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Sources of microbial oils with emphasis to Mortierella (Umbelopsis) isabellina fungus

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Abstract

The last years a constantly rising number of publications have appeared in the literature in relation to the production of oils and fats deriving from microbial sources (the “single cell oils”—SCOs). SCOs can be used as precursors for the synthesis of lipid-based biofuels or employed as substitutes of expensive oils rarely found in the plant or animal kingdom. In the present review-article, aspects concerning SCOs (economics, biochemistry, substrates, technology, scale-up), with emphasis on the potential of Mortierella isabellina were presented. Fats and hydrophilic substrates have been used as carbon sources for cultivating Zygomycetes. Among them, wild-type M. isabellina strains have been reported as excellent SCO-producers, with conversion yields on sugar consumed and lipid in DCW values reported comparable to the maximum ones achieved for genetically engineered SCO-producing strains. Lipids produced on glucose contain γ-linolenic acid (GLA), a polyunsaturated fatty acid (PUFA) of high dietary and pharmaceutical importance, though in low concentrations. Nevertheless, due to their abundance in oleic acid, these lipids are perfect precursors for the synthesis of 2nd generation biodiesel, while GLA can be recovered and directed to other usages. Genetic engineering focusing on over-expression of Δ6 and Δ12 desaturases and of C16 elongase may improve the fatty acid composition (viz. increasing the concentration of GLA or other nutritionally important PUFAs) of these lipids.

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Fig. 1

[Adapted from Papanikolaou and Aggelis (2010), Papanikolaou and Aggelis (2011a) and Vasiliadou et al. (2018)]

Fig. 2

[Adapted from Ratledge (1987), Ratledge and Wynn (2002), Papanikolaou et al. (2008), Papanikolaou and Aggelis (2009) and Papanikolaou and Aggelis (2011a)]

Fig. 3

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References

  • Aggelis G (1996) Two alternative pathways for substrate assimilation by Mucor circinelloides. Folia Microbiol 41:254–256

    CAS  Google Scholar 

  • Aggelis G, Ratomahenina R, Arnaud A, Galzy P, Martin-Privat P, Perraud JP, Pina M, Graille J (1988) Etude de l’influence des conditions de culture sur la teneur en acide gamma linolénique de souches de Mucor. Oléagineux 43:311–317

    CAS  Google Scholar 

  • Aggelis G, Komaitis M, Papanikolaou S, Papadopoulos G (1995a) A mathematical model for the study of lipid accumulation in oleaginous microorganisms. I. Lipid accumulation during growth of Mucor circinelloides CBS 172-27 on a vegetable oil. Gracas y Aceites 46:169–173

    CAS  Google Scholar 

  • Aggelis G, Komaitis M, Papanikolaou S, Papadopoulos G (1995b) A mathematical model for the study of lipid accumulation in oleaginous micro-organisms: II. Study of cellular lipids of Mucor circinelloides CBS 172-27 during growth on a vegetable oil. Grasas Aceites 46:245–250

    CAS  Google Scholar 

  • Aggelis G, Papadiotis G, Komaitis M (1997) Microbial fatty acid specificity. Folia Microbiol 42:117–120

    CAS  Google Scholar 

  • Alakhras R, Bellou S, Fotaki G, Stephanou G, Demopoulos N, Papanikolaou S, Aggelis G (2015) Fatty acid lithium salts from Cunninghamella echinulata have cytotoxic and genotoxic effects on HL-60 human leukemia cells. Eng Life Sci 15:243–253

    CAS  Google Scholar 

  • Aoki H, Miyamoto N, Furuya Y, Mankura M, Endo Y, Fujimoto K (2002) Incorporation and accumulation of docosahexaenoic acid from the medium by Pichia methanolica HA-32. Biosci Biotechnol Biochem 66:2632–2638

    CAS  PubMed  Google Scholar 

  • Athenaki M, Gardeli C, Diamantopoulou P, Tchakouteu SS, Sarris D, Philippoussis A, Papanikolaou S (2018) Lipids from yeasts and fungi: physiology, production and analytical considerations. J Appl Microbiol 124:336–367

