Log in

Orange peel waste–based liquid medium for biodiesel production by oleaginous yeasts

  • Bioenergy and biofuels
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Orange peel waste (OPW), the primary byproduct of the juice extraction process, is annually generated in massive amounts (21 Mton), and its aqueous extraction in biorefining operations yields a liquid fraction, referred to as orange peel extract (OPE). Although OPE contains significant amounts of easily assimilable carbohydrates, such as fructose, glucose, and sucrose, no investigations have been conducted yet to assess its possible use in biodiesel production by oleaginous yeasts. Consequently, the objective of the present study was to assess whether OPE might act as the basis of a liquid medium for microbial lipid production. A screening conducted with 18 strains of oleaginous yeasts in shaken flask on the OPE-based medium showed that Rhodosporidium toruloides NRRL 1091 and Cryptococcus laurentii UCD 68-201 gave the best results in terms of lipid production (5.8 and 4.5 g L−1, respectively) and accumulation (77 and 47% on a dry matter basis, respectively). The subsequent scale transfer of the process to a 3-L STR operated in batch mode halved the time required to reach the lipid peak with the ensuing increase in volumetric productivities in R. toruloides NRRL 1091 (3646 mg L−1 day−1) and C. laurentii UCD 68-201 (2970.7 mg L−1 day−1). The biodiesel yields from the lipids of the former and the latter strain were 36.9 and 31.9%, respectively. Based on multivariate analysis of fatty acid methyl ester compositions, the lipids from the former and the latter strain were highly resembling those of Jatropha and palm oils, two commonly used feedstocks for biodiesel manufacturing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Thailand)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ageitos JM, Vallejo JA, Veiga-Crespo P, Villa TG (2011) Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 90:1219–1227

    CAS  Google Scholar 

  • Ainsworth E, Gillespie K (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2:875–877

    CAS  PubMed  Google Scholar 

  • Anderson JM, Ingram JSI (1993) A handbook of methods. Trop. Soil Biol. Fertil. 2nd ed. CAB Int. Wallingford

  • Ángel Siles López J, Li Q, Thompson IP (2010) Biorefinery of waste orange peel. Crit Rev Biotechnol 30:63–69

    PubMed  Google Scholar 

  • Angerbauer C, Siebenhofer M, Mittelbach M, Guebitz GM (2008) Conversion of sewage sludge into lipids by Lipomyces starkeii for biodiesel production. Bioresour Technol 99:3051–3056

    CAS  PubMed  Google Scholar 

  • Atabani AE, Silitonga AS, Badruddin IA, Mahlia TMI, Masjuki HH, Mekhilef S (2012) A comprehensive review on biodiesel as an alternative energy resource and its characteristics. Renew Sust Energ Rev 16:2070–2093

    Google Scholar 

  • Balat M (2011) Potential alternatives to edible oils for biodiesel production - a review of current work. Energy Convers Manag 52:1479–1492

    CAS  Google Scholar 

  • Balu AM, Budarin V, Shuttleworth PS, Pfaltzgraff LA, Waldron K, Luque R, Clark JH (2012) Valorisation of orange peel residues: waste to biochemicals and nanoporous materials. ChemSusChem 5:1694–1697

    CAS  PubMed  Google Scholar 

  • Beopoulos A, Nicaud JM, Gaillardin C (2011) An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Appl Microbiol Biotechnol 90:1193–1206

    CAS  PubMed  Google Scholar 

  • Boluda-Aguilar M, García-Vidal L, del Pilar G-CF, López-Gómez A (2010) Mandarin peel wastes pretreatment with steam explosion for bioethanol production. Bioresour Technol 101(10):3506–3513

    CAS  PubMed  Google Scholar 

  • Carota E, Crognale S, D’Annibale A, Gallo AM, Stazi SR, Petruccioli M (2017) A sustainable use of ricotta cheese whey for microbial biodiesel production. Sci Total Environ 584-585:554–560

    CAS  PubMed  Google Scholar 

  • Carota E, Crognale S, D’Annibale A, Petruccioli M (2018) Bioconversion of agro-industrial waste into microbial oils by filamentous fungi. Process Saf Environ Protect 117:143–151

    CAS  Google Scholar 

  • Castanha RF, Mariano AP, de Morais LAS, Scramin S, Monteiro RTR (2014) Optimization of lipids production by Cryptococcus laurentii 11 using cheese whey with molasses. Brazil J Microbiol 45:379–387

    CAS  Google Scholar 

  • Cho HU, Park JM (2018) Biodiesel production by various oleaginous microorganisms from organic wastes. Bioresour Technol 256:502–508

    CAS  PubMed  Google Scholar 

  • Crognale S, Pesciaroli L, Petruccioli M, D’Annibale A (2012) Phenoloxidase-producing halotolerant fungi from olive brine wastewater. Process Biochem 47:1433–1437

