Skip to main content
Springer Nature Link
Log in

Influence of carbon and nitrogen sources on lipase production by a newly isolated Candida viswanathii strain

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Microorganisms can produce lipases with different biochemical characteristics making necessary the screening of new lipase-producing strains for different industrial applications. In this study, 90 microbial strains were screened as potential lipase producers using a sensitive agar plate method with a suitable medium supplemented with Tween 20 and also a liquid culture supplemented with olive oil. The highest cell growth and lipase production for Candida viswanathii were observed in triolein and oleic acid when used as the only pure carbon source. Renewable low-cost triacylglycerols supported the best cell growth, and olive oil was found to be the best inducer for lipase production (19.50 g/L and 58.50 U). The selected conditions for enzyme production were found with yeast extract as nitrogen source and 1.5 % (w/v) olive oil (85.70 U) that resulted in a good cell growth yield (YX/S = 1.234 g/g) and lipase productivity (1.204 U/h) after 72 h of shake-flask cultivation. C. viswanathii lipase presented high hydrolytic activity on esters bonds of triacylglycerols of long-chain, and this strain can be considered an important candidate for future applications in chemical industries.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Adamczak M, Bornscheuer UT, Bednarski W (2009) The application of biotechnological methods for the synthesis of biodiesel. Eur J Lipid Sci Technol 111:808–813. doi:10.1002/ejlt.200900078

    Article  Google Scholar 

  • Antonian E (1988) Recent advances in the purification, characterization and structure determination of lipases. Lipids 23:1101–1106. doi:10.1007/BF02535273

    Article  PubMed  CAS  Google Scholar 

  • Azeredo LAI, Gomes PM, Sant’anna GL Jr, Castilho LR, Freire DMG (2007) Production and regulation of lipase activity from Penicillium restrictum in submerged and solid-state fermentations. Curr Microbiol 54:361–365. doi:10.1007/s00284-006-0425-7

    Article  PubMed  CAS  Google Scholar 

  • Barth G, Gaillardin C (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19:19–237. doi:10.1111/j.1574-6976.1997.tb00299.x

    Article  Google Scholar 

  • Beopoulos A, Cescut J, Haddouche R, Uribelarrea JL, Molina-Jouve C, Nicaud JM (2009) Yarrowia lipolytica as a model for bio-oil production. Prog Lipid Res 48:357–387. doi:10.1016/j.plipres.2009.08.005

    Article  Google Scholar 

  • Björkling F, Godtfredsen SV, Kirk O (1991) The future impact of industrial lipases. Tibtech 9:360–363. doi:10.1016/0167-7799(91)90119-3

    Article  Google Scholar 

  • Bussamara R, Fuentefria AM, Oliveira ES, Broetto L, Simcikova M, Valente P, Schrank A, Vainstein MH (2010) Isolation of a lipase-secreting yeast for enzyme production in a pilot-plant scale batch fermentation. Biores Technol 101:268–275. doi:10.1016/j.biortech.2008.10.063

    Article  CAS  Google Scholar 

  • Chang SW, Shieh CJ, Lee GC, Akoh CC, Shaw JF (2006) Optimized growth kinetics of Pichia pastoris and recombinant Candida rugosa LIP1 production by RSM. J Mol Microb Biotechnol 11:28–40. doi:10.1159/000092817

    Article  CAS  Google Scholar 

  • Corzo G, Revah S (1999) Production and characterization of the lipase from Yarrowia lipolytica 681. Bioresource Technol 70:173–180. doi:10.1016/S0960-8524(99)00024-3

    Article  CAS  Google Scholar 

  • Dalmau E, Montesinos JL, Lotti M, Casas C (2000) Effect of different carbon sources on lipase production by Candida rugosa. Enzyme Microb Technol 26:657–663. doi:10.1016/S0141-0229(00)00156-3

    Article  PubMed  CAS  Google Scholar 

  • Darvishi F, Nahvi I, Zarkesh-Esfahani H, Momenbeik F (2009) Effect of plant oils upon lipase and citric acid production in Yarrowia lipolytica yeast. J Biomed Biotechnol. doi:10.1155/2009/562943

  • Darvishi F, Destain J, Nahvi I, Thonart P, Zarkesh-Esfahani H (2011) High-level production of extracellular lipase by Yarrowia lipolytica mutants from methyl oleate. New Biotechnol 28:756–760. doi:10.1016/j.nbt.2011.02.002

