DOI QR코드

DOI QR Code

Investigation of Filamentous Fungi Producing Safe, Functional Water-Soluble Pigments

  • Heo, Young Mok (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Kim, Kyeongwon (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Kwon, Sun Lul (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Na, Joorim (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Lee, Hanbyul (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Jang, Seokyoon (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Kim, Chul Hwan (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Jung, Jinho (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University) ;
  • Kim, Jae-Jin (Division of Environmental Science & Ecological Engineering College of Life Sciences & Biotechnology, Korea University)
  • Received : 2018.05.14
  • Accepted : 2018.07.17
  • Published : 2018.09.01

Abstract

The production of water-soluble pigments by fungal strains indigenous to South Korea was investigated to find those that are highly productive in submerged culture. Among 113 candidates, 34 strains that colored the inoculated potato dextrose agar medium were selected. They were cultured in potato dextrose broth and extracted with ethanol. The productivity, functionality (radical-scavenging activities), and color information (CIELAB values) of the pigment extracts were measured. Five species produced intense yellowish pigments, and two produced intense reddish pigments that ranked the highest in terms of absorbance units produced per day. The pigment extracts of Penicillium miczynskii, Sanghuangporus baumii, Trichoderma sp. 1, and Trichoderma afroharzianum exhibited high radical-scavenging activity. However, the S. baumii extract showed moderate toxicity in the acute toxicity test, which limits the industrial application of this pigment. In conclusion, P. miczynskii KUC1721, Trichoderma sp. 1 KUC1716, and T. afroharzianum KUC21213 were the best fungal candidates to be industrial producers of safe, functional water-soluble pigments.