    CAS  Google Scholar 

  • Demirbaş A (1998) Fuel properties and calculation of higher heating values of vegetable oils. Fuel 77:1117–1120

    Google Scholar 

  • Dobrowolski A, Mituła P, Rymowicz W, Mirończuk AM (2016) Efficient conversion of crude glycerol from various industrial wastes into single cell oil by yeast Yarrowia lipolytica. Bioresour Technol 207:237–243

    CAS  PubMed  Google Scholar 

  • Domini C, Vidal L, Cravotto G, Canals A (2009) A simultaneous, direct microwave/ultrasound-assisted digestion procedure for the determination of total Kjeldahl nitrogen. Ultrason Sonochem 16:564–569

    CAS  PubMed  Google Scholar 

  • Dourou M, Mizerakis P, Papanikolaou S, Aggelis G (2017) Storage lipid and polysaccharide metabolism in Yarrowia lipolytica and Umbelopsis isabellina. Appl Microbiol Biotechnol 101:7213–7226

    CAS  PubMed  Google Scholar 

  • Dourou M, Aggeli D, Papanikolaou S, Aggelis G (2018) Critical steps in carbon metabolism affecting lipid accumulation and their regulation in oleaginous microorganisms. Appl Microbiol Biotechnol 102:2509–2523

    CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • El-Nawawi SA, Shehata FR (1987) Extraction of pectin from Egyptian orange peel. Factors affecting the extraction. Biol Wastes 20:281–290

    CAS  Google Scholar 

  • Espina L, Somolinos M, Lorán S, Conchello P, García D, Pagán R (2011) Chemical composition of commercial citrus fruit essential oils and evaluation of their antimicrobial activity acting alone or in combined processes. Food Contr 22:896–902

    CAS  Google Scholar 

  • Fassinou WF, Sako A, Fofana A, Koua KB, Toure S (2010) Fatty acids composition as a means to estimate the high heating value (HHV) of vegetable oils and biodiesel fuels. Energy 35:4949–4954

    CAS  Google Scholar 

  • Fei Q, O’Brien M, Nelson R, Chen X, Lowell A, Dowe N (2016) Enhanced lipid production by Rhodosporidium toruloides using different fed-batch feeding strategies with lignocellulosic hydrolysate as the sole carbon source. Biotechnol Biofuels 9:130

    PubMed  PubMed Central  Google Scholar 

  • Gopinath A, Puhan S, Nagarajan G (2009) Theoretical modeling of iodine value andsaponification value of biodiesel fuels from their fatty acid composition. Renew Energy 34:1806–1811

    CAS  Google Scholar 

  • Izard J, Limberger RJ (2003) Rapid screening method for quantitation of bacterial cell lipids from whole cells. J Microbiol Meth 55:411–418

    CAS  Google Scholar 

  • Kalayasiri P, Jeyashoke N, Krisnangkura K (1996) Survey of seed oils for use as diesel fuels. J Am Oil Chem Soc 73:471–474

    CAS  Google Scholar 

  • Karamerou EE, Webb C (2019) Cultivation modes for microbial oil production using oleaginous yeasts–a review. Biochem Eng J 151:107322

    CAS  Google Scholar 

  • Kiran EU, Trzcinski A, Webb C (2013) Microbial oil produced from biodiesel by-products could enhance overall production. Bioresour Technol 129:650–654

    Google Scholar 

  • Kitcha S, Cheirsilp B (2011) Screening of oleaginous yeasts and optimization for lipid production using crude glycerol as a carbon source. Energy Procedia 9:274–282

    Google Scholar 

  • Knothe G (2005) Dependence of biodiesel fuel properties on the structure of fatty acid alkyl esters. Fuel Process Technol 86:1059–1070

    CAS  Google Scholar 

  • Krisnangkura K (1986) A simple method for estimation of cetane index of vegetable oil methyl esters. J Am Oil Chem Soc 63:552–553

    CAS  Google Scholar 

  • Leiva-Candia DE, Pinzi S, Redel-Macías MD, Koutinas A, Webb C, Dorado MP (2014) The potential for agro-industrial waste utilization using oleaginous yeast for the production of biodiesel. Fuel 123:33–42

    CAS  Google Scholar 

  • Li YH, Liu B, Zhao ZB, Bai FW (2006) Optimized culture medium and fermentation conditions for lipid production by Rhodosporidium toruloides. Chin J Biotechnol 22:650–656

    CAS  Google Scholar 

  • Liu Y, Wang Y, Liu H, Zhang JA (2015) Enhanced lipid production with undetoxified corncob hydrolysate by Rhodotorula glutinis using a high cell density culture strategy. Bioresour Technol 180:32–39

