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Spent yeast as an efficient medium supplement for fucoxanthin and eicosapentaenoic acid (EPA) production by Phaeodactylum tricornutum

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Abstract

Fucoxanthin and eicosapentaenoic acid (EPA) are high-value compounds that can be found in the marine diatom Phaeodactylum tricornutum. Yet, the growth rate of this microalga is relatively low under photoautotrophic conditions. The purpose of this study was to evaluate the feasibility of using spent yeast, the second-major by-product of the brewing industry, as a useful substrate for P. tricornutum cultivation. Different pretreatments, concentrations of spent yeast, and initial cell densities of P. tricornutum were investigated. After 12 days of cultivation in f/2 medium, P. tricornutum supplemented with 1.33 g L−1 preautoclaved spent yeast yielded 3.28 times more fucoxanthin (5.97 mg L−1) and 3.55 times more EPA (16.82 mg L−1) than P. tricornutum grown without the yeast (fucoxanthin 1.82 mg L−1, EPA 4.64 mg L−1). Nutrient analysis showed that the nitrogen and phosphorus released by the spent yeast were consumed over time. Overall, spent yeast effectively promoted the fucoxanthin and EPA yields of P. tricornutum.

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References

  • Andersen RA, Morton SL, Sexton JP (1997) Provasoli-Guillard National Center for Culture of Marine Phytoplankton 1997 list of strains. J Phycol 33:1–75

  • Anwaruzzaman SS, Usuda H, Yokota A (1995) Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activation by inorganic phosphate through stimulating the binding of the activator CO2 to the activation sites. Plant Cell Physiol 36:425–433

    CAS  Google Scholar 

  • Apt KE, Grossman AR, Kroth-Pancic PG (1996) Stable nuclear transformation of the diatom Phaeodactylum tricornutum. Mol Gen Genet 252:572–579

    CAS  PubMed  Google Scholar 

  • Avula B, Wang Y-H, Khan IA (2015) Arsenic speciation and fucoxanthin analysis from seaweed dietary supplements using LC-MS. J AOAC Int 98:321–329

    Article  CAS  PubMed  Google Scholar 

  • Botebol H, Sutak R, Scheiber IF, Blaiseau P-L, Bouget F-Y, Camadro J-M, Lesuisse E (2014) Different iron sources to study the physiology and biochemistry of iron metabolism in marine micro-algae. BioMetals 27:75–88

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  • Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C 146:60–78

    Article  CAS  Google Scholar 

  • Carvalho AP, Malcata FX (2005) Optimization of ω-3 fatty acid production by microalgae: crossover effects of CO2 and light intensity under batch and continuous cultivation modes. Mar Biotechnol 7:381–388

    Article  CAS  Google Scholar 

  • Cerón-García MC, Fernández-Sevilla JM, Sánchez-Mirón A, García-Camacho F, Contreras-Gómez A, Molina-Grima E (2013) Mixotrophic growth of Phaeodactylum tricornutum on fructose and glycerol in fed-batch and semi-continuous modes. Bioresour Technol 147:569–576

    Article  CAS  PubMed  Google Scholar 

  • Ceron-Garcia MC, Sánchez Mirón A, Fernández Sevilla JM, Molina Grima E, Garcia Camacho F (2005) Mixotrophic growth of the microalga Phaeodactylum tricornutum: influence of different nitrogen and organic carbon sources on productivity and biomass composition. Process Biochem 40:297–305

    Article  CAS  Google Scholar 

  • Chen K-Q, Li J, Ma J-F, Jiang M, Wei P, Liu Z-M, Ying H-J (2011) Succinic acid production by Actinobacillus succinogenes using hydrolysates of spent yeast cells and corn fiber. Bioresour Technol 102:1704–1708

    Article  CAS  PubMed  Google Scholar 

  • Cohen Z (1994) Production potential of eicosapentaenoic acid by Monodus subterraneus. J Am Oil Chem Soc 71:941–945

    Article  CAS  Google Scholar 

  • Dyhrman ST, Ruttenberg KC (2006) Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnol Oceanogr 51:1381–1390

    Article  CAS  Google Scholar 

  • Fábregas J, Morales ED, Lamela T, Cabezas B, Otero A (1997) Mixotrophic productivity of the marine diatom Phaeodactylum tricornutum cultured with soluble fractions of rye, wheat and potato. World J Microbiol Biotechnol 13:349–351

  • Ferreira IMPLVO, Pinho O, Vieira E, Tavarela JG (2010) Brewer’s Saccharomyces yeast biomass: characteristics and potential applications. Trends Food Sci Technol 21:77–84

    Article  CAS  Google Scholar 

  • Fillaudeau L, Blanpain-Avet P, Daufin G (2006) Water, wastewater and waste management in brewing industries. J Clean Prod 14:463–471

    Article  Google Scholar 

  • Galasso C, Corinaldesi C, Sansone C (2017) Carotenoids from marine organisms: biological functions and industrial applications. Antioxidants 6:96