    Article  CAS  Google Scholar 

  • Elibol M, Ozer D (2000) Influence of oxygen transfer on lipase production by Rhizopus arrhizus. Process Biochem 36:325–329. doi:10.1016/S0032-9592(00)00226-0

    Article  Google Scholar 

  • Fatima Y, Kansal H, Soni P, Banerjee UC (2007) Enantioselective reduction of aryl ketones using immobilized cells of Candida viswanathii. Process Biochem 42:1412–1418. doi:10.1016/j.procbio.2007.07.010

    Article  CAS  Google Scholar 

  • Fickers P, Nicaud JM, Gaillardin C, Destain J, Thonart P (2004) Carbon and nitrogen sources modulate lipase production in the yeast Yarrowia lipolytica. J App Microbiol 96:742–749. doi:10.1111/j.1365-2672.2004.02190.x

    Article  CAS  Google Scholar 

  • Fickers P, Destain J, Thornart P (2005) Hydrophobic substrate utilization by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543. doi:10.1016/j.femsyr.2004.09.004

    Article  PubMed  CAS  Google Scholar 

  • Gulati R, Isar J, Kumar V, Prasad AK, Parmar VS, Saxena RK (2005) Production of a novel alkaline lipase by Fusarium globulosum using neem oil, and its applications. Pure App Chem 77:251–262. doi:10.1351/pac200577010251

    Article  CAS  Google Scholar 

  • Gutarra MLE, Mateus GG, Castilho LR, Freire DMG (2007) Inoculum strategies for Penicillium simplicissimum lipase production by solid-state fermentation using a residue from Babassu oil industry. J Chem Technol Biotechnol 82:313–318. doi:10.1002/jctb.1674

    Article  CAS  Google Scholar 

  • Hankin L, Anagnostakis SG (1975) The use of solid media for detection of enzyme production by fungi. Mycology 67:597–607

    Article  Google Scholar 

  • Houde A, Kademi A, Leblanc D (2004) Lipases and their industrial applications. App Biochem Biotechnol 118:155–170. doi:10.1385/ABAB:118:1-3:155

    Article  CAS  Google Scholar 

  • Kalo P, Kemppinem A (2003) Triglycerides/structures and properties. Encyclopedia of Food Sciences and Nutrition. Elsevier 5857-5868

  • Kamzolova SV, Morgunov IG, Aurich A (2005) Lipase secretion and citric acid production in Yarrowia lipolytica yeast grown on animal and vegetable fat. Food Technol Biotechnol 43:113–122

    CAS  Google Scholar 

  • Kok RG, Nudel CB, Gonzalez RH, Nugteren-Roodzant IM, Hellingwerf KJ (1996) Physiological factors affecting production of extracellular lipase (LipA) in Acinetobacter calcoaceticus BD413: fatty acid repression of lipa expression and degradation of LipA. J Bacteriol 178:6025–6035

    PubMed  CAS  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts, a taxonomic study. Elsevier, San Diego

    Google Scholar 

  • Lakshmi BB, Kangueane P, Abraham B, Pennathur G (1999) Effect of vegetable oils in the secretion of lipase from Candida rugosa (DSM 2031). Lett Appl Microbiol 29:66–70. doi:10.1046/j.1365-2672.1999.00578.x

    Article  CAS  Google Scholar 

  • Leal MCMR (2000) Utilização de enzimas hidrolíticas no tratamento de resíduos da indústria de laticínios. Dissertation, Universidade Federal do Rio de Janeiro

  • Li Q, Yan Y (2010) Production of biodiesel catalysed by immobilization Pseudomonas cepacia lipase from Sapium sebiferum oil in micro-aqueous phase. App Energy 87:3148–3154. doi:10.1016/j.apenergy.2010.02.032

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 265-275

  • Mafakher L, Mirbagheri M, Darvishi F, Nahvi I, Zarkesh-Esfahani H, Emtiazi G (2010) Isolation of lipase and citric acid producing yeasts from agro-industrial wastewater. New Biotechnol 27:337–341. doi:10.1016/j.nbt.2010.04.006

    Article  CAS  Google Scholar 

  • Mahadik ND, Puntambekar US, Bastawde KB, Khire JM, Gokhale DV (2002) Production of acidic lipase by Aspergillus niger in solid state fermentation. Process Biochem 38:715–721. doi:10.1016/S0032-9592(02)00194-2