    CAS  PubMed  Google Scholar 

  • Lohrasbi M, Pourbafrani M, Niklasson C, Taherzadeh MJ (2010) Process design and economic analysis of a citrus waste biorefinery with biofuels and limonene as products. Bioresour Technol 101:7382–7388

    CAS  PubMed  Google Scholar 

  • Louhasakul Y, Cheirsilp B (2013) Industrial waste utilization for low-cost production of raw material oil through microbial fermentation. Appl Biochem Biotechnol 169:110–122

    CAS  PubMed  Google Scholar 

  • Luque L, Orr VCA, Chen S, Westerhof R, Oudenhoven S, Rossum GV, Kersten S, Berruti F, Rehmann L (2016) Lipid accumulation from pinewood pyrolysates by Rhodosporidium diobovatum and Chlorella vulgaris for biodiesel production. Bioresour Technol 214:660–669

    CAS  PubMed  Google Scholar 

  • MacGregor JF, Kourti T (1995) Statistical process control of multivariate processes. Control Eng Pract 3:403–414

    Google Scholar 

  • Matsakas L, Bonturi N, Miranda EA, Rova U, Christakopoulos P (2015) High concentrations of dried sorghum stalks as a biomass feedstock for single cell oil production by Rhodosporidium toruloides. Biotechnol Biofuels 8:6

    PubMed  PubMed Central  Google Scholar 

  • Oberoi HS, Vadlani PV, Madl RL, Saida L, Abeykoon JP (2010) Ethanol production from orange peels: two-stage hydrolysis and fermentation studies using optimized parameters through experimental design. J Agric Food Chem 58:3422–3429

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Aggelis G (2011) Lipids of oleaginous yeasts. Part I: Biochemistry of single cell oil production. Eur J Lipid Sci Technol 113:1031–1051

    CAS  Google Scholar 

  • Papanikolaou S, Chevalot I, Komaitis M, Marc I, Aggelis G (2002) Single cell oil production by Yarrowia lipolytica growing on an industrial derivative of animal fat in batch cultures. Appl Microbiol Biotechnol 58:308–312

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Kampisopoulou E, Blanchard F, Rondags E, Gardeli C, Koutinas AA, Chevalot I, Aggelis G (2017) Production of secondary metabolites through glycerol fermentation under carbon-excess conditions by the yeasts Yarrowia lipolytica and Rhodosporidium toruloides. Eur J Lipid Sci Technol 119:1600507

    Google Scholar 

  • Park WK, Moon M, Kwak MS, Jeon S, Choi GG, Yang JW, Lee B (2014) Use of orange peel extract for mixotrophic cultivation of Chlorella vulgaris: increased production of biomass and FAMEs. Bioresour Technol 171:343–349

    CAS  PubMed  Google Scholar 

  • Picataggio SK, Smittle RB (1979) Microbiological production of oil. Eur Pat Appl. EP 5277 A2 19791114

  • Pinzi S, Garcia IL, Lopez-Gimenez FJ, Luque de Castro MD, Dorado G, Dorado MP (2009) The ideal vegetable oil-based biodiesel composition: a review of social, economical and technical implications. Energy Fuel 23:2325–2341

    CAS  Google Scholar 

  • Rangarajan V, Rajasekharan M, Ravichandran R, Sriganesh K, Vaitheeswaran V (2010) Pectinase production from orange peel extract and dried orange peel solid as substrates using Aspergillus niger. Int J Biotechnol Biochem 6:445–453

    Google Scholar 

  • Sandhu KS, Minhas K (2006) Oranges and citrus juices. In: Hui YH (ed) Handbook of fruits and fruit processing. Blackwell, Oxford, pp 309–358

    Google Scholar 

  • Santi G, Jasiulewicz J, Crognale S, D’Annibale A, Petruccioli M, Moresi M (2015) High solid loading in dilute acid hydrolysis of orange peel waste improves ethanol production. Bioenergy Res 8:1292–1302

    CAS  Google Scholar 

  • Santomauro F, Fan J, Budarin VL, Parsons S, Clark J, Miller T, Chuck CJ (2018) Microbial oil produced from the fermentation of microwave-depolymerised rapeseed meal. Bioresour Technol Rep 4:159–165

    Google Scholar 

  • Schutter ME, Dick RP (2000) Comparison of fatty acid methyl ester (FAME) methods for characterizing microbial commun. Soil Sci Soc Am J 64:1659–1668

    CAS  Google Scholar 

  • Sitepu IR, Sestric R, Ignatia L, Levin D, German JB, Gillies LA, Boundy-Mills KL (2013) Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresour Technol 144:360–369

