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Fed-batch production of carotenoids by Sporidiobolus salmonicolor (CBS 2636): kinetic and stoichiometric parameters

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Abstract

This work studied the fed-batch production of carotenoids by Sporidiobolus salmonicolor (CBS 2636) using agro-industrial waste as substrates (glycerol, corn steep liquor, parboiled rice waste). The feed rate was varied after 24 h of bioproduction, using glycerol (85 % pure and crude), peptone and malt extract in the feed. The maximum concentration of total carotenoids found was 4,400 μg/L in 96 h of process at the conditions: 25 °C, initial pH 4.0, stirring rate 180 rpm, aeration rate of 1.5 vvm (air volume per volume of culture medium per minute), 80 g/L glycerol, 15 g/L peptone and 5 g/L malt extract, with a feed rate of 112.5 mL each 12 h. The use of crude glycerol yielded maximum carotenoids of 3,009 µg/L. The specific production of carotenoids (Y p/x ) was 859.1 μg/g, and maximum specific growth rate (μ max) was 0.05 h−1. The highest cell production in this study was 0.085 g/L h.

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References

  1. Botella-Pavía P, Rodríguez-Concepción M (2006) Carotenoid biotechnology in plants for nutritionally improved foods. Physiol Plants 126:369–381

    Article  Google Scholar 

  2. Frengova G, Beshkova D (2009) Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Microbiol Biotechnol 36:163–180

    Article  CAS  Google Scholar 

  3. Frengova G, Simova E, Beshkova D (2006) β-Carotene rich carotenoid–protein preparation and exopolysaccharide production by Rhodotorula rubra GED8 grown with a yogurt starter culture. Z Naturforsch 61:571–577

    CAS  Google Scholar 

  4. Venil CK, Zakaria ZA, Ahmad WA (2013) Bacterial pigments and their applications. Process Biochem 48:1065–1079

    Article  CAS  Google Scholar 

  5. El-Agamey A, Lowe GM, Mcgarvey DJ, Mortensen A, Phillip DM, Truscott G, Young AJ (2004) Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 430:37–48

    Article  CAS  Google Scholar 

  6. Andrew J, Young GM (2001) Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 85:20–27

    Google Scholar 

  7. Sotirios K, Vassiliki O (2006) Antioxidant properties of natural carotenoid extracts against the AAPH-initiated oxidation of food emulsions. Innov Food Sci Emerg Technol 7:132–139

    Article  Google Scholar 

  8. Gu Z, Deming C, Yongbin H, Zhigang C, Feirong G (2008) Optimization of carotenoids extraction from Rhodobacter sphaeroides. Food Sci Technol 14:1082–1088

    Google Scholar 

  9. Aguilar CP, González M, Cifuentes AS, Silva M (2004) Growth and accumulation of total carotenoids in two strains of Dunaliella salina Teod. (Chlorophyceae) from the northern and central coast of Perú. J Chilean Chem Soc 49:69–74

    Article  CAS  Google Scholar 

  10. Fazeli MR, Tofighi H, Samadi N, Jamalifar H (2006) Effects of salinity on b-carotene production by Dunaliella tertiolecta DCCBC 26 isolated from Urmia salt lake, North of Iran. Bioresour Technol 97:2453–2456

    Article  CAS  Google Scholar 

  11. Po-Fung I, Feng C (2005) Production of astaxanthin by the green microalga Chlorella zofingiensis in the dark. Process Biochem 40:733–738

    Article  Google Scholar 

  12. García-González M, Moreno J, Manzano JC, Florencio FJ, Guerrero MG (2005) Production of Dunaliella salina biomass rich in 9-cis-β-carotene and lutein in a closed tubular photobioreactor. J Biotechnol 115:81–90

    Article  Google Scholar 

  13. Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality. Trends Food Sci Technol 16:389–406

    Article  Google Scholar 

  14. Johnson EA, Schroeder WA (1995) Microbial carotenoids. Adv Biochem Eng Biotechnol 11:297–326

    Google Scholar 

  15. Goodwin TW (1980) The biochemistry of the carotenoids. Chapman & Hall, London

    Book  Google Scholar 

  16. Hu ZC, Zheng YG, Wang Z, Shen YC (2006) pH control strategy in astaxanthin fermentation bioprocess by Xanthophyllomyces dendrorhous. Enzyme Microb Technol 39:586–590

