Characterization of melanin and optimal conditions for pigment production by an endophytic fungus, Spissiomyces endophytica SDBR-CMU319
Autoři:
Nakarin Suwannarach aff001; Jaturong Kumla aff001; Bunta Watanabe aff003; Kenji Matsui aff004; Saisamorn Lumyong aff001
Působiště autorů:
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand
aff001; Center of Excellence in Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai, Thailand
aff002; Institute for Chemical Research, Kyoto University, Kyoto, Japan
aff003; Graduate School of Sciences and Technology for Innovation (Agriculture), Yamaguchi University, Yamaguchi, Japan
aff004; Academy of Science, The Royal Society of Thailand, Bangkok, Thailand
aff005
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222187
Souhrn
Melanin is a natural pigment that is produced by filamentous fungi. In this study, the endophytic species, Spissiomyces endophytica (strain SDBR-CMU319), produced a brown-black pigment in the mycelia. Consequently, the pigment was extracted from the dried fungal biomass. This was followed by pigment purification, characterization and identification. Physical and chemical characteristics of the pigment showed acid precipitation, alkali solubilization, decolorization with oxidizing agents, and insolubility in most organic solvents and water. The pigment was confirmed as melanin based on ultraviolet-visible spectroscopy, Fourier-transform infrared, and electron paramagnetic resonance spectra analyses. The analyses of the elemental composition indicated that the pigment possessed a low percentage of nitrogen, and therefore, was not 3,4-dihydroxyphenylalanine melanin. Inhibition studies involving specific inhibitors, both tricyclazole and phthalide, and suggest that fungal melanin could be synthesized through the 1,8-dihydroxynaphthalene pathway. The optimum conditions for fungal pigment production from this species were investigated. The highest fungal pigment yield was observed in glucose yeast extract peptone medium at an initial pH value of 6.0 and at 25°C over three weeks of cultivation. This is the first report on the production and characterization of melanin obtained from the genus Spissiomyces.
Klíčová slova:
Biology and life sciences – Plant science – Organisms – Eukaryota – Physical sciences – Chemistry – Chemical reactions – Research and analysis methods – Fungi – Plant pathology – Plant pathogens – Plant fungal pathogens – Rice blast fungus – Chemical compounds – Materials science – Materials – Organic compounds – Carbohydrates – Monosaccharides – Organic chemistry – Agriculture – Spectrum analysis techniques – Glucose – Fungiculture – Pigments – Organic pigments – Melanin – Chemical precipitation – Electron spin resonance spectroscopy
Zdroje
1. Malik K, Tokkas J, Goyal S. Microbial pigments: a review. Int J Microbial Res Technol. 2012; 1: 361−365.
2. Akilandeswari P, Pradeep BV. Exploration of industrially important pigments from soil fungi. Appl Microbiol Biotechnol. 2016; 100: 1631–164. doi: 10.1007/s00253-015-7231-8 26701360
3. Unagul P, Wongsa P, Kittakoop P, Intamas S, Kulchai PS, Tanticharoen M. Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis BCC 1869. J Ind Microbiol Biotechnol. 2005; 32: 135–140. doi: 10.1007/s10295-005-0213-6 15891934
4. Shindy HA. Problems and solutions in colors, dyes and pigments chemistry: a Review. Chem Int. 2017; 3: 97–105.
5. Joshi V, Attri D, Bala A, Bhushan S. Microbial Pigments. Indian J Biotechnol. 2003; 2: 362–369.
6. Venil CK, Lakshmanaperumalsamy P. An insightful overview on microbial pigment, prodigiosin. Elect J Biol. 2009; 5: 49–61.
7. Duffose L. Microbial production of food grade pigments, food grade pigments. Food Technol Biotechnol. 2006; 44: 313–321.