    CAS  PubMed  Google Scholar 

  • Barre E (2009) Borage, evening primrose, blackcurrant, and fungal oils: γ-linolenic acid-rich oils. In: Moreau RA, Kamal-Eldin A (eds) Gourmet and health-promoting specialty oils. Academic Press and AOCS Press, Champaign, pp 237–266

    Google Scholar 

  • Bati N, Hammond EG, Glatz BA (1984) Biomodification of fats and oils: trials with Candida lipolytica. J Am Oil Chem Soc 61:1743–1746

    CAS  Google Scholar 

  • Bellou S, Aggelis G (2012) Biochemical activities in Chlorella sp. and Nannochloropsis salina during lipid and sugar synthesis in a lab-scale open pond simulating reactor. J Biotechnol 164:318–329

    CAS  PubMed  Google Scholar 

  • Bellou S, Moustogianni A, Makri A, Aggelis G (2012) Lipids containing polyunsaturated fatty acids synthesized by zygomycetes grown on glycerol. Appl Biochem Biotechnol 166:146–158

    CAS  PubMed  Google Scholar 

  • Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493

    CAS  PubMed  Google Scholar 

  • Bellou S, Triantaphyllidou IE, Aggeli D, Elazzazy AM, Baeshen MN, Aggelis G (2016) Microbial oils as food additives: recent approaches for improving microbial oil production and its polyunsaturated fatty acid content. Curr Opin Biotechnol 37:24–35

    CAS  PubMed  Google Scholar 

  • Beopoulos A, Mrozova Z, Thevenieau F, Le Dall MT, Hapala I, Papanikolaou S, Chardot T, Nicaud JM (2008) Control of lipid accumulation in the yeast Yarrowia lipolytica. Appl Environ Microbiol 74:7779–7789

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beopoulos A, Haddouche R, Kabran P, Dulermo T, Chardot T, Nicaud JM (2012) Identification and characterization of DGA2, an acyltransferase of the DGAT1 acyl-CoA:diacylglycerol acyltransferase family in the oleaginous yeast Yarrowia lipolytica. New insights into the storage lipid metabolism of oleaginous yeasts. Appl Microbiol Biotechnol 93:1523–1537

    CAS  PubMed  Google Scholar 

  • Blazeck J, Hill A, Liu L, Knight R, Miller J, Pan A, Otoupal P, Alper HS (2014) Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production. Nat Commun 5:3131

    PubMed  Google Scholar 

  • Cai G, Moghaddam L, O’Hara IM, Zhang Z (2019) Microbial oil production from acidified glycerol pretreated sugarcane bagasse by Mortierella isabellina. RSC Adv 9:2539–2550

    CAS  Google Scholar 

  • Carsanba E, Papanikolaou S, Erten H (2018) Production of oils and fats by oleaginous microorganisms with an emphasis given to the potential of the nonconventional yeast Yarrowia lipolytica. Crit Rev Biotechnol 38:1230–1243

    CAS  PubMed  Google Scholar 

  • Čertik M, Shimizu S (1999) Biosynthesis and regulation of microbial polyunsaturated fatty acid production. J Biosci Bioeng 87:1–14

    PubMed  Google Scholar 

  • Čertik M, Balteszova L, Sajbidor J (1997) Lipid formation and γ-linolenic acid production by Mucorales fungi grown on sunflower oil. Lett Appl Microbiol 25:101–105

    Google Scholar 

  • Chatzifragkou A, Fakas S, Galiotou-Panayotou M, Komaitis M, Aggelis G, Papanikolaou S (2010) Commercial sugars as substrates for lipid accumulation in Cunninghamella echinulata and Mortierella isabellina. Eur J Lipid Sci Technol 112:1048–1057

    CAS  Google Scholar 

  • Dahiya JS (1991) Xylitol production by Petromyces albertensis grown on medium containing D-xylose. Can J Microbiol 37:14–18

    CAS  Google Scholar 

  • Daskalaki A, Vasiliadou IA, Bellou S, Tomaszewska-Hetman L, Chatzikotoula C, Kompoti B, Papanikolaou S, Vayenas D, Pavlou S, Aggelis G (2018) Data on cellular lipids of Yarrowia lipolytica grown on fatty substrates. Data Brief 21:1037–1044