    CAS  PubMed  Google Scholar 

  • Sitepu I, Selby T, Lin T, Zhu S, Boundy-Mills K (2014) Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species. J Ind Microbiol Biotechnol 41:1061–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soccol CR, Dalmas Neto CJJ, Soccol VT, Sydney EB, da Costa ESF, Medeiros ABP, Vandenberghe de Souza LP (2017) Pilot scale biodiesel production from microbial oil of Rhodosporidium toruloides DEBB 5533 using sugarcane juice: performance in diesel engine and preliminary economic study. Bioresour Technol 223:259–268

    CAS  PubMed  Google Scholar 

  • Taylor KA, Buchanan-Smith JG (1992) A colorimetric method for the quantitation of uronic acids and a specific assay for galacturonic acid. Anal Biochem 201:190–196

    CAS  PubMed  Google Scholar 

  • Tchakouteu SS, Chatzifragkou A, Kalantzi O, Koutinas AA, Aggelis G, Papanikolaou S (2015) Oleaginous yeast Cryptococcus curvatus exhibits interplay between biosynthesis of intracellular sugars and lipids. Eur J Lipid Sci Technol 117:657–672

    CAS  Google Scholar 

  • Torrado AM, Cortés S, Salgado JM, Max B, Rodríguez N, Bibbins BP, Converti A, Domínguez JM (2011) Citric acid production from orange peel wastes by solid-state fermentation. Brazil J Microbiol 42:394–409

    CAS  Google Scholar 

  • Tsakona S, Papadaki A, Kopsahelis N, Kachrimanidou V, Papanikolaou S, Koutinas A (2019) Development of a circular oriented bioprocess for microbial oil production using diversified mixed confectionery side-streams. Foods 8:300

    CAS  PubMed Central  Google Scholar 

  • Widmer W, Zhou W, Grohmann K (2010) Pretreatment effects on orange processing waste for making ethanol by simultaneous saccharification and fermentation. Bioresour Technol 101:5242–5249

    CAS  PubMed  Google Scholar 

  • Wiebe MG, Koivuranta K, Penttilä M, Ruohonen L (2012) Lipid production in batch and fed-batch cultures of Rhodosporidium toruloides from 5 and 6 carbon carbohydrates. BMC Biotechnol 12:26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xavier MCA, Coradini ALV, Deckmann AC, Franco TT (2017) Lipid production from hemicellulose hydrolysate and acetic acid by Lipomyces starkeyi and the ability of yeast to metabolize inhibitors. Biochem Eng J 118:11–19

    CAS  Google Scholar 

  • Xu X, Kim JY, Oh YR, Park JM (2014) Production of biodiesel from carbon sources of macroalgae, Laminaria japonica. Bioresour Technol 169:455–461

    CAS  PubMed  Google Scholar 

  • Yen HW, Yang YC, Yu YH (2012) Using crude glycerol and thin stillage for the production of microbial lipids through the cultivation of Rhodotorula glutinis. J Biosci Bioeng 114:453–456

    CAS  PubMed  Google Scholar 

  • Ykema A, Verbree EC, Kater MM, Smit H (1988) Optimization of lipid production in the oleaginous yeast Apiotrichum curvatum in whey permeate. Appl Microbiol Biotechnol 29:211–218

    CAS  Google Scholar 

  • Yong-Hong LI, Bo LIU, Zong-Bao ZHAO, Feng-Wu BAI (2006) Optimization of culture conditions for lipid production by Rhodosporidium toruloides. Chin J Biotechnol 22:650–656

    Google Scholar 

  • Yousuf A, Sannino F, Addorisio V, Pirozzi D (2010) Microbial conversion of olive oil mill wastewaters into lipids suitable for biodiesel production. J Agric Food Chem 58:8630–8635

    CAS  PubMed  Google Scholar 

  • Zhao X, Wu S, Hu C, Wang Q, Hua Y, Zhao ZK (2010) Lipid production from Jerusalem artichoke by Rhodosporidium toruloides Y4. J Ind Microbiol Biotechnol 37:581–585

    CAS  PubMed  Google Scholar 

  • Zhao X, Hu C, Wu S, Shen H, Zhao ZK (2011) Lipid production by Rhodosporidium toruloides Y4 using different substrate feeding strategies. J Ind Microbiol Biotechnol 38:627–632

    CAS  PubMed  Google Scholar 

Download references

Funding

This study was funded by the Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR) within the project “Piano Operativo Nazionale Biofeedstock” (grant no. ARS01_00985).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandro D’Annibale.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 315 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carota, E., Petruccioli, M., D’Annibale, A. et al. Orange peel waste–based liquid medium for biodiesel production by oleaginous yeasts. Appl Microbiol Biotechnol 104, 4617–4628 (2020). https://doi.org/10.1007/s00253-020-10579-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10579-y

Keywords

Navigation