    Article  CAS  Google Scholar 

  • Messias JM, Costa BZ, Lima VMG, Dekker RFH, Rezende MI, Krieger N, Barbosa AM (2009) Screening Botryosphaeria species for lipases: production of lipase by Botryosphaeria ribis EC-01 grown on soybean oil and other carbon sources. Enzyme Microb Techno 45:426–431. doi:10.1016/j.enzmictec.2009.08.013

    Article  CAS  Google Scholar 

  • Obradors N, Montesinos JL, Valero F, Lafuente FJ, Sola C (1993) Effects of different fatty acids in lipase production by Candida rugosa. Biotechnol Let 15:357–360. doi:10.1007/BF00128276

    Article  CAS  Google Scholar 

  • Ohnishi K, Yoshida Y, Sekiguchi J (1994) Lipase production of Aspergillus oryzae. J Fermentation Bioeng 77:490–495. doi:10.1016/0922-338X(94)90116-3

    Article  CAS  Google Scholar 

  • Palomo JM, Ortiz C, Fernández-Lorente G, Fuente M, Guisán JM, Fernández-Lafuente R (2005) Lipase-lipase interactions as a new tool to immobilize and modulate the lipase properties. Enzyme Microb Technol 36:447–454. doi:10.1016/j.enzmictec.2004.09.013

    Article  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. doi:10.1002/ejlt.200900197

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2011) Lipids of oleaginous yeasts. Part I: Biochemistry of single cell oil production. Eur J Lipid Sci Technol 113:1031–1051. doi:10.1002/ejlt.201100014

    Article  CAS  Google Scholar 

  • Papanikolaou S, Chevalot I, Galiotou-Panayotu M, Komatis 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. Electronic J Biotechnol 10. doi:10.2225/vol10-issue3-fulltext-8

  • Pogori N, Ahmad C, Yan X, Dong W (2008) Production and biochemical characterization of an extracellular lipase from Rhizopus chinesis CCTCC M201021. Biotechnology 7:710–717

    Article  CAS  Google Scholar 

  • Rodriguez JA, Mateos JC, Nungaray J, Gonzalez V, Bhagnagar T, Roussos S, Cordova J, Baratti J (2006) Improving lipase production by nutrient source modification using Rhizopus homothallicus cultured in solid state fermentation. Process Biochem 41:2264–2269. doi:10.1016/j.procbio.2006.05.017

    Article  CAS  Google Scholar 

  • Ruegger MJS, Tauk-Tornisielo SM (2004) Atividade da celulase de fungos isolados do solo da Estação Ecológica de Juréia-Itatins, São Paulo, Brasil. Rev Bras Bot 27:205–211

    Article  CAS  Google Scholar 

  • Salimon J, Noor DAM, Nazrizawati AT (2010) Fatty composition and physiological properties of Malaysian castor been Ricinus communis L. seed oil. Sains Malaysians 39:61–764. doi:10.1021/jf902726p

    Google Scholar 

  • Saravanan AN, Suchitra N, Dhandayuthapani K (2007) Role of saturated fatty acids in lipase production using Pseudomonas aeruginosa. J Food Biochem 31:748–756. doi:10.1111/j.1745-4514.2007.00140.x

    Article  CAS  Google Scholar 

  • Sarda L, Desnuelle P (1958) Action de la lipase pancreátique sur les esters em émulsion. Biochim Biophys Acta 30:513–521. doi:10.1016/0006-3002(58)90097-0

    Article  PubMed  CAS  Google Scholar 

  • Seitz EW (1974) Industrial application of microbial lipases: a review. J Am Oil Chem Soc 51:12–16. doi:10.1007/BF02545206

    Article  PubMed  CAS  Google Scholar 

  • Sharma R, Chisti Y, Banerjee UC (2001) Production, purification, characterization, and applications of lipases. Biotechn Adv 19:627–662. doi:10.1016/S0734-9750(01)00086-6

    Article  CAS  Google Scholar 

  • Sheng J, Wang F, Wang HY, Sun M (2011) Cloning, characterization and expression of a novel lipase gene from marine psychrotrophic Yarrowia lipolytica. Ann Microbiol. doi:10.1007/s13213-011-0348-9

  • Shimada Y, Sugihara A, Nagao T, Tominaga Y (1992) Induction of Geotrichium candidum lipase by long-chain fatty acids. J Fermentation Bioeng 74:77–80

