Abstract
Yarrowia lipolytica is able to metabolize high Mr hydrophobic natural compounds such as fatty acids and hydrocarbons. Characteristically, strains of Y. lipolytica can grow as populations with variable proportions of yeast and filamentous forms. In the present study, we describe the dimorphic characteristics of a variant designated as Y. lipolytica var. indica isolated from petroleum contaminated sea water and the effect of cell morphology on hydrocarbon metabolism. The variant behaved as a yeast monomorphic strain, under conditions at which terrestrial Y. lipolytica strain W29 and its derived strains, grow as almost uniform populations of mycelial cells. Using organic nitrogen sources and N-acetylglucosamine as carbon source, var. indica was able to form mycelial cells, the proportion of which increased when incubated under semi-anaerobic conditions. The cell surface characteristics of var. indica and W29 were found to be different with respect to contact angle and percent hydrophobicity. For instance, percent hydrophobicity of var. indica was 89.93 ± 1.95 while that of W29 was 70.78 ± 1.1. Furthermore, while all tested strains metabolize hydrocarbons, only var. indica was able to use it as a carbon source. Yeast cells of var. indica metabolized hexadecane with higher efficiency than the mycelial form, whereas the mycelial form of the terrestrial strain metabolized the hydrocarbon more efficiently, as occurred with the mycelial monomorphic mutant AC11, compared to the yeast monomorphic mutant AC1.
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Agnihotri M, Joshi S, Kumar AR, Zinjarde S, Kulkarni S (2009) Biosynthesis of gold nanoparticles by the tropical marine yeast Yarrowia lipolytica NCIM 3589. Mater Lett 63:1231–1234
Aguedo M, Waché Y, Mazoyer V, Sequeira-Le Grand A, Belin JM (2003) Increased electron donor and electron acceptor characters enhance the adhesion between oil droplets and cells of Yarrowia lipolytica as evaluated by a new cytometric assay. J Agric Food Chem 51:3007–3011
Amaral PFF, Lehocky M, Barros-Timmons AMV, Rocha-Leao MHM, Coelho MAZ, Coutinho JAP (2006) Cell surface characterization of Yarrowia lipolytica IMUFRJ 50682. Yeast 23:867–877
Andrade MJ, Rodriguez M, Sanchez B, Aranda E, Cordoba JJ (2006) DNA typing methods for differentiation of yeasts related to dry-cured meat products. Int J Food Microbiol 107:48–58
Bankar A, Winey M, Prakash D, Kumar AR, Gosavi S, Kapadnis B, Zinjarde S (2012) Bioleaching of fly ash by the tropical marine yeast, Yarrowia lipolytica NCIM 3589. Appl Biochem Biotechnol 168:2205–2217
Bassel JB, Mortimer RK (1985) Identification of mutations preventing n-hexadecane uptake among 26 n-alkane non-utilizing mutants of Yarrowia (Saccharomycopsis) lipolytica. Curr Genet 9:579–586
Cao C, Li R, Wan Z, Liu W, Wang X, Qiao J, Wang D, Bulmer G, Calderone R (2007) The effects of temperature, pH, and salinity on the growth and dimorphism of Penicillium marneffei. Med Mycol 45:401–407
Cervantes-Chavez JA, Ruiz-Herrera J (2006) STE11 disruption reveals the central role of a MAPK pathway in dimorphism and mating in Yarrowia lipolytica. FEMS Yeast Res 6:801–815
Cervantes-Chavez JA, Kronberg F, Passeron S, Ruiz-Herrera J (2009) Regulatory role of the PKA pathway in dimorphism and mating in Yarrowia lipolytica. Fungal Genet Biol 46:390–399
Fickers P, Benetti P-H, Wache Y, Marty A, Mauersberger S, Smit MS, Nicaud J-M (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543
Fukumaki T, Inoue A, Moriya K, Horikoshi K (1994) Isolation of a marine yeast that degrades hydrocarbon in the presence of organic solvent. Biosci Biotech Biochem 58:1784–1788
Guevara-Olvera L, Calvo-Mendez C, Ruiz-Herrera J (1993) The role of polyamine metabolism in dimorphism of Yarrowia lipolytica. J Gen Microbiol 193:485–493
Hirai M, Shimizu S, Teranishi Y, Tanaka A (1972) Effects of hydrocarbons on the morphology of Candida tropicalis pK 233. Agric Biol Chem 36:2335–2343
Huey B, Hall J (1989) Hypervariable DNA fingerprinting in Escherichia coli, Minisatellite probe from bacteriophage M13. J Bacteriol 171:2528–2532
Imandi SB, Garapati HR (2007) Lipase production by Yarrowia lipolytica NCIM 3589 in solid state fermentation using mixed substrate. Res J Microbiol 2:469–474