Keywords

References

  1. Scotter MJ. Colour additives for foods and beverages. Elsevier; 2015.
  2. Mapari SAS, Nielsen KF, Larsen TO, et al. Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol. 2005;16:231-238. https://doi.org/10.1016/j.copbio.2005.03.004
  3. Arnold LE, Lofthouse N, Hurt E. Artificial food colors and attention-deficit/hyperactivity symptoms: conclusions to dye for. Neurotherapeutics. 2012;9:599-609. https://doi.org/10.1007/s13311-012-0133-x
  4. Osman MY, Sharaf IA, Osman HMY, et al. Synthetic organic food colouring agents and their degraded products: effects on human and rat cholinesterases. Br J Biomed Sci. 2004;61:128-132. https://doi.org/10.1080/09674845.2004.11732657
  5. Stevens LJ, Burgess JR, Stochelski MA, et al. Amounts of artificial food colors in commonly consumed beverages and potential behavioral implications for consumption in children. Clin Pediatr (Phila). 2014;53:133-140. https://doi.org/10.1177/0009922813502849
  6. Stevens LJ, Kuczek T, Burgess JR, et al. Mechanisms of behavioral, atopic, and other reactions to artificial food colors in children. Nutr Rev. 2013;71:268-281. https://doi.org/10.1111/nure.12023
  7. Ogbonna CN. Production of food colourants by filamentous fungi. Afr J Microbiol Res. 2016;10:960-971. https://doi.org/10.5897/AJMR2016.7904
  8. Dufosse L, Fouillaud M, Caro Y, et al. Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr Opin Biotechnol. 2014;26:56-61. https://doi.org/10.1016/j.copbio.2013.09.007
  9. Velmurugan P, Kamala-Kannan S, Balachandar V, et al. Natural pigment extraction from five filamentous fungi for industrial applications and dyeing of leather. Carbohydr Polym. 2010;79:262-268. https://doi.org/10.1016/j.carbpol.2009.07.058
  10. Fox EM, Howlett BJ. Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol. 2008;11:481-487. https://doi.org/10.1016/j.mib.2008.10.007
  11. da Costa Souza PN, Grigoletto TLB, de Moraes LAB, et al. Production and chemical characterization of pigments in filamentous fungi. Microbiology (Reading Engl). 2016;162:12-22. https://doi.org/10.1099/mic.0.000168
  12. Feng Y, Shao Y, Chen F. Monascus pigments. Appl Microbiol Biotechnol. 2012;96:1421-1440. https://doi.org/10.1007/s00253-012-4504-3
  13. Gessler NN, Egorova AS, Belozerskaia TA. Fungal anthraquinones (review). Prikl Biokhim Mikrobiol. 2013;49:109-123.
  14. Teixeira MFS, Martins MS, Da Silva JC, et al. Amazonian Biodiversity: Pigments from Aspergillus and Penicillium-Characterizations, Antibacterial Activities and their Toxicities. Curr Trends Biotechnol Pharm. 2012;6:300-311.
  15. Blanc PJ, Laussac JP, Lebars J, et al. Characterization of monascidin A from Monascus as Citrinin. Int J Food Microbiol. 1995;27:201-213. https://doi.org/10.1016/0168-1605(94)00167-5
  16. Mapari SAS, Thrane U, Meyer AS. Fungal polyketide azaphilone pigments as future natural food colorants?. Trends Biotechnol. 2010;28:300-307. https://doi.org/10.1016/j.tibtech.2010.03.004
  17. Costa J, Marcos AT, de la Fuente JL, et al. Method of producing b-carotene by means of mixed culture fermentation using (+) and (-) strains of Blakeslea trispora. Int Patent WO. 2003;3:064673.
  18. Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113-118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
  19. Hong J-H, Jang S, Heo YM, et al. Investigation of marine-derived fungal diversity and their exploitable biological activities. Mar Drugs. 2015;13:4137-4155. https://doi.org/10.3390/md13074137
  20. White TJ, Bruns T, Lee S, et al. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. Academic Press; 1990. p. 315-22.
  21. O'Donnell K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol. 1997;7:103-116. https://doi.org/10.1006/mpev.1996.0376
  22. Glass NL, Donaldson GC. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995;61:1323-1330.
  23. Carbone I, Kohn LM. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia. 1999;91:553-556. https://doi.org/10.2307/3761358
  24. Samuels GJ, Dodd SL, Gams W, et al. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia. 2002;94:146-170. https://doi.org/10.1080/15572536.2003.11833257
  25. Re R, Pellegrini N, Proteggente A, et al. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med . 1999;26:1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
  26. Fukumoto LR, Mazza G. Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem. 2000;48:3597-3604. https://doi.org/10.1021/jf000220w
  27. OECD. Test No. 202: Daphnia sp. Acute Immobilisation Test: OECD Publishing; 2004.
  28. Hosoya T, Matsuoka T, Serizawa N, et al. Two morphological groups derived from Clonostachys cylindrospora and their relationship to trans-4-hydroxy-(L)-proline productivity. Mycoscience. 1995;36:193-197. https://doi.org/10.1007/BF02268557
  29. Esposito E, Silva M. Systematics and environmental application of the genus Trichoderma. Crit Rev Microbiol. 1998;24:89-98. https://doi.org/10.1080/10408419891294190
  30. Donnelly DMX, Sheridan MH. Anthraquinones from Trichoderma polysporum. Phytochemistry. 1986;25:2303-2304. https://doi.org/10.1016/S0031-9422(00)81684-2