8. Tuli HS, Chaudhary P, Beniwal V, Sharma AK. Microbial pigments as natural color sources: current trends and future perspectives. J Food Sci Technol. 2015; 52: 4669–4678. doi: 10.1007/s13197-014-1601-6 26243889
9. Mapari SAS, Nielsen NKF, Larsen TO, Frisvad JC, Meyer AS, Thrane U. Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol. 2005; 16: 231–238. doi: 10.1016/j.copbio.2005.03.004 15831392
10. Arumugam GK, Srinivasan SK, Joshi G, Gopal D, Ramalingam K. Production and characterization of bioactive metabolites from piezotolerant deep sea fungus Nigrospora sp. in submerged fermentation. J Appl Microbiol. 2015; 118: 99–111. doi: 10.1111/jam.12693 25393321
11. Wheeler MH, Bell AA. Melanins and their importance in pathogenic fungi. Curr Top Med Mycol 1988; 2: 338–387. 3288360
12. Huang L, Liu M, Huang H, Wen Y, Zhang X, Wei Y. Recent advances and progress on melanin-like materials and their biomedical applications. Biomacromolecules. 2018; 19: 1858–1868. doi: 10.1021/acs.biomac.8b00437 29791151
13. Plonka PM, Grabacka M. Melanin synthesis in microorganisms−biotechnological and medical aspects. Acta Biochim Pol. 2006; 53: 429–443. 16951740
14. ElObeid AS, Kamal-Eldin A, Abdelhalim MAK, Haseeb AM. Pharmacological properties of melanin and its function in health. Basic Clin Phamacol Toxicol. 2017; 120: 515–522. doi: 10.1111/bcpt.12748 28027430
15. Gomez BL, Nosanchuk JD. Melanin and fungi. Curr Opin Infect Dis. 2003; 16: 91–96. doi: 10.1097/01.aco.0000065076.06965.04 12734441
16. Eisenman HC, Casadevall A. Synthesis and assembly of fungal melanin. Appl Microbial Biotechnol. 2012. 93: 931−940. doi: 10.1007/s00253-011-3777-2 22173481
17. Singaravelan N, Grishkan I, Beharav A, Wakamatsu K, Ito S, Nevo E. Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at “Evolution Canyon”, Mount Carmel, Israel. PLoS One. 2008; 3: e2993. doi: 10.1371/journal.pone.0002993 18714346
18. Turick C, Knox A, Leverette C, Kritzas Y. In situ uranium stabilization by microbial metabolites. J Enviro Radioact. 2008; 99: 890–899. doi: 10.1016/j.jenvrad.2007.11.020 18222573
19. Rao MPN, Xiao M, Li WJ. Fungal and bacterial pigments: secondary metabolites with wide applications. Front Microbial. 2017; 8: 1113. doi: 10.3389/fmicb.2017.01113 28690593
20. Langfelder K, Streibel M, Jahn B. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet Biol. 2003; 38: 143–158. 12620252
21. Ellis DH, Griffiths DA. The location and analysis of melanins in the cell walls of some soil fungi. Can J Microbiol. 1974; 20: 1379–1386. https://doi.org/10.1139/m74-212
22. Filip Z, Haider K, Beutelspacher H, Martin JP. Comparison of IR spectra from melanins of microscopic soil fungi, humic acids and model phenol polymers. Geoderma. 1974; 11:37–52. https://doi.org/10.1016/0016-7061(74)90005-6
23. Bell AA, Wheeler MH. Biosyntesis and functions of fungal melanins. Annu Rev Phytopathol. 1986; 24: 411–451. https://doi.org/10.1146/annurev.py.24.090186.002211
24. Hamada T, Asnagi M, Satozawa T, Araki N, Banba S, Higashinura N, Akase T, Hirase K. Action mechanism of the novel rice blast fungicide tolprocarb distinct from that of conventional melanin biosynthesis inhibitors. J Pestic Sci. 2014; 39: 152−158. https://doi.org/10.1584/jpestics.D14-033
25. Pal AK, Gajjar DU, Vasavada AR. DOPA and DHN pathway orchestrate melanin synthesis in Aspergillus species. Med Mycol. 2014; 52: 10−18. doi: 10.3109/13693786.2013.826879 23998343
26. Liu D.H., Wei L., Guo T. Detection of DOPA-melanin in the dimorphic fungal pathogen Penicillium marneffei and its effect on macrophage phagocytosis in vitro. PLoS One. 2014; 9: e92610. doi: 10.1371/journal.pone.0092610 24647795
27. De la Rosa JM, Martin-Sanchez PM, Sanchez-Cortes S, Hermosin B, Knicker H, Saiz-Jimenez C. Structure of melanins from the fungi Ochroconis lascauxensis and Ochroconis anomala contaminating rock art in the Lascaux Cave. Sci Rep. 2017; 7: 13441. PMCID: PMC5647350 doi: 10.1038/s41598-017-13862-7 29044220
28. Martin JP, Haider K. Phenolic polymers of Stachybotrys atra, Stachybotrys chartarum and Epicoccum nigrum in relation to humic acid formation. Soil Sci. 1969; 107:260–270. https://doi.org/10.1097/00010694-196904000-00005
29. Rajagopal K, Kathiravan G, Karthikeyan S. Extraction and characterization of melanin from Phomopsis: a phellophytic fungi isolated from Azadirachta indica A. Juss. Afr J Microbiol Res. 2011; 5: 762−766.
