1887

Abstract

, an ascomycete with biotechnological potential, is able to form either yeast cells or hyphae and pseudohyphae in response to environmental conditions. This study shows that the morphology of , cultivated in batch cultures on hydrophilic (glucose and glycerol) and hydrophobic (olive oil) media, was not affected by the nature of the carbon source, nor by the nature or the concentration of the nitrogen source. By contrast, dissolved oxygen concentration (DOC) should be considered as the major factor affecting yeast morphology. Specifically, when growth occurred at low or zero DOC the mycelial and/or pseudomycelial forms predominated over the yeast form independently of the carbon and nitrogen sources used. Experimental data obtained from a continuous culture of on glycerol, being used as carbon and energy source, demonstrated that the mycelium-to-yeast form transition occurs when DOC increases from 0.1 to 1.5 mg l. DOC also affected the yeast physiology, as the activity of enzymes implicated in lipid biosynthesis (i.e. ATP-citrate lyase, malic enzyme) was upregulated at high DOC whereas the activity of enzymes implicated in glycerol assimilation (such as glycerol dehydrogenase and kinase) remained fundamentally unaffected in the cell-free extract.

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2014-04-01
2020-01-22
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References

  1. Aggelis G.. ( 1996;). Two alternative pathways for substrate assimilation by Mucor circinelloides . Folia Microbiol (Praha)41:254–256 [CrossRef]
    [Google Scholar]
  2. Bankar A. V., Kumar A. R., Zinjarde S. S.. ( 2009;). Environmental and industrial applications of Yarrowia lipolytica . Appl Microbiol Biotechnol84:847–865 [CrossRef][PubMed]
    [Google Scholar]
  3. Barth G., Gaillardin C.. ( 1997;). Physiology and genetics of the dimorphic fungus Yarrowia lipolytica . FEMS Microbiol Rev19:219–237 [CrossRef][PubMed]
    [Google Scholar]
  4. Bati N., Hammond E. G., Glatz B. A.. ( 1984;). Biomodification of fats and oils: trials with Candida lipolytica . J Am Oil Chem Soc61:1743–1746 [CrossRef]
    [Google Scholar]
  5. 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 Biotechnol164:318–329 [CrossRef][PubMed]
    [Google Scholar]
  6. Bellou S., Moustogianni A., Makri A., Aggelis G.. ( 2012;). Lipids containing polyunsaturated fatty acids synthesized by zygomycetes grown on glycerol. Appl Biochem Biotechnol166:146–158 [CrossRef][PubMed]
    [Google Scholar]
  7. Beopoulos A., Chardot T., Nicaud J. M.. ( 2009;). Yarrowia lipolytica: a model and a tool to understand the mechanisms implicated in lipid accumulation. Biochimie91:692–696 [CrossRef][PubMed]
    [Google Scholar]
  8. Bergmeyer H. U.. ( 1974;). Glycerol-3-phosphare dehydrogenase. Methods of Enzymatic Analysis468–469 Bergmeyer H. U.. New York: Academic Press;
    [Google Scholar]
  9. Bublitz C., Kennedy E. P.. ( 1954;). Synthesis of phosphatides in isolated mitochondria. III. The enzymatic phosphorylation of glycerol. J Biol Chem211:951–961[PubMed]
    [Google Scholar]
  10. Cervantes-Chávez J. A., Kronberg F., Passeron S., Ruiz-Herrera J.. ( 2009;). Regulatory role of the PKA pathway in dimorphism and mating in Yarrowia lipolytica . Fungal Genet Biol46:390–399 [CrossRef][PubMed]
    [Google Scholar]