    PubMed  PubMed Central  Google Scholar 

  • Davies RJ (1988) Yeast oil from cheese whey—process development. In: Moreton RS (ed) Single cell oil. Longman Scientific & Technical, Longman House, Burnt Mill, Harlow, pp 99–146

    Google Scholar 

  • Davies RJ, Holdsworth JE (1992) Synthesis of lipids in yeasts: biochemistry, physiology and production. Adv Appl Lipid Res 1:119–159

    CAS  Google Scholar 

  • Davies JL, Wobeser GA (2010) Systemic infection with Mortierella wolfii following abortion in a cow. Can Vet J 51:1391–1393

    PubMed  PubMed Central  Google Scholar 

  • Dellomonaco C, Clomburg JM, Miller EN, Gonzalez R (2011) Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 476:355–359

    CAS  PubMed  Google Scholar 

  • Demir M, Turhan I, Kucukcetin A, Alpkent Z (2013) Oil production by Mortierella isabellina from whey treated with lactase. Bioresour Technol 128:365–369

    CAS  PubMed  Google Scholar 

  • Diamantopoulou P, Papanikolaou S, Katsarou E, Komaitis M, Aggelis G, Philippoussis A (2012) Mushroom polysaccharides and lipids synthesized in liquid agitated and static cultures. Part II: study of Volvariella volvacea. Appl Biochem Biotechnol 167:1890–1906

    CAS  PubMed  Google Scholar 

  • Diamantopoulou P, Papanikolaou S, Komaitis M, Aggelis G, Philippoussis A (2014) Patterns of major metabolites biosynthesis by different mushroom fungi grown on glucose-based submerged cultures. Bioprocess Biosyst Eng 37:1385–1400

    CAS  PubMed  Google Scholar 

  • Diamantopoulou P, Papanikolaou S, Aggelis G, Philippoussis A (2016) Adaptation of Volvariella volvacea metabolism in high carbon to nitrogen ratio media. Food Chem 196:272–280

    CAS  PubMed  Google Scholar 

  • Diwan B, Parkhey P, Gupta P (2018) From agro-industrial wastes to single cell oils: a step towards prospective biorefinery. Folia Microbiol 63:547–568

    CAS  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 

  • Dulermo T, Nicaud JM (2011) Involvement of the G3P shuttle and β-oxidation pathway in the control of TAG synthesis and lipid accumulation in Yarrowia lipolytica. Metab Eng 13:482–491

    CAS  PubMed  Google Scholar 

  • Dulermo T, Tréton B, Beopoulos A, Kabran Gnankon AP, Haddouche R, Nicaud JM (2013) Characterization of the two intracellular lipases of Y. lipolytica encoded by TGL3 and TGL4 genes: new insights into the role of intracellular lipases and lipid body organisation. Biochim Biophys Acta 1831:1486–1495

    CAS  PubMed  Google Scholar 

  • Dyal SD, Narine SS (2005) Implications for the use of Mortierella fungi in the industrial production of essential fatty acids. Food Res Int 38:445–467

    CAS  Google Scholar 

  • Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011a) Modelling of single-cell oil production under nitrogen limited and substrate inhibition conditions. Biotechnol Bioeng 108:1049–1055

    CAS  PubMed  Google Scholar 

  • Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011b) Single cell oil production from rice hulls hydrolysate. Bioresour Technol 102:9737–9742

    CAS  PubMed  Google Scholar 

  • Fakas S, Papanikolaou S, Batsos A, Galiotou-Panayotou M, Mallouchos A, Aggelis G (2009) Evaluating renewable carbon sources as substrates for single cell oil production by Cunninghamella echinulata and Mortierella isabellina. Biomass Bioenergy 33:573–580

    CAS  Google Scholar 

  • Fang H, Zhao C, Chen S (2016) Single cell oil production by Mortierella isabellina from steam exploded corn stover degraded by three-stage enzymatic hydrolysis in the context of on-site enzyme production. Bioresour Technol 216:988–995

    CAS  PubMed  Google Scholar 

  • Fickers P, Benetti PH, Waché Y, Marty A, Mauersberger S, Smit MS, Nicaud JM (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543