    Article  CAS  Google Scholar 

  17. Aksu Z, Eren AT (2007) Production of carotenoids by isolated yeast of Rhodotorula glutinis. Biochem Eng J 35:107–113

    Article  CAS  Google Scholar 

  18. Schneider T, Graeff-Hönninger S, French WT, Hernandez R, Merkt N, Claupein W, Hetrick M, Pham P (2013) Lipid and carotenoid production by oleaginous red yeast Rhodotorula glutinis cultivated on brewery effluents. Energy 61:34–43

    Article  CAS  Google Scholar 

  19. Aksu Z, Eren AT (2005) Carotenoids production by the yeast Rhodotorula mucilaginosa: use of agricultural wastes as a carbon source. Process Biochem 40:2985–2991

    Article  CAS  Google Scholar 

  20. Irazusta V, Nieto-Peñalver CG, Cabral ME, Amoroso MJ, Figueroa LIC (2013) Relationship among carotenoid production, copper bioremediation and oxidative stress in Rhodotorula mucilaginosa RCL-11. Process Biochem 48:803–809

    Article  CAS  Google Scholar 

  21. Davoli P, Mierau V, Weber RWS (2004) Carotenoids and fatty acids in red yeasts Sporobolomyces roseus and Rhodotorula glutinis. Appl Biochem Microbiol 40:392–397

    Article  CAS  Google Scholar 

  22. Razavi SH, March I (2006) Effect of temperature and pH on the growth kinetics and carotenoid production by Sporobolomyces ruberrimus H110 using technical glycerol as carbon source. Iran J Chem Eng 23:59–64

    Google Scholar 

  23. Maldonade IR, Rodriguez-Amaya DB, Scamparini ARP (2008) Carotenoids of yeasts isolated from the Brazilian ecosystem. Food Chem 107:145–150

    Article  CAS  Google Scholar 

  24. Valduga E, Valerio A, Treichel H, Di Luccio M, Furigo AJ (2008) Study of the bio-production of carotenoids by Sporidiobolus salmonicolor (CBS 2636) using pre-treated agro-industrial substrates. J Chem Technol Biotechnol 83:1267–1274

    Article  CAS  Google Scholar 

  25. Valduga E, Tatsch PO, Tiggemann L, Treichel H, Toniazzo G, Zeni J, Di Luccio M, Furigo AJ (2009) Carotenoids production: microorganisms as source of natural dyes. Quím Nova 32:2429–2436

    Article  CAS  Google Scholar 

  26. Valduga E, Tatsch PO, Tiggemann L, Zeni J, Colet R, Cansian JM, Treichel H, Di Luccio M (2009) Evaluation of the conditions of carotenoids production in a synthetic medium by Sporidiobolus salmonicolor (CBS 2636) in a bioreactor. Int J Food Sci Technol 44:2445–2451

    Article  CAS  Google Scholar 

  27. Valduga E, Valerio A, Tatsch PO, Treichel H, Furigo AJ, Di Luccio M (2009) Assessment of cell disruption and carotenoids extraction from Sporidiobolus salmonicolor (CBS 2636). Food Bioproc Technol 2:234–238

    Article  CAS  Google Scholar 

  28. Valduga E, Valerio A, Treichel H, Furigo AJ, Di Luccio M (2009) Optimization of the bio-production of total carotenoids by Sporidiobolus salmonicolor (CBS 2636) using response surface technique. Food Bioproc Technol 2:415–421

    Article  CAS  Google Scholar 

  29. Valduga E, Schwartz CRM, Tatsch PO, Tiggemann L, Di Luccio M, Treichel H (2011) Evaluation of aeration and substrate concentration on the production of carotenoids by Sporidiobolus salmonicolor (CBS 2636) in bioreactor. Eur Food Res Technol 232:453–462

    Article  CAS  Google Scholar 

  30. Lim GB, Lee SY, Lee EK, Haam SJ, Kim WS (2002) Separation of astaxanthin from red yeast Phaffia rhodozyma by supercritical carbon dioxide extraction. Biochem Eng J 11:181–187

