Mycological Progress

, Volume 16, Issue 5, pp 507–512 | Cite as

Production of fatty acid methyl esters and other bioactive compounds in elicited cultures of the fungus Mucor circinelloides

  • P. J. Sánchez-Pujante
  • B. Miras-Moreno
  • P. Soluyanova
  • V. Garre
  • M. A. Pedreño
  • Lorena Almagro
Original Article
  • 168 Downloads

Abstract

In this work, the production of carotenoids and volatile compounds in Mucor circinelloides cell cultures treated with methyl jasmonate (MJ) and/or cyclodextrins (CD) was evaluated. CD increased the lutein concentration in the extracellular medium, reaching the highest levels in the combined treatment with MJ, whereas the levels of β-carotene were low. Therefore, the addition of CD to M. circinelloides cultures provokes a release of these compounds into the culture medium. Mucor circinelloides cultures also produced lichesterol, neoergosterol and ergone, suggesting that, under these stress conditions, this fungus diverts the carbon flow to sterol biosynthesis, which, in turn, is required for its survival. More interestingly, CD induced the secretion of sterols in a similar way to carotenoids. Mucor circinelloides cultures treated with MJ and/or CD also produced fatty acid methyl esters (FAMEs) and, in the presence of CD, they were released to culture medium, contributing to the formation of biodiesel. In this way, M. circinelloides cultures produced compounds of biotechnological interest and, therefore, these treated cultures can provide an alternative system, which is, at the same time, more sustainable, economical and ecological for their production.

Keywords

Carotenoids Cyclodextrins Methyl jasmonate Mucor circinelloides cultures Volatile compounds 

Notes

Acknowledgements

This study was funded by Fundación Séneca - Agencia de Ciencia y Tecnología de la Región de Murcia (19876/GERM/15) and the Ministerio de Economía y Competitividad (no. BIO2014-51861-R).

Compliance with ethical standards

Conflict of interest

The authors declare no conflicting interests related to this publication.