    CAS  PubMed  Google Scholar 

  • Gao D, Zeng J, Yu X, Dong T, Chen S (2014) Improved lipid accumulation by morphology engineering of oleaginous fungus Mortierella isabellina. Biotechnol Bioeng 111:1758–1766

    CAS  PubMed  Google Scholar 

  • Gardeli C, Athenaki M, Xenopoulos E, Mallouchos A, Koutinas AA, Aggelis G, Papanikolaou S (2017) Lipid production and characterization by Mortierella (Umbelopsis) isabellina cultivated on lignocellulosic sugars. J Appl Microbiol 123:1461–1477

    CAS  PubMed  Google Scholar 

  • Harde SM, Wang Z, Horne M, Zhu JY, Pan X (2016) Microbial lipid production from SPORL-pretreated Douglas fir by Mortierella isabellina. Fuel 175:64–74

    CAS  Google Scholar 

  • Huang C, Chen XF, Xiong L, Chen XD, Ma LL, Chen Y (2013) Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv 31:129–139

    CAS  PubMed  Google Scholar 

  • Ikeuchi T, Azuma M, Kato J, Ooshima H (1999) Screening of microorganisms for xylitol production and fermentation behavior in high concentrations of xylose. Biomass Bioenergy 16:333–339

    CAS  Google Scholar 

  • Kendrick A, Ratledge C (1996) Cessation of polyunsaturated fatty acid formation in four selected filamentous fungi when grown on plant oils. J Am Oil Chem Soc 73:431–435

    CAS  Google Scholar 

  • Kennedy MJ, Reader SL, Davies J, Rhoades DA, Silby HW (1994) The scale up of mycelial shake flask fermentations: a case study of gamma linolenic acid production by Mucor hiemalis IRL 51. J Ind Microbiol 13:212–216

    CAS  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 

  • Koritala S, Hesseltine CW, Pryde EH, Mounts TL (1987) Biochemical modification of fats by microorganisms: a preliminary study. J Am Oil Chem Soc 64:509–513

    CAS  Google Scholar 

  • Koutinas AA, Chatzifragkou A, Kopsahelis N, Papanikolaou S, Kookos IK (2014a) Design and techno-economic evaluation of microbial oil production as a renewable resource for biodiesel and oleochemical production. Fuel 116:566–577

    CAS  Google Scholar 

  • Koutinas AA, Vlysidis A, Pleissner D, Kopsahelis N, Garcia IL, Kookos IK, Papanikolaou S, Kwan TH, Lin SKC (2014b) Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. Chem Soc Rev 43:2587–2627

    CAS  PubMed  Google Scholar 

  • Kumar I, Ramalakshmi MA, Sivakumar U, Santhanakrishnan P, Zhan X (2011) Production of microbial oils from Mortierella sp. for generation of biodiesel livestock. Afr J Microbiol Res 5:4105–4111

    CAS  Google Scholar 

  • Leber C, Polson B, Fernandez-Moya R, Da Silva NA (2015) Overproduction and secretion of free fatty acids through disrupted neutral lipid recycle in Saccharomyces cerevisiae. Metab Eng 28:54–62

    CAS  PubMed  Google Scholar 

  • Matsuo T, Terashima M, Hashimoto Y, Hasida W (1981) Method for producing cacao butter substitute. US Patent 4,308,350

  • Meeuwse P, Tramper J, Rinzema A (2011a) Modeling lipid accumulation in oleaginous fungi in chemostat cultures: I. Development and validation of a chemostat model for Umbelopsis isabellina. Bioprocess Biosyst Eng 34:939–949

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meeuwse P, Tramper J, Rinzema A (2011b) Modeling lipid accumulation in oleaginous fungi in chemostat cultures. II: validation of the chemostat model using yeast culture data from literature. Bioprocess Biosyst Eng 34:951–961

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meeuwse P, Akbari P, Tramper J, Rinzema A (2012) Modeling growth, lipid accumulation and lipid turnover in submerged batch cultures of Umbelopsis isabellina. Bioprocess Biosyst Eng 35:591–603

    CAS  PubMed  Google Scholar 

  • Meeuwse P, Sanders JPM, Tramper J, Rinzema A (2013) Lipids from yeasts and fungi: tomorrow’s source of biodiesel? Biofuel Bioprod Biorefin 7:512–524

