioresour. Technol. 177, 87–93 (2015)

    Google Scholar 

  53. Liu, L., Wang, M., Du, G., Chen, J.: Enhanced hyaluronic acid production of Streptococcus zooepidemicus by an intermittent alkaline-stress strategy. Lett. Appl. Microbiol. 46, 383–388 (2008)

    Google Scholar 

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  1. Vocational School of Health Services, Bingol University, Bingol, Turkey

    Nazli Pinar Arslan

  2. Department of Biology, Science Faculty, Ataturk University, Erzurum, Turkey

    Mehmet Nuri Aydogan

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Correspondence to Nazli Pinar Arslan.

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Arslan, N.P., Aydogan, M.N. Evaluation of Sheep Wool Protein Hydrolysate and Molasses as Low-Cost Fermentation Substrates for Hyaluronic Acid Production by Streptococcus zooepidemicus ATCC 35246. Waste Biomass Valor 12, 925–935 (2021). https://doi.org/10.1007/s12649-020-01062-w

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