  11. Choi S. Y., Ryu D. D., Rhee J. S.. ( 1982;). Production of microbial lipid: effects of growth rate and oxygen on lipid synthesis and fatty acid composition of Rhodotorula gracilis. Biotechnol Bioeng24:1165–1172[PubMed][CrossRef]
    [Google Scholar]
  12. Coelho M. A. Z., Amaral P. F. F., Belo I.. ( 2010;). Yarrowia lipolytica: an industrial workhorse. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology930–944 Méndez-Vilas A.. Badajoz: Formatex;
    [Google Scholar]
  13. Cruz J. M., Dominguez J. M., Dominguez H., Parajo J. C.. ( 2000;). Dimorphic behaviour of Debaryomyces hansenii grown on barley bran acid hydrolyzates. Biotechnol Lett22:605–610 [CrossRef]
    [Google Scholar]
  14. Domínguez A., Fermiñán E., Gaillardin C.. ( 2000;). Yarrowia lipolytica: an organism amenable to genetic manipulation as a model for analyzing dimorphism in fungi. Dimorphism in Human Pathogenic and Apathogenic Yeast151–172 Ernst J. F., Schmidt A.. Basel: Karger; [CrossRef]
    [Google Scholar]
  15. Dulermo T., Tréton B., Beopoulos A., Kabran Gnankon A. P., Haddouche R., Nicaud J. M.. ( 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 Acta1831:1486–1495 [CrossRef][PubMed]
    [Google Scholar]
  16. Fickers P., Benetti P. H., Waché Y., Marty A., Mauersberger S., Smit M. S., Nicaud J. M.. ( 2005;). Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res5:527–543 [CrossRef][PubMed]
    [Google Scholar]
  17. Flores C. L., Martínez-Costa O. H., Sánchez V., Gancedo C., Aragón J. J.. ( 2005;). The dimorphic yeast Yarrowia lipolytica possesses an atypical phosphofructokinase: characterization of the enzyme and its encoding gene. Microbiology151:1465–1474 [CrossRef][PubMed]
    [Google Scholar]
  18. Folch J., Lees M., Sloane Stanley G. H.. ( 1957;). A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem226:497–509[PubMed]
    [Google Scholar]
  19. Förster A., Aurich A., Mauersberger S., Barth G.. ( 2007;). Citric acid production from sucrose using a recombinant strain of the yeast Yarrowia lipolytica . Appl Microbiol Biotechnol75:1409–1417 [CrossRef][PubMed]
    [Google Scholar]
  20. Geer B. W., Krochko D., Oliver M. J., Walker V. K., Williamson J. H.. ( 1979;). A comparative study of the NADP-malic enzymes from Drosophila and chick liver. Comp Biochem Physiol65:25–34
    [Google Scholar]
  21. Gellissen G., Kunze G., Gaillardin C., Cregg J. M., Berardi E., Veenhuis M., van der Klei I.. ( 2005;). New yeast expression platforms based on methylotrophic Hansenula polymorpha and Pichia pastoris and on dimorphic Arxula adeninivorans and Yarrowia lipolytica – a comparison. FEMS Yeast Res5:1079–1096 [CrossRef][PubMed]
    [Google Scholar]
  22. Gomes N., Aguedo M., Teixeira J., Belo I.. ( 2007;). Oxygen mass transfer in a biphasic medium: influence on the biotransformation of methyl ricinoleate into γ-decalactone by the yeast Yarrowia lipolytica . Biochem Eng J35:380–386 [CrossRef]
    [Google Scholar]
  23. Guevara-Olvera L., Calvo-Mendez C., Ruiz-Herrera J.. ( 1993;). The role of polyamine metabolism in dimorphism of Yarrowia lipolytica . J Gen Microbiol139:485–493 [CrossRef][PubMed]
    [Google Scholar]
  24. Gutierrez J. R., Erickson L. E.. ( 1977;). Hydrocarbon uptake in hydrocarbon fermentations. Biotechnol Bioeng19:1331–1349 [CrossRef][PubMed]
    [Google Scholar]
  25. Hurtado C. A., Rachubinski R. A.. ( 1999;). MHY1 encodes a C2H2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica . J Bacteriol181:3051–3057[PubMed]