    CAS  Google Scholar 

  • Metzger JO, Bornscheuer U (2006) Lipids as renewable resources: current state of chemical and biotechnological conversion and diversification. Appl Microbiol Biotechnol 71:13–22

    CAS  PubMed  Google Scholar 

  • Meyer KH, Schweizer E (1976) Control of fatty-acid synthetase levels by exogenous long-chain fatty acids in the yeasts Candida lipolytica and Saccharomyces cerevisiae. Eur J Biochem 65:317–324

    CAS  PubMed  Google Scholar 

  • Mličková K, Luo Y, D’Andrea S, Peč P, Chardot T, Nicaud JM (2004) Acyl-CoA oxidase, a key step for lipid accumulation in the yeast Yarrowia lipolytica. J Mol Catal B 28:81–85

    Google Scholar 

  • Moser BR (2009) Biodiesel production, properties, and feedstocks. In Vitro Cell Develop Biol Plant 45:229–266

    CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2009) Biotechnological valorization of biodiesel derived glycerol waste through production of single cell oil and citric acid by Yarrowia lipolytica. Lipid Technol 21:83–87

    CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2010) Yarrowia lipolytica: a model microorganism used for the production of tailor-made lipids. Eur J Lipid Sci Technol 112:639–654

    CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2011a) 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, Aggelis G (2011b) Lipids of oleaginous yeasts. Part II: technology and potential applications. Eur J Lipid Sci Technol 113:1052–1073

    CAS  Google Scholar 

  • Papanikolaou S, Chevalot I, Komaitis M, Aggelis G, Marc I (2001) Kinetic profile of the cellular lipid composition in an oleaginous Yarrowia lipolytica capable of producing a cocoa-butter substitute from industrial fats. Antonie Van Leeuwenhoek 80:215–224

    CAS  PubMed  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, Muniglia L, Chevalot I, Aggelis G, Marc I (2003) Accumulation of a cocoa-butter-like lipid by Yarrowia lipolytica cultivated on agro-industrial residues. Curr Microbiol 46:124–130

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Sarantou S, Komaitis M, Aggelis G (2004a) Repression of reserve lipid turnover in Cunninghamella echinulata and Mortierella isabellina cultivated in multiple-limited media. J Appl Microbiol 97:867–875

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Komaitis M, Aggelis G (2004b) Single cell oil (SCO) production by Mortierella isabellina grown on high-sugar content media. Bioresour Technol 95:287–291

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Galiotou-Panayotou M, Chevalot I, Komaitis M, Marc I, Aggelis G (2006) Influence of glucose and saturated free-fatty acid mixtures on citric acid and lipid production by Yarrowia lipolytica. Curr Microbiol 52:134–142

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2007a) Industrial derivative of tallow: a promising renewable substrate for microbial lipid, single-cell protein and lipase production by Yarrowia lipolytica.. Electron J Biotechnol 10:425–435

    CAS  Google Scholar 

  • Papanikolaou S, Galiotou-Panayotou M, Fakas S, Komaitis M, Aggelis G (2007b) Lipid production by oleaginous Mucorales cultivated on renewable carbon sources. Eur J Lipid Sci Technol 109:1060–1070

    CAS  Google Scholar 

  • Papanikolaou S, Fakas S, Fick M, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2008) Biotechnological valorisation of raw glycerol discharged after bio-diesel (fatty acid methyl-esters) manufacturing process: production of 1,3-propanediol, citric acid and single cell oil. Biomass Bioenergy 32:60–71

    CAS  Google Scholar 

  • Papanikolaou S, Dimou A, Fakas S, Diamantopoulou P, Philippoussis A, Galiotou-Panayotou M, Aggelis G (2011) Biotechnological conversion of waste cooking olive oil into lipid-rich biomass using Aspergillus and Penicillium strains. J Appl Microbiol 110:1138–1150

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Beopoulos A, Koletti A, Thevenieau F, Koutinas AA, Nicaud JM, Aggelis G (2013) Importance of the methyl-citrate cycle on glycerol metabolism in the yeast Yarrowia lipolytica. J Biotechnol 168:303–314

