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

  • Seraphim PapanikolaouEmail author
  • George Aggelis


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.


Mortierella isabellina Zygomycetes Single cell oil 


Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.


  1. Aggelis G (1996) Two alternative pathways for substrate assimilation by Mucor circinelloides. Folia Microbiol 41:254–256CrossRefGoogle Scholar
  2. 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 43:311–317Google Scholar
  3. 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 46:169–173CrossRefGoogle Scholar
  4. 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 46:245–250CrossRefGoogle Scholar
  5. Aggelis G, Papadiotis G, Komaitis M (1997) Microbial fatty acid specificity. Folia Microbiol 42:117–120CrossRefGoogle Scholar
  6. 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 15:243–253CrossRefGoogle Scholar
  7. 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 66:2632–2638PubMedCrossRefPubMedCentralGoogle Scholar
  8. 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 124:336–367PubMedCrossRefPubMedCentralGoogle Scholar
  9. 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 237–266CrossRefGoogle Scholar
  10. Bati N, Hammond EG, Glatz BA (1984) Biomodification of fats and oils: trials with Candida lipolytica. J Am Oil Chem Soc 61:1743–1746CrossRefGoogle Scholar
  11. 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 164:318–329PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bellou S, Moustogianni A, Makri A, Aggelis G (2012) Lipids containing polyunsaturated fatty acids synthesized by zygomycetes grown on glycerol. Appl Biochem Biotechnol 166:146–158PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493PubMedCrossRefPubMedCentralGoogle Scholar
  14. 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 37:24–35PubMedCrossRefPubMedCentralGoogle Scholar
  15. 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 74:7779–7789PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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 93:1523–1537PubMedCrossRefPubMedCentralGoogle Scholar
  17. 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 5:3131PubMedCrossRefPubMedCentralGoogle Scholar
  18. Cai G, Moghaddam L, O’Hara IM, Zhang Z (2019) Microbial oil production from acidified glycerol pretreated sugarcane bagasse by Mortierella isabellina. RSC Adv 9:2539–2550CrossRefGoogle Scholar
  19. 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 38:1230–1243PubMedCrossRefPubMedCentralGoogle Scholar
  20. Čertik M, Shimizu S (1999) Biosynthesis and regulation of microbial polyunsaturated fatty acid production. J Biosci Bioeng 87:1–14PubMedCrossRefPubMedCentralGoogle Scholar
  21. Čertik M, Balteszova L, Sajbidor J (1997) Lipid formation and γ-linolenic acid production by Mucorales fungi grown on sunflower oil. Lett Appl Microbiol 25:101–105CrossRefGoogle Scholar
  22. 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 112:1048–1057CrossRefGoogle Scholar
  23. Dahiya JS (1991) Xylitol production by Petromyces albertensis grown on medium containing D-xylose. Can J Microbiol 37:14–18CrossRefGoogle Scholar
  24. 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 21:1037–1044PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 99–146Google Scholar
  26. Davies RJ, Holdsworth JE (1992) Synthesis of lipids in yeasts: biochemistry, physiology and production. Adv Appl Lipid Res 1:119–159Google Scholar
  27. Davies JL, Wobeser GA (2010) Systemic infection with Mortierella wolfii following abortion in a cow. Can Vet J 51:1391–1393PubMedPubMedCentralGoogle Scholar
  28. Dellomonaco C, Clomburg JM, Miller EN, Gonzalez R (2011) Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 476:355–359PubMedCrossRefPubMedCentralGoogle Scholar
  29. Demir M, Turhan I, Kucukcetin A, Alpkent Z (2013) Oil production by Mortierella isabellina from whey treated with lactase. Bioresour Technol 128:365–369PubMedCrossRefPubMedCentralGoogle Scholar
  30. 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 167:1890–1906PubMedCrossRefGoogle Scholar
  31. 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 37:1385–1400PubMedCrossRefGoogle Scholar
  32. Diamantopoulou P, Papanikolaou S, Aggelis G, Philippoussis A (2016) Adaptation of Volvariella volvacea metabolism in high carbon to nitrogen ratio media. Food Chem 196:272–280PubMedCrossRefGoogle Scholar