    [Google Scholar]
  26. Juszczyk P., Tomaszewska L., Kita A., Rymowicz W.. ( 2013;). Biomass production by novel strains of Yarrowia lipolytica using raw glycerol, derived from biodiesel production. Bioresour Technol137:124–131 [CrossRef][PubMed]
    [Google Scholar]
  27. Kamath R. S., Bungay H. R.. ( 1988;). Growth of yeast colonies on solid media. J Gen Microbiol134:3061–3069[PubMed]
    [Google Scholar]
  28. Kamzolova S. V., Morgunov I. G.. ( 2013;). α-Ketoglutaric acid production from rapeseed oil by Yarrowia lipolytica yeast. Appl Microbiol Biotechnol97:5517–5525 [CrossRef][PubMed]
    [Google Scholar]
  29. Kamzolova S. V., Shishkanova N. V., Morgunov I. G., Finogenova T. V.. ( 2003;). Oxygen requirements for growth and citric acid production of Yarrowia lipolytica . FEMS Yeast Res3:217–222 [CrossRef][PubMed]
    [Google Scholar]
  30. Kamzolova S. V., Fatykhova A. R., Dedyukhina E. G., Anastassiadis S. G., Golovchenko N. P., Morgunov I. G.. ( 2011;). Citric acid production by yeast grown on glycerol-containing waste from biodiesel industry. Food Technol Biotechnol49:65–74
    [Google Scholar]
  31. Kamzolova S. V., Chiglintseva M. N., Lunina J. N., Morgunov I. G.. ( 2012;). α-Ketoglutaric acid production by Yarrowia lipolytica and its regulation. Appl Microbiol Biotechnol96:783–791 [CrossRef][PubMed]
    [Google Scholar]
  32. Kamzolova S. V., Dedyukhina E. G., Samoilenko V. A., Lunina J. N., Puntus I. F., Allayarov R. L., Chiglintseva M. N., Mironov A. A., Morgunov I. G.. ( 2013;). Isocitric acid production from rapeseed oil by Yarrowia lipolytica yeast. Appl Microbiol Biotechnol97:9133–9144 [CrossRef][PubMed]
    [Google Scholar]
  33. Kawasse F. M., Amaral P. F., Rocha-Leão M. H. M., Amaral A. L., Ferreira E. C., Coelho M. A. Z.. ( 2003;). Morphological analysis of Yarrowia lipolytica under stress conditions through image processing. Bioprocess Biosyst Eng25:371–375 [CrossRef][PubMed]
    [Google Scholar]
  34. Kim J., Cheon S. A., Park S., Song Y., Kim J.-Y.. ( 2000;). Serum-induced hypha formation in the dimorphic yeast Yarrowia lipolytica . FEMS Microbiol Lett190:9–12 [CrossRef][PubMed]
    [Google Scholar]
  35. Kornberg A.. ( 1955;). Isocitrate dehydrogenase of yeast (TPN). Methods Enzymol1:705–709 [CrossRef]
    [Google Scholar]
  36. Madzak C., Gaillardin C., Beckerich J. M.. ( 2004;). Heterologous protein expression and secretion in the non-conventional yeast Yarrowia lipolytica: a review. J Biotechnol109:63–81 [CrossRef][PubMed]
    [Google Scholar]
  37. Makri A., Fakas S., Aggelis G.. ( 2010;). Metabolic activities of biotechnological interest in Yarrowia lipolytica grown on glycerol in repeated batch cultures. Bioresour Technol101:2351–2358 [CrossRef][PubMed]
    [Google Scholar]
  38. Martinez-Vazquez A., Gonzalez-Hernandez A., Domínguez A., Rachubinski R., Riquelme M., Cuellar-Mata P., Guzman J. C. T.. ( 2013;). Identification of the transcription factor Znc1p, which regulates the yeast-to-hypha transition in the dimorphic yeast Yarrowia lipolytica . PLoS ONE8:e66790 [CrossRef][PubMed]
    [Google Scholar]
  39. Morales-Vargas A. T., Domínguez A., Ruiz-Herrera J.. ( 2012;). Identification of dimorphism-involved genes of Yarrowia lipolytica by means of microarray analysis. Res Microbiol163:378–387 [CrossRef][PubMed]
    [Google Scholar]