    Article  CAS  Google Scholar 

  31. Liu YS, Wu JY, Ho KP (2006) Characterization of oxygen transfer conditions and their effects on Phaffia rhodozyma growth and carotenoid production in shake-flask cultures. Biochem Eng J 27:331–335

    Article  Google Scholar 

  32. Bhatt PC, Ahmad M, Panda BP (2013) Enhanced bioaccumulation of astaxanthin in Phaffia rhodozyma by utilising low-cost agro products as fermentation substrate. Biocatal Agric Biotechnol 2:58–63

    Google Scholar 

  33. Saenge C, Cheirsilp B, Suksaroge TT, Bourtoom T (2011) Potential use of oleaginous red yeast Rhodotorula glutinis for the bioconversion of crude glycerol from biodiesel plant to lipids and carotenoids. Process Biochem 446:210–218

    Article  Google Scholar 

  34. Silveira ST, Daroit DJ, Sant’Anna V, Brandelli A (2013) Stability modeling of red pigments produced by Monascus purpureus in submerged cultivations with sugarcane bagasse. Food Bioprocess Technol 6:1007–1014

    Article  CAS  Google Scholar 

  35. Tinoi J, Rakariyatham N, Deming RL (2005) Simplex optimization of carotenoid production by Rhodotorula glutinis using hydrolyzed mung bean waste flour as substrate. Process Biochem 40:2551–2557

    Article  CAS  Google Scholar 

  36. Faria OLV, Koetz PR, Santos MS, Nunes WA (2006) Rice parboilization waste water phosphorus removal by enhanced biological assimilation in sequencing batch reactor (SBR). Cienc Tecn Alim 26:309–317

    Article  CAS  Google Scholar 

  37. Dasari MA, Kiatsimkul PP, Sutterlin WR, Suppes GJ (2005) Low-pressure hydrogenolysis of glycerol to propylene glycol. Appl Catal A Gen 281:225–231

    Article  CAS  Google Scholar 

  38. Cerrate S, Yan F, Wang Z, Coto C, Sacakli P, Waldroup PW (2006) Evaluation of glycerine from biodiesel production as a feed ingredient for broilers. Int J Poult Sci 5:1001–1007

    Article  Google Scholar 

  39. Zheng ZM, Xu YZ, Liu HJ, Guo NN, Cai ZZ, Liu DH (2008) Physiologic mechanisms of sequential products synthesis in 1,3-propanediol fed-batch fermentation by Klebsiella pneumoniae. Biotechnol Bioeng 100:923–932

    Article  CAS  Google Scholar 

  40. Tang S, Boehme L, Lam H, Zhang Z (2009) Pichia pastoris fermentation for phytase production using crude glycerol from biodiesel production as the sole carbon source. Biochem Eng J 43:157–162

    Article  CAS  Google Scholar 

  41. Mu Y, Xiu ZL, Zhang DJ (2007) A combined bioprocess of biodiesel production by of crude glycerol resulting from biodiesel production. Environ Prog 26:338–348

    Article  Google Scholar 

  42. Cavalheiro JMBT, Rodrigo S, Raposo M, Catarina MD, Almeida M, Cesário T, Sevrin C, Grandfils C, Fonseca MMR (2012) Effect of cultivation parameters on the production of poly (3-hydroxybutyrate-co-4-hydroxybutyrate) and poly (3-hydroxybutyrate-4-hydroxybutyrate-3-hydroxyvalerate) by Cupriavidus necator using waste glycerol. Bioresour Technol 111:391–397

    Article  CAS  Google Scholar 

  43. García IL, López JA, Dorado MP, Kopsahelis N, Alexandri M, Papanikolaou S, Villar MA, Koutinas AA (2013) Evaluation of by-products from the biodiesel industry as fermentation feedstock for poly (3-hydroxybutyrate-co-3-hydroxyvalerate) production by Cupriavidus necator. Bioresour Technol 130:16–22

    Article  Google Scholar 

  44. Kachrimanidou V, Kopsahelis N, Chatzifragkou A, Papanikolaou S, Yanniotis S, Kookos I, Apostolis A, Koutinas AA (2013) Utilization of by-products from sunflower-based biodiesel production processes for the production of fermentation feedstock. Waste Biomass Valoriz 4:529–537