References

  1. Bayer M, Proksch P, Felsner I, Brenden H, Kohne Z, Walli R, Duong TN, Götz C, Krutmann J, Grether-Beck S (2011) Photoprotection against UVAR: effective triterpenoids require a lipid raft stabilizing chemical structure. Exp Dermatol 20:955–958. doi: 10.1111/j.1600-0625.2011.01350.x CrossRefPubMedGoogle Scholar
  2. Belchí-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreño MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89. doi: 10.1007/s00299-011-1141-8 CrossRefPubMedGoogle Scholar
  3. Briceño Z, Almagro L, Sabater-Jara AB, Calderón AA, Pedreño MA, Ferrer MA (2012) Enhancement of phytosterols, taraxasterol and induction of extracellular pathogenesis-related proteins in cell cultures of Solanum lycopersicum cv Micro-Tom elicited with cyclodextrins and methyl jasmonate. J Plant Physiol 169:1050–1058. doi: 10.1016/j.jplph.2012.03.008 CrossRefPubMedGoogle Scholar
  4. Debieu D, Bach J, Montesinos E, Fillinger S, Leroux P (2013) Role of sterol 3-ketoreductase sensitivity in susceptibility to the fungicide fenhexamid in Botrytis cinerea and other phytopathogenic fungi. Pest Manag Sci 69:642–651. doi: 10.1002/ps.3418 CrossRefPubMedGoogle Scholar
  5. Fatimah AMZ, Norazian MH, Rashidi O (2012) Identification of carotenoid composition in selected ‘ulam’ or traditional vegetables in Malaysia. Int Food Res J 19:527–530Google Scholar
  6. Lawrence RV, Schuller WH (1971) Conversion of ergosterol into the estrogen neoergosterol by direct peroxide cleavage. J Med Chem 14:466CrossRefPubMedGoogle Scholar
  7. Li CH, Cervantes M, Springer DJ, Boekhout T, Ruiz-Vazquez RM, Torres-Martinez SR, Heitman J, Lee SC (2011) Sporangiospore size dimorphism is linked to virulence of Mucor circinelloides. PLoS Pathog 7:1–18. doi: 10.1371/journal.ppat.1002086 Google Scholar
  8. López-Nicolás JM, Rodríguez-Bonilla P, García-Carmona F (2014) Cyclodextrins and antioxidants. CRC Crit Rev Food Sci Nutr 54:251–276. doi: 10.1080/10408398.2011.582544 CrossRefGoogle Scholar
  9. Moses T, Pollier J, Almagro L, Buyst D, Van Montagu M, Pedreño MA, Martins JC, Thevelein JM, Goossens A (2014) Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16α hydroxylase from Bupleurum falcatum. Proc Natl Acad Sci U S A 111:1634–1639. doi: 10.1073/pnas.1323369111 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Nicolás FE, Calo S, Murcia-Flores L, Garre V, Ruiz-Vázquez RM, Torres-Martínez S (2008) A RING-finger photocarotenogenic repressor involved in asexual sporulation in Mucor circinelloides. FEMS Microbiol Lett 280:81–88. doi: 10.1111/j.1574-6968.2007.01044.x CrossRefPubMedGoogle Scholar
  11. Pedreño MA, Belchí-Navarro S, Almagro L, Bru R (2009) Combined use of methyl jasmonate and cyclodextrins for the production of resveratrol. Patent number WO 2009106662 A1Google Scholar
  12. Rao AV, Agarwal S (2000) Role of antioxidant lycopene in cancer and heart disease. J Am Coll Nutr 19:563–569. doi: 10.1080/07315724.2000.10718953 CrossRefPubMedGoogle Scholar
  13. Rizzello F, De Paolis A, Durante M, Blando F, Mita G, Caretto S (2014) Enhanced production of bioactive isoprenoid compounds from cell suspension cultures of Artemisia annua L. using β-cyclodextrins. Int J Mol Sci 15:19092–19105. doi: 10.3390/ijms151019092 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Rodríguez-Frómeta RA, Gutiérrez A, Torres-Martínez S, Garre V (2013) Malic enzyme activity is not the only bottleneck for lipid accumulation in the oleaginous fungus Mucor circinelloides. Appl Microbiol Biotechnol 97:3063–3072. doi: 10.1007/s00253-012-4432-2 CrossRefPubMedGoogle Scholar
  15. Schipper MAA (1976) On Mucor circinelloides, Mucor racemosus and related species. Stud Mycol 12:1–40Google Scholar
  16. Schlosser D, Irrgang S, Schmauder HP (1993) Steroid hydroxylation with free and immobilized cells of Penicillium raistrickii in the presence of β-cyclodextrin. Appl Microbiol Biotechnol 39:16–20. doi: 10.1007/BF00166841 CrossRefPubMedGoogle Scholar
  17. Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Asp Med 24:345–351. doi: 10.1016/S0098-2997(03)00030-X CrossRefGoogle Scholar
  18. Vicente G, Bautista LF, Rodríguez R, Gutiérrez FJ, Sádaba I, Ruiz-Vázquez RM, Torres-Martínez S, Garre V (2009) Biodiesel production from biomass of an oleaginous fungus. Biochem Eng J 48:22–27. doi: 10.1016/j.bej.2009.07.014 CrossRefGoogle Scholar
  19. Wu FL, Shi L, Yao J, Ren A, Zhou C, Mu DS, Zhao MW (2013) The cloning, characterization, and functional analysis of a gene encoding an isopentenyl diphosphate isomerase involved in triterpene biosynthesis in the Lingzhi or reishi medicinal mushroom Ganoderma lucidum (higher Basidiomycetes). Int J Med Mushrooms 15:223–232. doi: 10.1615/IntJMedMushr.v15.i3.10 CrossRefPubMedGoogle Scholar
  20. Yusoff MFM, Xu X, Guo Z (2014) Comparison of fatty acid methyl and ethyl esters as biodiesel base stock: a review on processing and production requirements. J Am Oil Chem Soc 91:525–531. doi: 10.1007/s11746-014-2443-0 CrossRefGoogle Scholar
  21. Zhao YY, Shen X, Cheng XL, Wei F, Bai X, Lin RC (2012) Urinary metabonomics study on the protective effects of ergosta-4,6,8(14),22-tetraen-3-one on chronic renal failure in rats using UPLC Q-TOF/MS and a novel MS E data collection technique. Process Biochem 47:1980–1987. doi: 10.1016/j.procbio.2012.07.008 CrossRefGoogle Scholar
  22. Zidovetzki R, Levitan I (2007) Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. BBA-Biomembranes 1768:1311–1324. doi: 10.1016/j.bbamem.2007.03.026 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • P. J. Sánchez-Pujante
    • 1
  • B. Miras-Moreno
    • 1
  • P. Soluyanova
    • 1
  • V. Garre
    • 2
  • M. A. Pedreño
    • 1
  • Lorena Almagro
    • 1
  1. 1.Department of Plant Biology, Faculty of BiologyUniversity of MurciaMurciaSpain
  2. 2.Department of Genetics and Microbiology, Faculty of BiologyUniversity of MurciaMurciaSpain

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