  40. Morgunov I. G., Kamzolova S. V., Lunina J. N.. ( 2013;). The citric acid production from raw glycerol by Yarrowia lipolytica yeast and its regulation. Appl Microbiol Biotechnol97:7387–7397 [CrossRef][PubMed]
    [Google Scholar]
  41. Nicaud J. M.. ( 2012;). Yarrowia lipolytica . Yeast29:409–418 [CrossRef][PubMed]
    [Google Scholar]
  42. O’Shea D. G., Walsh P. K.. ( 1996;). Morphological characterization of the dimorphic yeast Kluyveromyces marxianus var. marxianus NRRLy2415 by semi-automated image analysis. Biotechnol Bioeng51:679–690 [CrossRef][PubMed]
    [Google Scholar]
  43. O’Shea D. G., Walsh P. K.. ( 2000;). The effect of culture conditions on the morphology of the dimorphic yeast Kluyveromyces marxianus var. marxianus NRRLy2415: a study incorporating image analysis. Appl Microbiol Biotechnol53:316–322 [CrossRef][PubMed]
    [Google Scholar]
  44. Okoshi H., Sato S., Mukataka S., Takahashi J.. ( 1987;). Citric acid production by Candida tropicalis under high dissolved oxygen concentrations. Agric Biol Chem51:257–258 [CrossRef]
    [Google Scholar]
  45. Oliveira A. A. C., Sousa T. V. S., Amaral P. F. F., Coelho M. A. Z., Araujo O. Q. F.. ( 2010;). Study of morphological and physiological parameters of cultures of Yarrowia lipolytica undergone electrochemical stress. Chem Eng Trans20:133–138
    [Google Scholar]
  46. Oswal N., Sarma P. M., Zinjarde S. S., Pant A.. ( 2002;). Palm oil mill effluent treatment by a tropical marine yeast. Bioresour Technol85:35–37 [CrossRef][PubMed]
    [Google Scholar]
  47. Ota Y., Oikawa S., Morimoto Y., Minoda Y.. ( 1984;). Nutritional factors causing mycelial development of Saccharomycopsis lipolytica . Agric Biol Chem48:1933–1939 [CrossRef]
    [Google Scholar]
  48. Papanikolaou S., Aggelis G.. ( 2002;). Lipid production by Yarrowia lipolytica growing on industrial glycerol in a single-stage continuous culture. Bioresour Technol82:43–49 [CrossRef][PubMed]
    [Google Scholar]
  49. 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 Technol21:83–87 [CrossRef]
    [Google Scholar]
  50. 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 Leeuwenhoek80:215–224 [CrossRef][PubMed]
    [Google Scholar]
  51. Papanikolaou S., Muniglia L., Chevalot I., Aggelis G., Marc I.. ( 2002;). Yarrowia lipolytica as a potential producer of citric acid from raw glycerol. J Appl Microbiol92:737–744 [CrossRef][PubMed]
    [Google Scholar]
  52. Papanikolaou S., Sarantou S., Komaitis M., Aggelis G.. ( 2004;). Repression of reserve lipid turnover in Cunninghamella echinulata and Mortierella isabellina cultivated in multiple-limited media. J Appl Microbiol97:867–875 [CrossRef][PubMed]
    [Google Scholar]
  53. Papanikolaou S., Chevalot I., Galiotou-Panayotou M., Komaitis M., Marc I., Aggelis G.. ( 2007;). Industrial derivative of tallow: a promising renewable substrate for microbial lipid, single-cell protein and lipase production by Yarrowia lipolytica . Electron J Biotechnol10:425–435 [CrossRef]
    [Google Scholar]
  54. Papanikolaou S., Galiotou-Panayotou M., Fakas S., Komaitis M., Aggelis G.. ( 2008;). Citric acid production by Yarrowia lipolytica cultivated on olive-mill wastewater-based media. Bioresour Technol99:2419–2428 [CrossRef][PubMed]
    [Google Scholar]