    Article  CAS  PubMed Central  Google Scholar 

  • Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J Phycol 29:755–766

    Article  CAS  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals: proceedings — 1st conference on culture of marine invertebrate animals greenport. Springer US, Boston, pp 29–60

    Chapter  Google Scholar 

  • Gupta A, Wilkens S, Adcock JL, Puri M, Barrow CJ (2013) Pollen baiting facilitates the isolation of marine Thraustochytrids with potential in omega-3 and biodiesel production. J Ind Microbiol Biotechnol 40:1231–1240

    Article  CAS  PubMed  Google Scholar 

  • Hayward J (1968) Studies on the growth of Phaeodaetylum tricornutum. Physiol Plant 21:100–108

    Article  CAS  Google Scholar 

  • Karas BJ, Diner RE, Lefebvre SC, Mcquaid J, Phillips AP, Noddings CM, Brunson JK, Valas RE, Deerinck TJ, Jablanovic J (2015) Designer diatom episomes delivered by bacterial conjugation. Nat Commun 6:6925

    Article  CAS  PubMed  Google Scholar 

  • Koh HY, Lee JH, Han SJ, Park H, Lee SG (2015) Effect of the antifreeze protein from the arctic yeast Leucosporidium sp. AY30 on cryopreservation of the marine diatom Phaeodactylum tricornutum. Appl Biochem Biotechnol 175:677–686

    Article  CAS  PubMed  Google Scholar 

  • Komoda Y, Isogai Y, Satoh K (1983) Isolation from humus and identification of two growth promoters, adenosine and 2′-deoxyadenosine, effective in culturing the diatom Phaeodactylum tricornutum. Chem Pharm Bull 31:3771–3774

    Article  CAS  Google Scholar 

  • Kustka A, Carpenter EJ, Sañudo-Wilhelmy SA (2002) Iron and marine nitrogen fixation: progress and future directions. Res Microbiol 153:255–262

    Article  CAS  PubMed  Google Scholar 

  • Lin H-Y, Shih C-Y, Liu H-C, Chang J, Chen Y-L, Chen Y-R, Lin H-T, Chang Y-Y, Hsu C-H, Lin H-J (2013) Identification and characterization of an extracellular alkaline phosphatase in the marine diatom Phaeodactylum tricornutum. Mar Biotechnol 15:425–436

    Article  CAS  Google Scholar 

  • McClure DD, Luiz A, Gerber B, Barton GW, Kavanagh JM (2018) An investigation into the effect of culture conditions on fucoxanthin production using the marine microalgae Phaeodactylum tricornutum. Algal Res 29:41–48

    Article  Google Scholar 

  • Milligan AJ, Harrison PJ (2000) Effects of non-steady-state iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 36:78–86

    Article  CAS  Google Scholar 

  • Mu K, Wang S, Kitts D (2016) Evidence to indicate that Maillard reaction products can provide selective antimicrobial activity. Integr Food Nutr Metab 3:330–335

    Article  Google Scholar 

  • Myers J (1953) Growth characteristics of algae in relation to the problems of mass culture. In: Algal culture from laboratory to pilot plant, vol 600. Carnegie Institute of Washington, pp 37–50

  • Nur MMA, Muizelaar W, Boelen P, Buma AGJ (2019) Environmental and nutrient conditions influence fucoxanthin productivity of the marine diatom Phaeodactylum tricornutum grown on palm oil mill effluent. J Appl Phycol 31:111–122

    Article  CAS  Google Scholar 

  • O’Brien J, Morrissey PA, Ames JM (1989) Nutritional and toxicological aspects of the Maillard browning reaction in foods. Crit Rev Food Sci Nutr 28:211–248

    Article  PubMed  Google Scholar 

  • Ou L, Cai Y, Jin W, Wang Z, Lu S (2018) Understanding the nitrogen uptake and assimilation of the Chinese strain of Aureococcus anophagefferens (Pelagophyceae). Algal Res 34:182–190

    Article  Google Scholar 

  • Patel A, Matsakas L, Hrůzová K, Rova U, Christakopoulos P (2019) Biosynthesis of nutraceutical fatty acids by the oleaginous marine microalgae Phaeodactylum tricornutum utilizing hydrolysates from organosolv-pretreated birch and spruce biomass. Mar Drugs 17:119

    Article  CAS  PubMed Central  Google Scholar 

  • Perezgarcia O, Escalante FME, Debashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36

    Article  CAS  Google Scholar 

  • Rakowska R, Sadowska A, Dybkowska E, F Ś (2017) Spent yeast as natural source of functional food additives. Rocz Panstw Zakl Hig 68 (2):115–121

  • Seo S, Jeon H, Chang KS, Jin E (2018) Enhanced biomass production by Phaeodactylum tricornutum overexpressing phosphoenolpyruvate carboxylase. Algal Res 31:489–496