  33. Diwan B, Parkhey P, Gupta P (2018) From agro-industrial wastes to single cell oils: a step towards prospective biorefinery. Folia Microbiol 63:547–568CrossRefGoogle Scholar
  34. Dourou M, Mizerakis P, Papanikolaou S, Aggelis G (2017) Storage lipid and polysaccharide metabolism in Yarrowia lipolytica and Umbelopsis isabellina. Appl Microbiol Biotechnol 101:7213–7226PubMedCrossRefGoogle Scholar
  35. 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 102:2509–2523PubMedCrossRefGoogle Scholar
  36. 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 13:482–491PubMedCrossRefGoogle Scholar
  37. 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 1831:1486–1495PubMedCrossRefPubMedCentralGoogle Scholar
  38. Dyal SD, Narine SS (2005) Implications for the use of Mortierella fungi in the industrial production of essential fatty acids. Food Res Int 38:445–467CrossRefGoogle Scholar
  39. Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011a) Modelling of single-cell oil production under nitrogen limited and substrate inhibition conditions. Biotechnol Bioeng 108:1049–1055PubMedCrossRefPubMedCentralGoogle Scholar
  40. Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011b) Single cell oil production from rice hulls hydrolysate. Bioresour Technol 102:9737–9742PubMedCrossRefGoogle Scholar
  41. 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 33:573–580CrossRefGoogle Scholar
  42. 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 216:988–995PubMedCrossRefGoogle Scholar
  43. 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 5:527–543PubMedCrossRefGoogle Scholar
  44. Gao D, Zeng J, Yu X, Dong T, Chen S (2014) Improved lipid accumulation by morphology engineering of oleaginous fungus Mortierella isabellina. Biotechnol Bioeng 111:1758–1766PubMedCrossRefGoogle Scholar
  45. 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 123:1461–1477PubMedCrossRefGoogle Scholar
  46. Harde SM, Wang Z, Horne M, Zhu JY, Pan X (2016) Microbial lipid production from SPORL-pretreated Douglas fir by Mortierella isabellina. Fuel 175:64–74CrossRefGoogle Scholar
  47. 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 31:129–139PubMedCrossRefGoogle Scholar
  48. 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 16:333–339CrossRefGoogle Scholar
  49. 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 73:431–435CrossRefGoogle Scholar
  50. 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 13:212–216CrossRefGoogle Scholar
  51. Knothe G (2005) Dependence of biodiesel fuel properties on the structure of fatty acid alkyl esters. Fuel Process Technol 86:1059–1070CrossRefGoogle Scholar
  52. Koritala S, Hesseltine CW, Pryde EH, Mounts TL (1987) Biochemical modification of fats by microorganisms: a preliminary study. J Am Oil Chem Soc 64:509–513CrossRefGoogle Scholar
  53. 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 116:566–577CrossRefGoogle Scholar
  54. 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 43:2587–2627PubMedCrossRefGoogle Scholar
  55. 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 5:4105–4111Google Scholar
  56. 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 28:54–62PubMedCrossRefGoogle Scholar
  57. Matsuo T, Terashima M, Hashimoto Y, Hasida W (1981) Method for producing cacao butter substitute. US Patent 4,308,350Google Scholar
  58. 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 34:939–949PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 34:951–961PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 35:591–603PubMedCrossRefPubMedCentralGoogle Scholar
  61. Meeuwse P, Sanders JPM, Tramper J, Rinzema A (2013) Lipids from yeasts and fungi: tomorrow’s source of biodiesel? Biofuel Bioprod Biorefin 7:512–524CrossRefGoogle Scholar
  62. Metzger JO, Bornscheuer U (2006) Lipids as renewable resources: current state of chemical and biotechnological conversion and diversification. Appl Microbiol Biotechnol 71:13–22PubMedCrossRefPubMedCentralGoogle Scholar
  63. 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 65:317–324PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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 28:81–85CrossRefGoogle Scholar