  55. Papanikolaou S., Chatzifragkou A., Fakas S., Galiotou-Panayotou M., Komaitis M., Nicaud J. M., Aggelis G.. ( 2009;). Biosynthesis of lipids and organic acids by Yarrowia lipolytica strains cultivated on glucose. Eur J Lipid Sci Technol111:1221–1232 [CrossRef]
    [Google Scholar]
  56. Pérez-Campo F. M., Domínguez A.. ( 2001;). Factors affecting the morphogenetic switch in Yarrowia lipolytica . Curr Microbiol43:429–433 [CrossRef][PubMed]
    [Google Scholar]
  57. Pollack J. H., Hashimoto T.. ( 1987;). The role of glucose in the pH regulation of germ-tube formation in Candida albicans . J Gen Microbiol133:415–424[PubMed]
    [Google Scholar]
  58. Rane K. D., Sims K. A.. ( 1994;). Oxygen uptake and citric acid production by Candida lipolytica Y 1095. Biotechnol Bioeng43:131–137 [CrossRef][PubMed]
    [Google Scholar]
  59. Rane K. D., Sims K. A.. ( 1995;). Citric acid production by Candida lipolytica Y 1095 in cell recycle and fed-batch fermentors. Biotechnol Bioeng46:325–332 [CrossRef][PubMed]
    [Google Scholar]
  60. Rodríguez C., Domínguez A.. ( 1984;). The growth characteristics of Saccharomycopsis lipolytica: morphology and induction of mycelium formation. Can J Microbiol30:605–612 [CrossRef]
    [Google Scholar]
  61. Ruiz-Herrera J., Sentandreu R.. ( 2002;). Different effectors of dimorphism in Yarrowia lipolytica . Arch Microbiol178:477–483 [CrossRef][PubMed]
    [Google Scholar]
  62. Rymowicz W., Fatykhova A. R., Kamzolova S. V., Rywińska A., Morgunov I. G.. ( 2010;). Citric acid production from glycerol-containing waste of biodiesel industry by Yarrowia lipolytica in batch, repeated batch, and cell recycle regimes. Appl Microbiol Biotechnol87:971–979 [CrossRef][PubMed]
    [Google Scholar]
  63. Rywińska A., Rymowicz W.. ( 2010;). High-yield production of citric acid by Yarrowia lipolytica on glycerol in repeated-batch bioreactors. J Ind Microbiol Biotechnol37:431–435 [CrossRef][PubMed]
    [Google Scholar]
  64. Rywińska A., Musiał I., Rymowicz W., Żarowska B., Boruczkowski T.. ( 2012;). Effect of agitation and aeration on the citric acid production by Yarrowia lipolytica grown on glycerol. Prep Biochem Biotechnol42:279–291 [CrossRef][PubMed]
    [Google Scholar]
  65. San-Blas G., San-Blas F., Mackenzie D. W. R.. ( 1984;). Molecular aspects of fungal dimorphism. Crit Rev Microbiol11:101–127 [CrossRef][PubMed]
    [Google Scholar]
  66. Srere P. A.. ( 1959;). The citrate cleavage enzyme. I. Distribution and purification. J Biol Chem234:2544–2547[PubMed]
    [Google Scholar]
  67. Szabo R., Štofaníková V.. ( 2002;). Presence of organic sources of nitrogen is critical for filament formation and pH-dependent morphogenesis in Yarrowia lipolytica . FEMS Microbiol Lett206:45–50 [CrossRef][PubMed]
    [Google Scholar]
  68. Walker G. M., O’Neill J. M.. ( 1990;). Morphological and metabolic changes in the yeast Kluyveromyces marxianus var. marxianus NRRLy2415 during fermentation on lactose. J Chem Technol Biotechnol49:75–89 [CrossRef]
    [Google Scholar]
  69. Zinjarde S. S., Chinnathambi S., Lachke A. H., Pant A.. ( 1997;). Isolation of an emulsifier from Yarrowia lipolytica NCIM 3589 using a modified mini isoelectric focusing unit. Lett Appl Microbiol24:117–121 [CrossRef]
    [Google Scholar]
  70. Zinjarde S., Pant A., Deshpande M.. ( 1998;). Dimorphic transition in Yarrowia lipolytica isolated from oil-polluted sea water. Mycol Res102:553–558 [CrossRef]
    [Google Scholar]
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