    Article  Google Scholar 

  • Silva Benavides AM, Torzillo G, Kopecký J, Masojídek J (2013) Productivity and biochemical composition of Phaeodactylum tricornutum (Bacillariophyceae) cultures grown outdoors in tubular photobioreactors and open ponds. Biomass Bioenergy 54:115–122

    Article  CAS  Google Scholar 

  • Singh B, Satyanarayana T (2011) Microbial phytases in phosphorus acquisition and plant growth promotion. Physiol Mol Biol Plants 17:93–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slattery SS, Diamond A, Wang H, Therrien JA, Lant JT, Jazey T, Lee K, Klassen Z, Desgagné-Penix I, Karas BJ, Edgell DR (2018) An expanded plasmid-based genetic toolbox enables cas9 genome editing and stable maintenance of synthetic pathways in Phaeodactylum tricornutum. ACS Synth Biol 7:328–338

    Article  CAS  PubMed  Google Scholar 

  • Stukenberg D, Zauner S, Dell’Aquila G, Maier UG (2018) Optimizing CRISPR/Cas9 for the diatom Phaeodactylum tricornutum. Front Plant Sci 9:740

  • Tanguler H, Erten H (2008) Utilisation of spent brewer’s yeast for yeast extract production by autolysis: the effect of temperature. Food Bioprod Process 86:317–321

    Article  Google Scholar 

  • Timm U, Klinck JM, Okubo A (1991) Self- and mutual shading and competition effect on competing algal distributions: biological implications of the model. Ecol Model 59:11–36

    Article  Google Scholar 

  • Tocher DR, Betancor MB, Sprague M, Olsen RE, Napier JA (2019) Omega-3 long-chain polyunsaturated fatty acids, EPA and DHA: bridging the gap between supply and demand. Nutrients 11:89

    Article  CAS  PubMed Central  Google Scholar 

  • Veronesiv D, D’Imporzano G, Salati S, Adani F (2017) Pre-treated digestate as culture media for producing algal biomass. Ecol Eng 105:335–340

    Article  Google Scholar 

  • Weyman PD, Beeri K, Lefebvre SC, Rivera J, Mccarthy JK, Heuberger AL, Peers G, Allen AE, Dupont CL (2015) Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis. Plant Biotechnol J 13:460–470

    Article  CAS  PubMed  Google Scholar 

  • Wheeler PA, North BB, Stephens GC (1974) Amino acid uptake by marine phytoplankters. Limnol Oceanogr 19:249–259

    Article  CAS  Google Scholar 

  • Wu H, Li T, Wang G, Dai S, He H, Xiang W (2016) A comparative analysis of fatty acid composition and fucoxanthin content in six Phaeodactylum tricornutum strains from diff erent origins. Chin J Oceanol Limnol 34:391–398

    Article  CAS  Google Scholar 

  • Yongmanitchai W, Ward OP (1991) Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Appl Environ Microbiol 57:419–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamalloa C, De Vrieze J, Boon N, Verstraete W (2012) Anaerobic digestibility of marine microalgae Phaeodactylum tricornutum in a lab-scale anaerobic membrane bioreactor. Appl Microbiol Biotechnol 93:859–869

    Article  CAS  PubMed  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE (2000) Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36:379–386

    Article  CAS  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE (2001) Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science 292:2073–2075

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Wang F, Gao B, Huang L, Zhang C (2018) An integrated biorefinery process: stepwise extraction of fucoxanthin, eicosapentaenoic acid and chrysolaminarin from the same Phaeodactylum tricornutum biomass. Algal Res 32:193–200

    Article  Google Scholar 

  • Zhao P, Gu W, Huang A, Wu S, Liu C, Huan L, Gao S, Xie X, Wang G (2018) Effect of iron on the growth of Phaeodactylum tricornutum via photosynthesis. J Phycol 54:34–43

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by the Natural Science Foundation of Fujian Province (Grant No. 2017J01622) and the Sugar Crop Research System (Grant No. CARS-170501).

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Authors and Affiliations

  1. The Public Service Platform for Industrialization Development Technology of Marine Biological Medicine and Product of State Oceanic Administration, College of Life Sciences, Fujian Normal University, Fuzhou, 350117, People’s Republic of China

    Xue Yuan, Limin Liang, Kui Liu, Luqiang Huang, Wenjin He, Youqiang Chen & Ting Xue

  2. Center of Engineering Technology Research for Microalgae Germplasm Improvement of Fujian, Southern Institute of Oceanography, Fujian Normal University, Fuzhou, 350117, People’s Republic of China

    Xue Yuan, Limin Liang, Lijuan Xie, Luqiang Huang, Youqiang Chen & Ting Xue

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  1. Xue Yuan
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  2. Limin Liang
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Yuan, X., Liang, L., Liu, K. et al. Spent yeast as an efficient medium supplement for fucoxanthin and eicosapentaenoic acid (EPA) production by Phaeodactylum tricornutum. J Appl Phycol 32, 59–69 (2020). https://doi.org/10.1007/s10811-019-01909-3

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