    CAS  PubMed  Google Scholar 

  • Papanikolaou S, Rontou M, Belka A, Athenaki M, Gardeli C, Mallouchos A, Kalantzi O, Koutinas AA, Kookos IK, Zeng AP, Aggelis G (2017) Conversion of biodiesel-derived glycerol into biotechnological products of industrial significance by yeast and fungal strains. Eng Life Sci 17:262–281

    CAS  Google Scholar 

  • Patel A, Arora N, Sartaj K, Pruthi V, Pruthi PA (2016) Sustainable biodiesel production from oleaginous yeasts utilizing hydrolysates of various non-edible lignocellulosic biomasses. Renew Sustain Energy Rev 62:836–855

    CAS  Google Scholar 

  • Patel A, Arora N, Mehtani J, Pruthi V, Pruthi PA (2017) Assessment of fuel properties on the basis of fatty acid profiles of oleaginous yeast for potential biodiesel production. Renew Sustain Energy Rev 77:604–616

    CAS  Google Scholar 

  • Philippoussis A, Diamantopoulou P (2012) Exploitation of the biotechnological potential of agro-industrial by-products through mushroom cultivation. In: Petre M, Berovic M (eds) Mushroom biotechnology and bioengineering. University of Pitesti, CD Press, Bucharest, pp 161–184

    Google Scholar 

  • Qiao K, Imam Abidi SH, Liu H, Zhang H, Chakraborty S, Watson N, Kumaran Ajikumar P, Stephanopoulos G (2015) Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica. Metab Eng 29:56–65

    CAS  PubMed  Google Scholar 

  • Qiao K, Wasylenko TM, Zhou K, Xu P, Stephanopoulos G (2017) Lipid production in Yarrowia lipolytica is maximized by engineering cytosolic redox metabolism. Nat Biotechnol 35:173–177

    CAS  PubMed  Google Scholar 

  • Qin L, Liu L, Zeng AP, Wei D (2017) From low-cost substrates to single cell oils synthesized by oleaginous yeasts. Bioresour Technol 245:1507–1519

    CAS  PubMed  Google Scholar 

  • Ratledge C (1987) Lipid biotechnology: a wonderland for the microbial physiologist. J Am Oil Chem Soc 64:1647–1656

    CAS  Google Scholar 

  • Ratledge C (1988) Biochemistry, stoichiometry, substrates and economics. In: Moreton RS (ed) Single cell oil. Longman Scientific & Technical, Longman House, Burnt Mill, Harlow, pp 33–70

    Google Scholar 

  • Ratledge C (1994) Yeasts, moulds, algae and bacteria as sources of lipids. In: Kamel BS, Kakuda Y (eds) Technological advances in improved and alternative sources of lipids. Blackie Academic and Professional, London, pp 235–291

    Google Scholar 

  • Ratledge C (2011) Are algal oils realistic options for biofuels? Eur J Lipid Sci Technol 113:135–136

    CAS  Google Scholar 

  • Ratledge C (2013a) Microbial oils: an introductory overview of current status and future prospects. Oilseeds Fats Crops Lipids (OCL) 20:D602

    Google Scholar 

  • Ratledge C (2013b) Oils from microalgae: achievements and prospects http://bioprosp.com/programme/2013/oils-microalgae-achievements-and-prospects. Accessed 22 Mar 2017

  • Ratledge C, Cohen Z (2008) Microbial and algal oils: do they have a future for biodiesel or as commodity oils? Lipid Technol 20:155–160

    Google Scholar 

  • Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51

    CAS  PubMed  Google Scholar 

  • Rogers PJ, Clark-Walker GD, Stewart PR (1974) Effects of oxygen and glucose on energy metabolism and dimorphism of Mucor genevensis grown in continuous culture: reversibility of yeast-mycelium conversion. J Bacteriol 119:282–293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roux-Van der Merwe MP, Badenhorst J, Britz TJ (2005) Fungal treatment of an edible-oil-containing industrial effluent. World J Microbiol Biotechnol 21:947–953

    Google Scholar 

  • Ruan Z, Zanotti M, Wang X, Ducey C, Liu Y (2012) Evaluation of lipid accumulation from lignocellulosic sugars by Mortierella isabellina for biodiesel production. Bioresour Technol 110:198–205