30. Zou Y, Hou X. Optimization of culture medium for production of melanin by Auricularia auricular. Food Sci Technol. 2017; 37: 153–157. http://dx.doi.org/10.1590/1678-457x.18016
31. Jacobson ES. Pathogenic roles for fungal melanins. Clin Microbiol Rev. 2000; 13: 708–717. doi: 10.1128/cmr.13.4.708-717.2000 11023965
32. Morris-Jones R, Gomez BL, Diez S, Uran M, Morris-Jones SD, Casadevall A, Nosanchuk JD, Hamilton AJ. Synthesis of melanin pigment by Candida albicans in vitro and during infection. Infect Immun. 2005; 73: 6147–6150. doi: 10.1128/IAI.73.9.6147-6150.2005 16113337
33. Gessler N, Egorova A, Belozerskaya T. Melanin pigments of fungi under extreme environmental conditions (review). Appl Biochem Microbiol. 2014; 50: 105–113. https://doi.org/10.1134/S0003683814020094. 25272728
34. Suwannarach N, Kumla J, Lumyong S. Spissiomyces endophytica (Dothideomycetes, Ascomycota), a new endophytic fungus from Thailand. Phytotaxa. 2018; 33: 219–227. https://doi.org/10.11646/phytotaxa.333.2.5
35. Hou R, Liu X, Xiang K, Chen L, Wu X, Lin W, Zheng M. Fu J. Characterization of the physicochemical properties and extraction optimization of natural melanin from Inonotus hispidus mushroom. Food Chem. 2019; 277: 533–542. doi: 10.1016/j.foodchem.2018.11.002 30502181
36. Wang H, Pan Y, Tang X, Huang Z. Isolation and characterization of melanin from Osmanthus fragrans’ seeds. LWT-Food Sci Technol. 2006; 39: 496–502. https://doi.org/10.1016/j.lwt.2005.04.001
37. Booner TG, Duncan A. Infra-red spectra of some melanins. Nature. 1962; 194: 1078–1079. doi: 10.1038/1941078a0 13871035
38. Kannan P, Ganjewala D. Preliminary characterization of melanin isolated from fruits and seed of Nyctanthes arbor-tritis. J Sci Res. 2009; 1: 6555–661.
39. Senesi N, Miano TM, Martin JP (1987) Elemental, funcional infrared and free radical characterization of humic acid-type fungal polymers (melanins). Biol Fertil Soils. 1987; 5: 120–125. https://doi.org/10.1007/BF00257646
40. Bridelli MG, Tampellini D, Zecca L. The structure of neuromelanin and its iron binding site studied by infrared spectroscopy. FEBS Lett. 1999; 457: 18–22. doi: 10.1016/s0014-5793(99)01001-7 10486555
41. Coates J. Interpretation of infrared spectra, a practical approach. In Mayers RA. Editor. Encyclopedia of Analytical Chemistry. Chichester: Jon Wiley & Sons LTd.; 2006. pp. 10815–10837.