  65. Moser BR (2009) Biodiesel production, properties, and feedstocks. In Vitro Cell Develop Biol Plant 45:229–266CrossRefGoogle Scholar
  66. 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 21:83–87CrossRefGoogle Scholar
  67. Papanikolaou S, Aggelis G (2010) Yarrowia lipolytica: a model microorganism used for the production of tailor-made lipids. Eur J Lipid Sci Technol 112:639–654CrossRefGoogle Scholar
  68. Papanikolaou S, Aggelis G (2011a) Lipids of oleaginous yeasts. Part I: biochemistry of single cell oil production. Eur J Lipid Sci Technol 113:1031–1051CrossRefGoogle Scholar
  69. Papanikolaou S, Aggelis G (2011b) Lipids of oleaginous yeasts. Part II: technology and potential applications. Eur J Lipid Sci Technol 113:1052–1073CrossRefGoogle Scholar
  70. 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 80:215–224PubMedCrossRefPubMedCentralGoogle Scholar
  71. 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 58:308–312PubMedCrossRefPubMedCentralGoogle Scholar
  72. 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 46:124–130PubMedCrossRefPubMedCentralGoogle Scholar
  73. 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 97:867–875PubMedCrossRefPubMedCentralGoogle Scholar
  74. Papanikolaou S, Komaitis M, Aggelis G (2004b) Single cell oil (SCO) production by Mortierella isabellina grown on high-sugar content media. Bioresour Technol 95:287–291PubMedCrossRefPubMedCentralGoogle Scholar
  75. 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 52:134–142PubMedCrossRefPubMedCentralGoogle Scholar
  76. 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 10:425–435CrossRefGoogle Scholar
  77. 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 109:1060–1070CrossRefGoogle Scholar
  78. 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 32:60–71CrossRefGoogle Scholar
  79. 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 110:1138–1150PubMedCrossRefPubMedCentralGoogle Scholar
  80. 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 168:303–314PubMedCrossRefPubMedCentralGoogle Scholar
  81. 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 17:262–281CrossRefGoogle Scholar
  82. 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 62:836–855CrossRefGoogle Scholar
  83. 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 77:604–616CrossRefGoogle Scholar
  84. 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 161–184Google Scholar
  85. 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 29:56–65PubMedCrossRefPubMedCentralGoogle Scholar
  86. 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 35:173–177PubMedCrossRefPubMedCentralGoogle Scholar
  87. Qin L, Liu L, Zeng AP, Wei D (2017) From low-cost substrates to single cell oils synthesized by oleaginous yeasts. Bioresour Technol 245:1507–1519PubMedCrossRefPubMedCentralGoogle Scholar
  88. Ratledge C (1987) Lipid biotechnology: a wonderland for the microbial physiologist. J Am Oil Chem Soc 64:1647–1656CrossRefGoogle Scholar
  89. Ratledge C (1988) Biochemistry, stoichiometry, substrates and economics. In: Moreton RS (ed) Single cell oil. Longman Scientific & Technical, Longman House, Burnt Mill, Harlow, pp 33–70Google Scholar
  90. 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 235–291CrossRefGoogle Scholar
  91. Ratledge C (2011) Are algal oils realistic options for biofuels? Eur J Lipid Sci Technol 113:135–136CrossRefGoogle Scholar
  92. Ratledge C (2013a) Microbial oils: an introductory overview of current status and future prospects. Oilseeds Fats Crops Lipids (OCL) 20:D602Google Scholar
  93. Ratledge C (2013b) Oils from microalgae: achievements and prospects Accessed 22 Mar 2017
  94. Ratledge C, Cohen Z (2008) Microbial and algal oils: do they have a future for biodiesel or as commodity oils? Lipid Technol 20:155–160CrossRefGoogle Scholar
  95. Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51PubMedCrossRefPubMedCentralGoogle Scholar
  96. 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 119:282–293PubMedPubMedCentralGoogle Scholar
  97. Roux-Van der Merwe MP, Badenhorst J, Britz TJ (2005) Fungal treatment of an edible-oil-containing industrial effluent. World J Microbiol Biotechnol 21:947–953CrossRefGoogle Scholar
  98. 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 110:198–205PubMedCrossRefPubMedCentralGoogle Scholar
  99. Ruan Z, Zanotti M, Zhong Y, Liao W, Ducey C, Liu Y (2013) Co-hydrolysis of lignocellulosic biomass for microbial lipid accumulation. Biotechnol Bioeng 110:1039–1049PubMedCrossRefPubMedCentralGoogle Scholar
  100. 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 163:12–17PubMedCrossRefPubMedCentralGoogle Scholar
  101. 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 183:18–24PubMedCrossRefPubMedCentralGoogle Scholar
  102. 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 48:148–166CrossRefGoogle Scholar
  103. Sakuradani E, Shimizu S (2009) Single cell oil production by Mortierella alpina. J Biotechnol 114:31–36CrossRefGoogle Scholar
  104. Sarris D, Papanikolaou S (2016) Biotechnological production of ethanol: biochemistry, processes and technologies. Eng Life Sci 16:307–329CrossRefGoogle Scholar
  105. 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 66:937–948CrossRefGoogle Scholar
  106. 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 91:1521–1530CrossRefGoogle Scholar
  107. Szczęsna-Antczak M, Kubiak A, Antczak T, Bielecki S (2006a) Enzymatic biodiesel synthesis—key factors affecting efficiency of the process. Renew Energy 34:1185–1194CrossRefGoogle Scholar
  108. 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 39:1214–1222CrossRefGoogle Scholar
  109. 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 265:110–118PubMedCrossRefPubMedCentralGoogle Scholar
  110. Tai M, Stephanopoulos G (2013) Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab Eng 15:1–9PubMedCrossRefPubMedCentralGoogle Scholar
  111. 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–e00014PubMedPubMedCentralCrossRefGoogle Scholar
  112. Tatsumi C, Hashimoto Y, Terashima M, Matsuo T (1977) Method for producing cacao butter substitute. US Patent 4,032,405Google Scholar
  113. 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 40:342–345PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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 117:657–672CrossRefGoogle Scholar
  115. 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 18:932–942CrossRefGoogle Scholar
  116. 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 10:348–360CrossRefGoogle Scholar
  117. 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 200:1111–1129CrossRefGoogle Scholar
  118. 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 30:77–93PubMedPubMedCentralCrossRefGoogle Scholar
  119. Weber RWS, Tribe HT (2003) Oil as a substrate for Mortierella species. Mycologist 17:134–139CrossRefGoogle Scholar
  120. Woodbine M (1959) Microbial fat: microorganisms as potential fat producers. Prog Ind Microbiol 1:181–238Google Scholar
  121. 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 443–472Google Scholar
  122. Xing D, Wang H, Pan A, Wang J, Xue D (2012) Assimilation of corn fiber hydrolysates and lipid accumulation by Mortierella isabellina. Biomass Bioenergy 39:494–501CrossRefGoogle Scholar
  123. 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 11:57–65CrossRefGoogle Scholar
  124. 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 14:653–660PubMedCrossRefPubMedCentralGoogle Scholar
  125. 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 100:9393–9405PubMedCrossRefPubMedCentralGoogle Scholar
  126. Zhang S, Skerker JM, Rutter CD, Maurer MJ, Arkin AP, Rao CV (2016b) Engineering Rhodosporidium toruloides for increased lipid production. Biotechnol Bioeng 113:1056–1066PubMedCrossRefPubMedCentralGoogle Scholar
  127. Zhao C, Deng L, Fang H, Chen S (2017) Microbial oil production by Mortierella isabellina from corn stover under different pretreatments. RSC Adv 7:56239–56246CrossRefGoogle Scholar
  128. 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 130:281–289CrossRefGoogle Scholar
  129. Zhong JJ, Tang YJ (2004) Submerged cultivation of medicinal mushrooms for production of valuable bioactive metabolites. Adv Biochem Eng Biotechnol 87:25–59PubMedPubMedCentralGoogle Scholar
  130. 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 114:1020–1032PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratory of Food Microbiology and Biotechnology, Department of Food Science and Human NutritionAgricultural University of AthensAthensGreece
  2. 2.Unit of Microbiology, Department of Biology, Division of Genetics, Cell Biology and DevelopmentUniversity of PatrasPatrasGreece

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