  31. Reino JL, Guerrero RF, Hernandez-Galan R, et al. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev. 2007;7:89-123. https://doi.org/10.1007/s11101-006-9032-2
  32. Wichmann G, Herbarth O, Lehmann I. The mycotoxins citrinin, gliotoxin, and patulin affect interferon-${\gamma}$ rather than interleukin-4 production in human blood cells. Environ Toxicol. 2002;17:211-218. https://doi.org/10.1002/tox.10050
  33. Frisvad JC, Yilmaz N, Thrane U, et al. Talaromyces atroroseus, a new species efficiently producing industrially relevant red pigments. PLoS One. 2013;8:e84102. https://doi.org/10.1371/journal.pone.0084102
  34. Bouhet JC, Pham Van Chuong P, Toma F, et al. Isolation and characterization of luteoskyrin and rugulosin, two hepatotoxic anthraquinonoids from Penicillium islandicum Sopp. and Penicillium rugulosum Thom. J Agric Food Chem. 1976;24:964-972. https://doi.org/10.1021/jf60207a028
  35. Emeh CO, Marth EH. Yields of rubratoxin from Penicillium rubrum. Trans Br Mycol Soc. 1977;68:112-115. https://doi.org/10.1016/S0007-1536(77)80163-0
  36. Ishii K, Itoh T, Kobayashi K, et al. Isolation and characterization of a cytotoxic metabolite of Talaromyces bacillosporus. Appl Environ Microbiol. 1995;61:941.
  37. Nakagawa M, Kawai K, Kawai K. Contact allergy to kojic acid in skin care products. Contact Derm. 1995;32:9-13. https://doi.org/10.1111/j.1600-0536.1995.tb00832.x
  38. Pitt JI. Biology and ecology of toxigenic Penicillium species. In: DeVries JW, Trucksess MW, Jackson LS, editors. Mycotoxins and Food Safety. Boston, MA: Springer; 2002. p. 29-41.
  39. LoBuglio KF, Taylor JW. Phylogeny and PCR identification of the human pathogenic fungus Penicillium marneffei. J Clin Microbiol. 1995;33:85-89.
  40. Mapari SAS, Meyer AS, Thrane U, et al. Identification of potentially safe promising fungal cell factories for the production of polyketide natural food colorants using chemotaxonomic rationale. Microb Cell Fact. 2009;8:24. https://doi.org/10.1186/1475-2859-8-24
  41. El-Shanawany AA, Mostafa ME, Barakat A. Fungal populations and mycotoxins in silage in Assiut and Sohag governorates in Egypt, with a special reference to characteristic Aspergilli toxins. Mycopathologia. 2005;159:281-289. https://doi.org/10.1007/s11046-004-5494-1
  42. Singh PD, Johnson JH, Aklonis CA, et al. Two new inhibitors of phospholipase A2 produced by Penicillium chermesinum. Taxonomy, fermentation, isolation, structure determination and biological properties. J Antibiot. 1985;38:706-712. https://doi.org/10.7164/antibiotics.38.706
  43. Christensen M, Frisvad JC, Tuthill D. Taxonomy of the Penicillium miczynskii group based on morphology and secondary metabolites. Mycol Res. 1999;103:527-541. https://doi.org/10.1017/S0953756298007515
  44. Hwang HJ, Kim SW, Lim JM, et al. Hypoglycemic effect of crude exopolysaccharides produced by a medicinal mushroom Phellinus baumii in streptozotocin-induced diabetic rats. Life Sci. 2005;76:3069-3080. https://doi.org/10.1016/j.lfs.2004.12.019
  45. Jang B-S, Kim J-C, Bae J-S, et al. Extracts of Phellinus gilvus and Phellinus baumii inhibit pulmonary inflammation induced by lipopolysaccharide in rats. Biotechnol Lett. 2004;26:31-33. https://doi.org/10.1023/B:BILE.0000009456.63616.32
  46. Kim H-M, Lee D-H. Characterization of anti-inflammation effect of aqueous extracts from Phellinus baumii. Korean J Mycol. 2010;38:179-183. https://doi.org/10.4489/KJM.2010.38.2.179
  47. Luo J, Liu J, Sun Y, et al. Medium optimization, preliminary characterization and antioxidant activity in vivo of mycelial polysaccharide from Phellinus baumii Pilat. Carbohydr Polym. 2010;81:533-540. https://doi.org/10.1016/j.carbpol.2010.03.010
  48. Park J, Kang KA, Zhang R, et al. Antioxidant activity of water extract from the cultured mycelia of Phellinus baumii. Cancer Prevent Res. 2006;11:329-335.
  49. Bae J-S, Freeman HS. Aquatic toxicity evaluation of copper-complexed direct dyes to the Daphnia magna. Dyes and Pigments. 2007;73:126-132. https://doi.org/10.1016/j.dyepig.2005.10.019

Cited by

  1. Fungal Pigments and Their Prospects in Different Industries vol.7, pp.12, 2018, https://doi.org/10.3390/microorganisms7120604
  2. Diversity of Trichoderma spp. in Marine Environments and Their Biological Potential for Sustainable Industrial Applications vol.12, pp.10, 2018, https://doi.org/10.3390/su12104327
  3. Fungal Pigments: Potential Coloring Compounds for Wide Ranging Applications in Textile Dyeing vol.6, pp.2, 2018, https://doi.org/10.3390/jof6020068
  4. Antioxidant Activity and Role of Culture Condition in the Optimization of Red Pigment Production by Talaromyces purpureogenus KKP Through Response Surface Methodology vol.77, pp.8, 2018, https://doi.org/10.1007/s00284-020-01995-4
  5. Molecular Characterization of Fungal Pigments vol.7, pp.5, 2018, https://doi.org/10.3390/jof7050326
  6. Safety Evaluation of Fungal Pigments for Food Applications vol.7, pp.9, 2021, https://doi.org/10.3390/jof7090692