    Article  CAS  Google Scholar 

  • Simões MLG, Tauk-Tornisielo SM (2006) Comparação da técnica tradicional e do método turbidimétrico automático no cultivo em diferentes fortes de carbono de fungos filamentosos isolados de área de caatinga. Holos Env 5:94–103

    Google Scholar 

  • Soares J Jr, Mariano AP, Angelis DF (2008) Biodegradation of biodiesel/diesel blends by Candida viswanathii. Afr J Biotechn 8:2774–2778. doi:10.5897/AJB09.238

    Google Scholar 

  • Takaç S, Unlu AE, Erden B (2010) Oxygen transfer strategy modulates the production of lipase and esterase enzymes by Candida rugosa. J Mol Cat B-Enz 64:150–154. doi:10.1016/j.molcatb.2009.07.005

    Article  Google Scholar 

  • Tan T, Zhang M, Xu J, Zhang J (2004) Optimization of culture conditions and properties of lipase from Penicillium camembertii Thom PG-3. Process Biochem 39:1495–1502. doi:10.1016/S0032-9592(03)00296-6

    Article  CAS  Google Scholar 

  • Teng Y, Xu Y, Wang D (2009) Production and regulation of different lipase activities from Rhizopus chinensis in submerged fermentations by lipids. J Mol Cat B-Enz 57:292–298. doi:10.1016/j.molcatb.2008.10.003

    Article  CAS  Google Scholar 

  • Treichel H, Oliveira D, Mazutti MA, Di Luccio M, Oliveira JV (2010) A review on microbial lipases production. Food Bioprocess Technol 3:182–196. doi:10.1007/s11947-009-0202-2

    Article  CAS  Google Scholar 

  • Vakhlu J, Kour A (2006) Yeast lipases: enzyme purification, biochemical properties and gene cloning. Electronic J Biotechnol 9. doi:10.2225/vol9-issue1-fulltext-9

  • Vargas GDLP, Treichel H, Oliveira D, Beneti SC, Freire DMG, Di Luccio M (2008) Optimization of lipase production by Penicillium simplicissimun in soybean meal. J Chem Technol Biotechnol 83:47–54. doi:10.1002/jctb.1776

    Article  CAS  Google Scholar 

  • Vogel HJ (1956) A convenient growth medium for Neurospora crassa (medium N). Microbiol Gen Bull 13:42–43

    Google Scholar 

  • Wang L, Chi Z, Wang X, Liu Z, Li J (2007) Diversity of lipase-producing yeasts from marine environments and oil hydrolysis by their crude enzymes. Ann Microbiol 57:495–501. doi:10.1007/BF03175345

    Article  CAS  Google Scholar 

  • Yang J, Koga Y, Nakano H, Yamane T (2002) Modifying the chaing-length selectivity of the lipase from Burkholderia cepacia KWI-56 through in vitro combinatorial mutagenesis in the substrate-binding site. Protein Eng 15:147–152. doi:10.1093/protein/15.2.147

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the National Council of Technological and Scientific Development (CNPq) for financial support and for the scholarship awarded to the first author; Dr. Paula Benevides de Morais for providing the yeasts of Cerrado environment; Dr. Dejanira de Franceschi de Angelis for providing the Candida viswanathii strain for this study; and Dr. César R. F. Terrasan for his suggestions on the manuscript.

Author information

Authors and Affiliations

  1. Environmental Studies Center, Universidade Estadual Paulista, Rio Claro, Av. 24-A, 1515, Bela Vista, Rio Claro, São Paulo State, Brazil, 13506-900

    Alex Fernando de Almeida & Sâmia Maria Taulk-Tornisielo

  2. Biochemistry and Microbiology Department, Universidade Estadual Paulista, Rio Claro, Av. 24-A, 1515, Bela Vista, Rio Claro, São Paulo State, Brazil, 13506-900

    Eleonora Cano Carmona

Authors
  1. Alex Fernando de Almeida
    View author publications

    Search author on:PubMed Google Scholar

  2. Sâmia Maria Taulk-Tornisielo
    View author publications

    Search author on:PubMed Google Scholar

  3. Eleonora Cano Carmona
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Eleonora Cano Carmona.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Almeida, A.F., Taulk-Tornisielo, S.M. & Carmona, E.C. Influence of carbon and nitrogen sources on lipase production by a newly isolated Candida viswanathii strain. Ann Microbiol 63, 1225–1234 (2013). https://doi.org/10.1007/s13213-012-0580-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-012-0580-y

Keywords