    CAS  PubMed  Google Scholar 

  • Ruan Z, Zanotti M, Zhong Y, Liao W, Ducey C, Liu Y (2013) Co-hydrolysis of lignocellulosic biomass for microbial lipid accumulation. Biotechnol Bioeng 110:1039–1049

    CAS  PubMed  Google Scholar 

  • Ruan Z, Zanotti M, Archer S, Liao W, Liu Y (2014) Oleaginous fungal lipid fermentation on combined acid- and alkali-pretreated corn stover hydrolysate for advanced biofuel production. Bioresour Technol 163:12–17

    CAS  PubMed  Google Scholar 

  • Ruan Z, Hollinshead W, Isaguirre C, Tang YJ, Liao W, Liu Y (2015) Effects of inhibitory compounds in lignocellulosic hydrolysates on Mortierella isabellina growth and carbon utilization. Bioresour Technol 183:18–24

    CAS  PubMed  Google Scholar 

  • Rywińska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W (2013) Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenergy 48:148–166

    Google Scholar 

  • Sakuradani E, Shimizu S (2009) Single cell oil production by Mortierella alpina. J Biotechnol 114:31–36

    Google Scholar 

  • Sarris D, Papanikolaou S (2016) Biotechnological production of ethanol: biochemistry, processes and technologies. Eng Life Sci 16:307–329

    CAS  Google Scholar 

  • Sayegh F, Elazzazy A, Bellou S, Moustogianni A, Elkady AI, Baeshen MN, Aggelis G (2016) Production of polyunsaturated single cell oils possessing antimicrobial and anticancer properties. Ann Microbiol 66:937–948

    CAS  Google Scholar 

  • Saygün A, Şahin-Yeşilçubuk N, Aran N (2014) Effects of different oil sources and residues on biomass and metabolite production by Yarrowia lipolytica YB 423–12. J Am Oil Chem Soc 91:1521–1530

    Google Scholar 

  • Szczęsna-Antczak M, Kubiak A, Antczak T, Bielecki S (2006a) Enzymatic biodiesel synthesis—key factors affecting efficiency of the process. Renew Energy 34:1185–1194

    Google Scholar 

  • Szczęsna-Antczak M, Antczak T, Piotrowicz-Wasiak M, Rzyska M, Binkowska N, Bielecki S (2006b) Relationships between lipases and lipids in mycelia of two Mucor strains. Enzyme Microb Technol 39:1214–1222

    Google Scholar 

  • Szczęsna-Antczak M, Struszczyk-Świta K, Rzyska M, Szeląg J, Stańczyk Ł, Antczak T (2018) Oil accumulation and in situ trans/esterification by lipolytic fungal biomass. Bioresour Technol 265:110–118

    PubMed  Google Scholar 

  • Tai M, Stephanopoulos G (2013) Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab Eng 15:1–9

    CAS  PubMed  Google Scholar 

  • Takeda I, Tamano K, Yamane N, Ishii T, Miura A, Umemura M, Terai G, Baker SE, Koike H, Machida M (2014) Genome sequence of the Mucoromycotina fungus Umbelopsis isabellina, an effective producer of lipids. Genome Announc 2:e00071–e00014

    PubMed  PubMed Central  Google Scholar 

  • Tatsumi C, Hashimoto Y, Terashima M, Matsuo T (1977) Method for producing cacao butter substitute. US Patent 4,032,405

  • Tauk-Tornisielo SM, Arasato LS, de Almeida AF, Govone JS, Malagutti EN (2009) Lipid formation and γ-linolenic acid production by Mucor circinelloides and Rhizopus sp., grown on vegetable oil. Braz J Microbiol 40:342–345

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tchakouteu S, 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 

  • Tzirita M, Papanikolaou S, Chatzifragkou A, Quilty B (2018) Waste fat biodegradation and biomodification by Yarrowia lipolytica and a bacterial consortium composed of Bacillus spp. and Pseudomonas putida. Eng Life Sci 18:932–942

    CAS  Google Scholar 

  • Vamvakaki AN, Kandarakis I, Kaminarides S, Komaitis M, Papanikolaou S (2010) Cheese whey as a renewable substrate for microbial lipid and biomass production by zygomycetes. Eng Life Sci 10:348–360