42. Paim S, Linhares LF, Mangrich AS, Martim JP. Characterization of fungal melanins and soil humic acids by chemical analysis and infrared spectroscopy. Biol Fertil Soils. 1990; 10: 72–76. https://doi.org/10.1007/BF00336128
43. Drewnowska JM, Zambrzycka M, Kalska-Szostko B, Fiedoruk K, Swiecicka I. Melanin-like pigment synthesis by soil Bacillus weihenstephanensis isolated from northeastern Poland. PLoS One. 2015; 10: e0125428. doi: 10.1371/journal.pone.0125428 25909751
44. Chen SR, Jiang B, Zheng JJ, Xu GY, Li JY, Yang N. Isolation and characterization of natural melanin derived from silky fowl (Gallus gallus domesticus Brisson). Food Chem. 2008; 111: 745–749. https://doi.org/10.1016/j.foodchem.2008.04.053
45. Gonçalves RCR, Lisboa HCF, Pomberiro-Sponchiado SR. Characterization of melanin pigment produced by Aspergillus nidulans. World J Microbiol Biotechnol. 2012; 28: 1467–1474. doi: 10.1007/s11274-011-0948-3 22805928
46. Raman N.M., Shah PH, Mohan M, Ramasamy S. Improved production of melanin from Aspergillus fumigatus AFGRD105 by optimization of media factors. AMB Express. 2015; 5: 1–9. doi: 10.1186/s13568-015-0161-0 26597959
47. Suryanarayanan TS, Ravishankar JP, Venkatesan G, Murali TS. Characterization of the melanin pigment of a cosmopolitan fungal endophyte. Mycol Res. 2004; 108: 974–978. https://doi.org/10.1017/S0953756204000619 15449603
48. Zhan F, He Y, Zu Y, Li T, Zhao Z. Characterization of melanin isolated from a dark septate endophyte (DSE), Exophiala pisciphila. World Microbiol Biotechnol. 2011; 27: 2483–2489. https://doi.org/10.1007/s11274-011-0712-8
49. Selvakumar P, Rajasekar S, Periasamy K, Raaman N. Isolation and characterization of melanin pigment from Pleurotus cystidiosus (telomorph of Antromycopsis macrocarpa). World J Microbiol Biotechnol. 2008; 24: 2125–2131. doi: 10.1080/21501203.2018.1494060 PMID: 30533254
50. Zhang M, Xiao G, Thring RW, Chen W, Zhou H, Yang H. Production and characterization of melanin by submerged culture of culinary and medicinal fungi Auricularia auricula. Appl Biochem Biotechnol. 2015; 176: 253–266. doi: 10.1007/s12010-015-1571-9 25800528
51. Enochs WS, Nilges MJ, Swartz HM. A standardized test for the identification and characterization of melanins using electron paramagnetic resonance (EPR) spectroscopy. Pigment Cell Res. 1993; 6: 91–99. 8391699
52. Nosanchuk JD, Casadevall A. The contribution of melanin to microbial pathogenesis. Cell Microbiol. 2003; 5: 203–223. 12675679
53. Henson JM, Butler MJ, Day AW. The dark side of the mycelium: Melanins of phytopathogenic fungi. Annu Rev Phytopathol. 1999; 37: 447–471. doi: 10.1146/annurev.phyto.37.1.447 11701831
54. Revskaya E, Chu P, Howell RC, Schweitzer AD, Bryan RA, Harris M, Gerfen G, Jiang Z, Jandl T, Kim K, Ting LM, Sellers RS, Dadachova E, Casadevall A. Compton scattering by internal shields based on melanin-containing mushrooms provides protection of gastrointestinal tract from ionizing radiation. Cancer Biother Radiopharm. 2012; 27: 570–576. doi: 10.1089/cbr.2012.1318 23113595
55. Bull AT, Faulkner BM. Melanin synthesis in wild-type and mutant strains of Aspergillus nidulans. J Gen Microbiol. 1965; 41: iv
56. Wheeler MH, Klich MA. The effects of tricyclazole, pyroquilon, phthalide, and related fungicides on the production of conidial wall pigments by Penicillium and Aspergillus species. Pestic Biochem Physiol. 1995; 52: 125–136.
57. Saiz-Jimenez C. Microbial melanins in stone monuments. Sci Total Environ. 1995; 167: 273–286
58. Wu Y, Shan L, Yang S, Ma A. Identification and antioxidant activity of melanin isolated from Hypoxylon archeri, a companion fungus of Tremella fuciformis. J Basic Microbiol. 2008; 48: 217–221. doi: 10.1002/jobm.200700366 18506908
59. Sapmak A, Boyce KJ, Andrianopoulos A. The pbrB gene encodes a laccase required for DHN-melanin synthesis in conidia of Talaromyces (Penicillium) marneffei. PLoS One. 2015; 10: e0122728. doi: 10.1371/journal.pone.0122728 25866870
60. Panesar R, Kaur S, Panesar PS. Production of microbial pigments utilizing agro-industrial waste: a review. Curr Opin Food Sci. 2015; 1: 70–76. http://dx.doi.org/10.1016/j.cofs.2014.12.002.
61. Thaira H, Raval K, Balakrishnan RM. Optimizing the biosynthesis of melanin nanoparticles used for heavy metal removal. Res J Chem Environ Sci. 2016; 12–18.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania