Skip to main content
SpringerLink
Log in

Eighteen new oleaginous yeast species

  • Bioenergy/Biofuels/Biochemicals
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Of 1600 known species of yeasts, about 70 are known to be oleaginous, defined as being able to accumulate over 20 % intracellular lipids. These yeasts have value for fundamental and applied research. A survey of yeasts from the Phaff Yeast Culture Collection, University of California Davis was performed to identify additional oleaginous species within the Basidiomycota phylum. Fifty-nine strains belonging to 34 species were grown in lipid inducing media, and total cell mass, lipid yield and triacylglycerol profiles were determined. Thirty-two species accumulated at least 20 % lipid and 25 species accumulated over 40 % lipid by dry weight. Eighteen of these species were not previously reported to be oleaginous. Triacylglycerol profiles were suitable for biodiesel production. These results greatly expand the number of known oleaginous yeast species, and reveal the wealth of natural diversity of triacylglycerol profiles within wild-type oleaginous Basidiomycetes.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Aggelis G, Komaitis M (1999) Enhancement of single cell oil production by Yarrowia lipolytica growing in the presence of Teucrium polium L. aqueous extract. Biotechnol Lett 21:747–749

    Article  CAS  Google Scholar 

  3. Alper H, Stephanopoulos G (2009) Engineering for biofuels: exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Microbiol 7:715–723

    Article  CAS  PubMed  Google Scholar 

  4. Antoni D, Zverlov VV, Schwarz WH (2007) Biofuels from microbes. Appl Microbiol Biotechnol 77:23–35

    Article  CAS  PubMed  Google Scholar 

  5. Aono R (1990) Taxonomic distribution of alkali-tolerant yeasts. Syst Appl Microbiol 13:394–397

    Article  Google Scholar 

  6. Baffi MA, Tobal T, Henrique J, Lago G, Leite RS, Boscolo M, Gomes E, Da-Silva R (2011) A novel β-glucosidase from Sporidiobolus pararoseus: characterization and application in winemaking. J Food Sci 76:C997–C1002

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bickel P, Tansey J, Welte M (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta (BBA) Mol Cell Biol Lipids 179:419–440

    Article  Google Scholar 

  9. Boundy-Mills K (2008) The phaff yeast culture collection has found its niche. Soc Ind Microbiol News 58:49–56

    Google Scholar 

  10. Brennan L, Owende P (2010) Biofuels from microlagae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14:557–577

    Article  CAS  Google Scholar 

  11. Cardenas F, De Castro M, Sanchez-Montero J, Sinisterra J, Valmaseda M, Elson S, Alvarez E (2001) Novel microbial lipases: catalytic activity in reactions in organic media. Enzyme Microbial Technol 28:145–154

    Article  CAS  Google Scholar 

  12. Chen Y, Daviet L, Schalk M, Siewers V, Nielsen J (2013) Establishing a platform cell factory through engineering of yeast acetyl-CoA metabolism. Metab Eng 15:48–54

    Article  CAS  PubMed  Google Scholar 

  13. Choi J-H, Ryu Y-W, Seo J-H (2005) Biotechnological production and applications of coenzyme Q10. Appl Microbiol Biotechnol 68:9–15

    Article  CAS  PubMed  Google Scholar 

  14. Cohen Z, Ratledge C (2005) Single Cell Oils. AOCS Press, Champaign

    Google Scholar 

  15. Davis RW, Fishman D, Frank E, Wigmosta M (2012) Renewable diesel from algal lipids: an integrated baseline for cost, emissions, and resource potential from a harmonized model. Technical report ANL.ESD/12-4, NREL/TP-5100-55431, PNNL-21437. US Department of Energy Biomass Program

  16. Garay L, Boundy-Mills K, German J (2014) Accumulation of high value lipids in single cell microorganisms: a mechanistic approach and future perspectives. J Agric Food Chem 62:2709–2727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Golomb BL, Morales V, Jung A, Yau B, Boundy-Mills KL, Marco ML (2013) Effects of pectinolytic yeast on the microbial composition and spoilage of olive fermentations. Food Microbiol 33:97–106

    Article  CAS  PubMed  Google Scholar 

  18. Guamán-Burneo C, Carvajal-Barriga J (2009) Caracterización e identificación de aislados de levaduras carotenogénicas de varias zonas naturales del Ecuador. Univ Sci 14:187–197

    Article  Google Scholar 

  19. Hamby KA, Hernández A, Boundy-Mills K, Zalom FG (2012) Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl Environ Microbiol 78:4869–4873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hanna M, Isom L, Campbell J (2005) Biodiesel: current perspectives and future. J Sci Ind Res 64:854

    CAS  Google Scholar 

  21. Huang R, Che H, Zhang J, Yang L, Jiang D, Li G (2012) Evaluation of Sporidiobolus pararoseus strain YCXT3 as biocontrol agent of Botrytis cinerea on post-harvest strawberry fruits. Biol Control 62:53–63

    Article  Google Scholar 

  22. Jacob Z (1993) Yeast lipid biotechnology. Adv Appl Microbiol 39:185

    Article  CAS  PubMed  Google Scholar 

  23. Janderova B, Gášková D, Bendova O (1995) Consequences of Sporidiobolus pararoseus killer toxin action on sensitive cells. Folia Microbiol 40:165–167

    Article  CAS  Google Scholar 

  24. Katre G, Joshi C, Khot M, Zinjarde S, RaviKumar A (2012) Evaluation of single cell oil (SCO) from a tropical marine yeast Yarrowia lipolytica NCIM 3589 as a potential feedstock for biodiesel. AMB Express 2:1–14

    Article  Google Scholar 

  25. Kim JY (2009) Isolation of Sporidiobolus ruineniae CO-3 and characterization of its extracellular protease. J Korean Soc Appl Biol Chem 52:1–10

    Article  CAS  Google Scholar 

  26. Kind T, Liu K-H, Lee DY, DeFelice B, Meissen JK, Fiehn O (2013) LipidBlast in silico tandem mass spectrometry database for lipid identification. Nat Methods 10:755–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Knothe G (2008) “Designer” biodiesel: optimizing fatty ester composition to improve fuel properties. Energy Fuels 22:1358–1364

    Article  CAS  Google Scholar 

  29. Kosa M, Ragauskas AJ (2011) Lipids from heterotrophic microbes: advances in metabolism research. Trends Biotechnol 29:53–61

    Article  CAS  PubMed  Google Scholar 

  30. Kumar S, Kushwaha H, Kumar Bachhawat A, Singh Raghava G, Ganesan K (2012) Genome sequence of the oleaginous red yeast Rhodosporidium toruloides MTCC 457. Eukaryot Cell 11:1083–1084

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kurtzman C, Fell J, Boekhout T (2011) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam

    Google Scholar 

  32. Liu H, Zhao X, Wang F, Li Y, Jiang X, Ye M, Zhao ZK, Zou H (2009) Comparative proteomic analysis of Rhodosporidium toruloides during lipid accumulation. Yeast 26:553–566. doi:10.1002/yea.1706

    Article  PubMed  Google Scholar 

  33. Liu H, Zhao X, Wang F, Jiang X, Zhang S, Ye M, Zhao Z, Zou H (2011) The proteome analysis of oleaginous yeast Lipomyces starkeyi. FEMS Yeast Res 11:42–51. doi:10.1111/j.1567-1364.2010.00687.x

    Article  PubMed  Google Scholar 

  34. Liu L, Redden H, Alper HS (2013) Frontiers of yeast metabolic engineering: diversifying beyond ethanol and Saccharomyces. Curr Opin Biotechnol 24:1023–1030

    Article  CAS  PubMed  Google Scholar 

  35. Liu Y, Koh CMJ, Sun L, Hlaing MM, Du M, Peng N, Ji L (2013) Characterization of glyceraldehyde-3-phosphate dehydrogenase gene RtGPD1 and development of genetic transformation method by dominant selection in oleaginous yeast Rhodosporidium toruloides. Appl Microbiol Biotechnol 97:719–729

    Article  CAS  PubMed  Google Scholar 

  36. Lundin H (1950) Fat synthesis by micro-organisms and its possible applications in industry. J Inst Brew 56:17–28

    Article  CAS  Google Scholar 

  37. Maharajh D, Roth R, Lalloo R, Simpson C, Mitra R, Görgens J, Ramchuran S (2008) Multi-copy expression and fed-batch production of Rhodotorula araucariae epoxide hydrolase in Yarrowia lipolytica. Appl Microbiol Biotechnol 79:235–244

    Article  CAS  PubMed  Google Scholar 

  38. McCluskey K, Bates S, Boundy-Mills K, Broggiato A, Cova A, Desmeth P, DebRoy C, Fravel D, Garrity G, del Mar Jiménez Gasco M, Joseph L, Lindner D, Lomas M, Morton J, Nobles D, Turner J, Ward T, Wertz J, Wiest A, Geiser D (2014) Meeting report: 2nd workshop of the united states culture collection network. May 19–21, 2014, State College, PA, USA. Stand Genom Sci 9:27–31

    Google Scholar 

  39. McCluskey K, Wiest A, Boundy-Mills K (2014) Chapter 4: Genome data drives change at culture collections. In: Newrousian M (ed) Fungal genomics. Springer, Berlin, pp 81-96

    Chapter  Google Scholar 

  40. Moreton RS (1988) Physiology of lipid accumulating yeasts. In: Moreton RS (ed) Single Cell Oil. Longman, Harlow, UK, pp 1–32

    Google Scholar 

  41. Paddon CJ, Keasling JD (2014) Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Microbiol 12:355–367

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  43. Patel A, Pravez M, Deeba F, Pruthi V, Singh RP, Pruthi PA (2014) Boosting accumulation of neutral lipids in Rhodosporidium kratochvilovae HIMPA1 grown on hemp (Cannabis sativa Linn) seed aqueous extract as feedstock for biodiesel production. Bioresour Technol 165:214–222

    Article  CAS  PubMed  Google Scholar 

  44. Pereyra V, Martinez A, Rufo C, Vero S (2014) Oleaginous yeasts form Uruguay and Antarctica as renewable raw material for biodiesel production. Am J of Biosci 2:251–257

    Article  Google Scholar 

  45. Pfaller R, Leonhartsberger S (2004) Process for producing Sporidiobolus ruineniae strains with improved coenzyme Q10 production. Google Patents

  46. Qi F, Kitahara Y, Wang Z, Zhao X, Du W, Liu D (2013) Novel mutant strains of Rhodosporidium toruloides by plasma mutagenesis approach and their tolerance for inhibitors in lignocellulosic hydrolyzate. J Chem Technol Biotechnol 89:735–742

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  48. Ratledge C (1988) Yeasts for lipid production. Biochem Soc Trans 16:1088

    Article  CAS  PubMed  Google Scholar 

  49. Ratledge C (1993) Single cell oils—have they a biotechnological future? Trends Biotechnol 11:278–284

    Article  CAS  PubMed  Google Scholar 

  50. Ratledge C (2002) Regulation of lipid accumulation in oleaginous micro-organisms. Biochem Soc Trans 30:1047–1050

    Article  CAS  PubMed  Google Scholar 

  51. Ratledge C, Wilkinson SG (1988) Microbial lipids, vol 1. Academic Press, London

    Google Scholar 

  52. Rattray J, Scheibeci A, Kidby D (1975) Lipids of yeasts. Bacteriol Rev 39:197–231

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Schulze I, Hansen S, Großhans S, Rudszuck T, Ochsenreither K, Syldatk C, Neumann A (2014) Characterization of newly isolated oleaginous yeasts—Cryptococcus podzolicus, Trichosporon porosum and Pichia segobiensis. AMB Express 4:1–11

    Article  Google Scholar 

  54. Schweizer M (2004) Lipids and membranes. The metabolism and molecular physiology of Saccharomyces cerevisiae. CRC Press, London, pp 140–223

    Google Scholar 

  55. Sitepu I, Ignatia L, Franz A, Wong D, Faulina S, Tsui M, Kanti A, Boundy-Mills K (2012) An improved high-throughput Nile red fluorescence assay for estimating intracellular lipids in a variety of yeast species. J Microbiol Methods 91:321–328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sitepu IR, Sestric R, Ignatia L, Levin D, Bruce German J, Gillies LA, Almada 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 yeasts species. Bioresour Technol 144:360–369

    Article  CAS  PubMed  Google Scholar 

  57. Sitepu I, Garay L, Sestric R, Levin D, Block DE, German J, Boundy-Mills K (2014) Oleaginous yeasts for biodiesel: current and future trends in biology and production. J Biotechnol Adv 32:1336–1360. doi:10.1016/j.biotechadv.2014.08.003

    Article  CAS  Google Scholar 

  58. Sitepu I, Jin M, Fernandez J, Sousa L, Balan V, Boundy-Mills K (2014) Identification of oleaginous yeast strains able to accumulate high intracellular lipids when cultivated in alkaline pretreated corn stover. Appl Microbiol Biotechnol 98:7645–7657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Sitepu I, Selby T, Zhu S, Lin T, Boundy-Mills K (2014) Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species. J Ind Microbiol Biotechnol 41:1061–1070. doi:10.1007/s10295-014-1447-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sitepu I, Shi S, Simmons BA, Singer S, Boundy-Mills K, Simmons C (2014) Yeast tolerance to the ionic liquid 1-ethyl-3-methylimidazolium acetate. FEMS Yeast Res 14:1286–1294

    Article  CAS  PubMed  Google Scholar 

  61. Steen E, Kang Y, Bokinsky G, Hu Z, Schirmer A, McClure A, del Cardayre S, Keasling J (2010) Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463:559–562

    Article  CAS  PubMed  Google Scholar 

  62. Sugiyama J, Fukagawa M, Chiu S-W, Komagata K (1985) Cellular carbohydrate composition, DNA base composition, ubiquinone systems, and Diazonium Blue B color test in the genera Rhodosporidium, Leucosporidium, Rhodotorula and related basidiomycetous yeasts. J Gen Appl Microbiol 31:519–550

    Article  CAS  Google Scholar 

  63. Suutari M, Priha P, Laakso S (1993) Temperature shifts in regulation of lipids accumulated by Lipomyces starkeyi. J Am Oil Chem Soc 70:891–894

    Article  CAS  Google Scholar 

  64. Turcotte G, Kosaric N (1988) Biosynthesis of lipids by Rhodosporidium toruloides ATCC 10788. J Biotechnol 8:221–237

    Article  CAS  Google Scholar 

  65. Valduga E, Ribeiro AHR, Cence K, Colet R, Tiggemann L, Zeni J, Toniazzo G (2014) Carotenoids production from a newly isolated Sporidiobolus pararoseus strain using agroindustrial substrates. Biocatal Agric Biotechnol 3:207–213

    Google Scholar 

  66. Wang C, Leger R (2007) The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J Biol Chem 282:21110–21115

    Article  CAS  PubMed  Google Scholar 

  67. Woodbine M (1959) Microbial fat: micro-organisms as potential fat producers. In: Hockenhull (ed) Progress in Industrial Microbiology, vol 1. Elsevier, London, UK, pp 181–245

  68. Zhao X, Kong X, Hua Y, Feng N, Zhao Z (2008) Medium optimization for lipid production through co-fermentation of glucose and xylose by the oleaginous yeast Lipomyces starkeyi. Eur J Lipid Sci Technol 110:405–412

    Article  CAS  Google Scholar 

  69. Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Erin Cathcart, Jennifer Lincoln, Lauren Enriquez for technical assistance. This research was funded by Grant Number U01TW008160 from the NIH Fogarty International Center, the NIH Office of Dietary Supplements, the National Science Foundation and the Department of Energy. This project was supported by the USDA Agricultural Food Research Initiative of the National Food and Agriculture, USDA, Grant Number 35621-04750. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Fogarty International Center or the National Institutes of Health, the Office of Dietary Supplements, the National Science Foundation, the Department of Energy, or the Department of Agriculture. This work was supported by the Science Translation and Innovation Research (STAIR) Grant Program of the University of California Davis, and by the Consejo Nacional de Ciencia y Tecnología (CONACYT) Grant Number 291795. Funding by NIH HL113452 and NIH DK097154 (to OF) is greatly appreciated. NIH instrument funding by NIH S10-RR031630 (to OF) is acknowledged. Strains UCDFST 10-421, 10-451, 12-776, 10-1058, 10-1109, 10-453, 11-470 and 10-441 were obtained through a collaboration between UC Davis and the Government of the Republic of Indonesia.Thanks to Sarah Faulina and Sira Silaban for isolating strain Rhodotorula mucilaginosa UCDFST 13-478. All authors have agreed to submit this manuscript to the “Journal of Industrial Microbiology and Biotechnology”.

Author information

Author notes

    Authors and Affiliations

    1. Phaff Yeast Culture Collection, Department of Food Science and Technology, University of California, One Shields Ave, Davis, CA, 95616-8598, USA

      Luis A. Garay, Irnayuli R. Sitepu, Idelia Chandra, Sandy Shi, Ting Lin & Kyria L. Boundy-Mills

    2. Bioentrepreneurship Department, Indonesia International Institute for Life Sciences, Jalan Pulo Mas Barat Kav. 88, East Jakarta, DKI Jakarta, 13210, Indonesia

      Irnayuli R. Sitepu

    3. Metabolomics, UC Davis Genome Center, University of California Davis, 451 Health Sciences Drive, Davis, CA, 95616, USA

      Tomas Cajka & Oliver Fiehn

    4. Department of Food Science and Technology, University of California, One Shields Ave, Davis, CA, 95616, USA

      J. Bruce German

    5. Biochemistry Department, Faculty of Science, King Abdulaziz University, PO Box 80203, Jeddah, 21589, Saudi Arabia

      Oliver Fiehn

    Authors
    1. Luis A. Garay
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Irnayuli R. Sitepu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Tomas Cajka
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Idelia Chandra
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Sandy Shi
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Ting Lin
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. J. Bruce German
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Oliver Fiehn
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Kyria L. Boundy-Mills
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Kyria L. Boundy-Mills.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    L. A. Garay, I. R. Sitepu and T. Cajka contributed equally to the realization of the manuscript and are co-first authors.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (PDF 90 kb)

    Supplementary material 2 (PDF 204 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Garay, L.A., Sitepu, I.R., Cajka, T. et al. Eighteen new oleaginous yeast species. J Ind Microbiol Biotechnol 43, 887–900 (2016). https://doi.org/10.1007/s10295-016-1765-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10295-016-1765-3

    Keywords

    Search

    Navigation