    Article  CAS  Google Scholar 

  45. Valduga E, Ribeiro AHR, Cence K, Colet R, Tiggemann L, Zeni J, Toniazzo G (2013) Carotenoids production from a newly isolated Sporidiobolus pararoseus strain using agroindustrial substrates. Biocatal Agric Biotechnol 3:207–213

    Google Scholar 

  46. Gharibzahedi SMT, Razavi SH, Mousavi SM, Moayedi V (2012) High efficiency canthaxanthin production by a novel mutant isolated from Dietzia natronolimnaea HS-1 using central composite design analysis. Ind Crops Prod 40:345–354

    Article  CAS  Google Scholar 

  47. Mcneil B, Harvey LM (1990) Viscous fermentation products. Crit Rev Biotechnol 13:275–304

    Article  Google Scholar 

  48. Ramírez J, Obledo N, Arellano M, Herrera E (2006) Astaxanthin production by Phaffia rhodozyma in a fedbatch culture using a low cost medium feeding. Rev Dig Cient Technol e-Gnosis 4:1–9

    Google Scholar 

  49. Liu YS, Wu JY (2007) Optimization of cell growth and carotenoid production of Xanthophyllomyces dendrorhous through statistical experiment design. Biochem Eng J 36:182–189

    Article  Google Scholar 

  50. Hiss H (2001) Cinética de processos fermentativos. In: Schmidell W, Lima UA, Aquarone E, Borzani W (eds) Biotec Ind: Eng Bioqu, São Paulo: Editora Edgar Blucher Ltda, 6:93–121

  51. Bailey JE, Ollis DF (1986) Biochemical engineering fundamentals, 2nd edn. McGraw Hill Publishing Company, New York, p 984

  52. Davies BH (1976) Carotenoid. In: Goodwin TW (ed) Chem Biochem Plant Pig New York. Academic Press, pp 138–165

  53. Standard UNE-EN 14105 (2003) Determination of free and total glycerol and mono-, di-, triglyceride contents, issued by Asociación Española de Normalización y Certificación, Madrid

  54. Santos JR (2010) Utilization of glycerol as a carbon source for obtaining carotenoids Rhodotorula glutinis. Thesis in Chemical Engineering, Federal University of Ceará, Fortaleza, CE, Brazil

  55. Frengova G, Simova E, Pavlova K, Beshkova D (1994) Formation of carotenoids by Rhodotorula glutinis in whey ultrafiltrate. Biotechnol Bioeng 44:888–894

    Article  CAS  Google Scholar 

  56. Garbayo I, Vilchez C, Nava-Saucedo JE, Barbotin JN (2003) Nitrogen, carbon and light-mediated regulation studies of carotenoid biosynthesis in immobilized mycelia of Gibberella fujikuroi. Enzyme Microb Technol 33:629–634

    Article  CAS  Google Scholar 

  57. Kusdiyantini E, Gaudin P, Goma G, Blanc PJ (1998) Growth kinetics and astaxanthin production of Phaffia rhodozyma on glycerol as a carbon source during batch fermentation. Biotechnol Lett 20:929–934

    Article  CAS  Google Scholar 

  58. Branco LSC, Almeida MMT, Caetano M, Pinto GAS, Azeredo HMC (2010) Study of expansion of scale in the production of biomass Rhodotorula sp. CNPAT-02 in batch process to obtain carotenoids. In: International Congress of Chemical Engineering, 18, 2010, Foz do Iguaçu. Annals. Sao Paulo: Brazilian Association of Chemical Engineering, 2010, pp 6926–6934. 1 CD-Rom

  59. Luna-Flores CH, Ramírez-Cordova JJ, Pelayo-Ortiz C, Femat R, Herrera-López EJ (2010) Batch and fed-batch modeling of carotenoids production by Xanthophyllomyces dendrorhous using Yucca fillifera date juice as substrate. Biochem Eng J 53:131–136

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank CNPq, CAPES and FAPERGS for the financial support and scholarships.

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This article does not contain any studies with human or animal subjects.

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Correspondence to Eunice Valduga.

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Colet, R., Di Luccio, M. & Valduga, E. Fed-batch production of carotenoids by Sporidiobolus salmonicolor (CBS 2636): kinetic and stoichiometric parameters. Eur Food Res Technol 240, 173–182 (2015). https://doi.org/10.1007/s00217-014-2318-5

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