    CAS  Google Scholar 

  • Vasiliadou IA, Bellou S, Daskalaki A, Tomaszewska-Hetman L, Chatzikotoula C, Kompoti B, Papanikolaou S, Vayenas D, Pavlou S, Aggelis G (2018) Biomodification of fats and oils and scenarios of adding value on renewable fatty materials through microbial fermentations: modelling and trials with Yarrowia lipolytica. J Clean Prod 200:1111–1129

    CAS  Google Scholar 

  • Wagner L, Stielow B, Hoffmann K, Petkovits T, Papp T, Vágvölgyi C, de Hoog GS, Verkley G, Voigt K (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia 30:77–93

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weber RWS, Tribe HT (2003) Oil as a substrate for Mortierella species. Mycologist 17:134–139

    Google Scholar 

  • Woodbine M (1959) Microbial fat: microorganisms as potential fat producers. Prog Ind Microbiol 1:181–238

    Google Scholar 

  • Wynn JP, Ratledge C (2005) Microbial production of oils and fats. In: Shetty K, Paliyath G, Pometto A, Levin RE (eds) Food Biotechnology, 2nd edn. CRC Press, Boca Raton FL, pp 443–472

    Google Scholar 

  • Xing D, Wang H, Pan A, Wang J, Xue D (2012) Assimilation of corn fiber hydrolysates and lipid accumulation by Mortierella isabellina. Biomass Bioenergy 39:494–501

    CAS  Google Scholar 

  • Xiong D, Zhang H, Xie Y, Tang N, Berenjian A, Song Y (2015) Conversion of mutton fat to cocoa butter equivalent by increasing the unsaturated fatty acids at the sn-2 position of triacylglycerol through fermentation by Yarrowia lipolytica. Am J Biochem Biotechnol 11:57–65

    CAS  Google Scholar 

  • Zhang F, Ouellet M, Batth TS, Adams PD, Petzold CJ, Mukhopadhyay A, Keasling JD (2012) Enhancing fatty acid production by the expression of the regulatory transcription factor FadR. Metab Eng 14:653–660

    CAS  PubMed  Google Scholar 

  • Zhang S, Ito M, Skerker JM, Arkin AP, Rao CV (2016a) Metabolic engineering of the oleaginous yeast Rhodosporidium toruloides IFO0880 for lipid overproduction during high-density fermentation. Appl Microbiol Biotechnol 100:9393–9405

    CAS  PubMed  Google Scholar 

  • Zhang S, Skerker JM, Rutter CD, Maurer MJ, Arkin AP, Rao CV (2016b) Engineering Rhodosporidium toruloides for increased lipid production. Biotechnol Bioeng 113:1056–1066

    CAS  PubMed  Google Scholar 

  • Zhao C, Deng L, Fang H, Chen S (2017) Microbial oil production by Mortierella isabellina from corn stover under different pretreatments. RSC Adv 7:56239–56246

    CAS  Google Scholar 

  • Zhao C, Xie B, Zhao R, Fang H (2019) Microbial oil production by Mortierella isabellina from sodium hydroxide pretreated rice straw degraded by three-stage enzymatic hydrolysis in the context of on-site cellulase production. Renew Energy 130:281–289

    CAS  Google Scholar 

  • Zhong JJ, Tang YJ (2004) Submerged cultivation of medicinal mushrooms for production of valuable bioactive metabolites. Adv Biochem Eng Biotechnol 87:25–59

    CAS  PubMed  Google Scholar 

  • Zikou E, Chatzifragkou A, Koutinas AA, Papanikolaou S (2013) Evaluating glucose and xylose as cosubstrates for lipid accumulation and γ-linolenic acid biosynthesis of Thamnidium elegans. J Appl Microbiol 114:1020–1032

    CAS  PubMed  Google Scholar 

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Papanikolaou, S., Aggelis, G. Sources of microbial oils with emphasis to Mortierella (Umbelopsis) isabellina fungus. World J Microbiol Biotechnol 35, 63 (2019). https://doi.org/10.1007/s11274-019-2631-z

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