Jain MR, Zinjarde SS, Deobagkar DD, Deobagkar DN (2004) 2,4,6-Trinitrotoluene transformation by a tropical marine yeast, Yarrowia lipolytica NCIM 3589. Mar Pollut Bull 49:783–788
Katre G, Joshi C, Khot M, Zinjarde S, Kumar AR (2012) Evaluation of single cell oil (SCO) from a tropical marine yeast Yarrowia lipolytica NCIM 3589 as a potential feedstock for biodiesel. AMB Express 2:36–49
Martins FF, Ferreira TF, Azevedo DA, Coelho MAZ (2012) Evaluation of crude oil degradation by Yarrowia lipolytica. Chem Eng Trans 27:223–228
Mauersberger S, Wang H-J, Gaillardin C, Barth G, Nicaud J-M (2001) Insertional mutagenesis in the n-alkane assimilating yeast Yarrowia lipolytica: generation of tagged mutations in genes involved in hydrophobic substrate utilization. J Bacteriol 183:5102–5109
Michely S, Gaillardin C, Nicaud J-M, Neuveglise C (2013) Comparative physiology of oleaginous species from the Yarrowia clade. PLoS ONE 8:e63356
Oswal N, Sarma PM, Zinjarde SS, Pant A (2002) Palm oil mill effluent treatment by a tropical marine yeast. Biores Technol 85:35–37
Pramateftaki PV, Lanaridis P, Typas MA (2000) Molecular identification of wine yeasts at species or strain level: a case study with strains from two vine-growing areas of Greece. J Appl Microbiol 89:236–248
Rodriguez C, Dominguez A (1984) The growth-characteristics of Saccharomycopsis lipolytica. Morphology and induction of mycelium formation. Can J Microbiol 30:605–612
Ruiz-Herrera J, Sentandreu R (2002) Different effectors of dimorphism in Yarrowia lipolytica. Arch Microbiol 178:477–483
Sambrook J, Russell DW (2001) Molecular cloning, a laboratory manual, 1st edn. Cold Spring Harbor laboratory press, Cold Spring Harbor, New York
Thevenieau F, Le Dall M-T, Nthangeni B, Mauersberger S, Marchal R, Nicaud J-M (2007) Characterization of Yarrowia lipolytica mutants affected in hydrophobic substrate utilization. Fungal Genet Biol 44:531–542
Thevenieau F, Beopoulos A, Desfougeres T, Sabirova J, Albertin K, Zinjarde S, Nicaud J-M (2010) Uptake and assimilation of hydrophobic substrates by the oleaginous yeast Yarrowia lipolytica. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1514–1525
van der Mei HC, van de Belt-Gritter B, Busscher HJ (1995) Implications of microbial adhesion to hydrocarbons for evaluating cell surface hydrophobicity 2. Adhesion mechanisms. Colloids Surf B 5:117–126
van der Mei HC, Bos R, Busscher HJ (1998) A reference guide to microbial cell surface hydrophobicity based on contact angles. Colloids Surf B 11:213–221
Vatsal A, Zinjarde SS, Kumar AR (2011) Growth of a tropical marine yeast Yarrowia lipolytica NCIM 3589 on bromoalkanes: relevance of cell size and cell surface properties. Yeast 28:721–732
Zinjarde SS, Pant A, Deshpande MV (1998) Dimorphic transition in Yarrowia lipolytica isolated from oil-polluted sea water. Mycol Res 102:553–558
Zinjarde SS, Kale BV, Vishwasrao PV, Kumar AR (2008) Morphogenetic behavior of tropical marine yeast Yarrowia lipolytica in response to hydrophobic substrates. J Microbiol Biotechnol 18:1522–1528
Zvyagilskaya R, Andreishcheva E, Soares MIM, Khozin I, Berhe A, Persson BL (2001) Isolation and characterisation of a novel leaf inhabiting osmo-, salt-, and alkali-tolerant Yarrowia lipolytica yeast strain. J Basic Microbiol 5:289–303
Acknowledgments
Authors are grateful to Department of Science and Technology, New Delhi and CONACYT, México, for the financial support to the Indo-Mexico visit exchange programme. ASP thanks Council of Scientific and Industrial Research, India for research fellowship. SVK thanks University Grants Commission (UGC) for Teacher’s Fellowship. Authors are thankful to Dr. A. Sen, National Chemical Laboratory, Pune for the GC analysis.
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Communicated by Erko Stackebrandt.
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Palande, A.S., Kulkarni, S.V., León-Ramirez, C. et al. Dimorphism and hydrocarbon metabolism in Yarrowia lipolytica var. indica . Arch Microbiol 196, 545–556 (2014). https://doi.org/10.1007/s00203-014-0990-2
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DOI: https://doi.org/10.1007/s00203-014-0990-2