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Applied Microbiology and Biotechnology

, Volume 103, Issue 17, pp 6973–6987 | Cite as

Optimization and characterization of red pigment production from an endophytic fungus, Nigrospora aurantiaca CMU-ZY2045, and its potential source of natural dye for use in textile dyeing

  • Nakarin Suwannarach
  • Jaturong Kumla
  • Yuzo Nishizaki
  • Naoki Sugimoto
  • Jomkwan Meerak
  • Kenji Matsui
  • Saisamorn LumyongEmail author
Biotechnological products and process engineering
  • 129 Downloads

Abstract

Some of the most important natural pigments have been produced from fungi and used for coloring in food, cosmetics, textiles, and pharmaceutical products. Forty-seven isolates of endophytic fungi were isolated from Cinnamomum zeylanicum in northern Thailand. Only one isolate, CMU-ZY2045, produced an extracellularly red pigment. This isolate was identified as Nigrospora aurantiaca based on morphological characteristics and the molecular phylogenetic analysis of a combined four loci (large subunit and internal transcribed spacer of ribosomal DNA, β-tubulin, and translation elongation factor 1-alpha genes). The optimum conditions for red pigment production from this fungus were investigated. The results indicated that the highest red pigment yield was observed in the liquid medium containing glucose as a carbon source and yeast extract as a nitrogen source, at a pH value of 5.0 and at 27 °C with shaking for 5 days. The crude red pigment revealed the highest level of solubility in methanol. A fungal red pigment was found to have high stability at temperatures ranging from 20 to 50 °C and pH values at a range of 5.0–6.0. Based on liquid chromatography-mass spectrometry analyses, the red pigment was characterized as bostrycin. The extracted pigment was used for the textile dyeing process. Crude fungal red pigment revealed the highest staining ability in cotton fabrics and displayed excellent fastness to washing, which showing negative cytotoxicity at the concentrations used to cell culture. This is the first report on bostrycin production from N. aurantiaca.

Keywords

Bostrycin Fungal pigment Solubility Stability Textile dye 

Notes

Acknowledgments

We are grateful to Mr. Russell K. Hollis for English proofreading.

Funding

This work was supported by grants from the Chiang Mai University, Center of Excellence on Biodiversity (BDC), Office of Higher Education Commission (BDC-PG2–159010), National Research Council of Thailand (NRCT) and Japan Society for the Promotion of Science (JSPS) in Core-to-Core Program (Establishment of an international research core for new bio-research fields with microbes from tropical area).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors

Supplementary material

253_2019_9926_MOESM1_ESM.pdf (301 kb)
ESM 1 (PDF 301 kb)

References

  1. Ahmad WA, Yusof NZ, Nordin N, Zakaria ZA, Rezali MF (2012) Production and characterization of violacein by locally isolated Chromobacterium violaceum grown in agricultural wastes. Appl Biochem Biotechnol 167:1220–1234.  https://doi.org/10.1007/s12010-012-9553-7 CrossRefGoogle Scholar
  2. Akilandeswari P, Pradeep BV (2016) Exploration of industrially important pigment from soil fungi. Appl Microbiol Biotechnol 100:1631–1643.  https://doi.org/10.1007/s00253-015-7231-8 CrossRefGoogle Scholar
  3. Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov Chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266CrossRefGoogle Scholar
  4. Anchana devi A (2014) Extraction of natural dyes from fungus-an alternate for textile dyeing. J Nat Sci Res 4:1–6Google Scholar
  5. Arumugam GK, Srinivasan SK, Joshi G, Gopal D, Ramalingam K (2014) Production and characterization of bioactive metabolites from piezotolerant deep sea fungus Nigrospora sp. in submerged fermentation. J Appl Microbiol 118:99–111.  https://doi.org/10.1111/jam.12693 CrossRefGoogle Scholar
  6. Babitha S, Soccol CR, Pandey A (2007) Solid-state fermentation for the production of Monascus pigment from jack fruit seed. Bioresour Technol 98:1554–1560.  https://doi.org/10.1016/j.biortech.2006.06.005 CrossRefGoogle Scholar
  7. Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556Google Scholar
  8. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB (1987) Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 47:936–942Google Scholar
  9. Chadni Z, Rahaman MH, Jerin I, Hoque KMF, Reza MA (2017) Extraction and optimization of red pigment production as secondary metabolites from Talaromyces verruculosus and potential use in textile industries. Mycology 8:48–57.  https://doi.org/10.1080/21501203.2017.1302013 CrossRefGoogle Scholar
  10. Charudattan R, Rao KV (1982) Bostrycin and 4-deoxybostrycin: two nonspecific phytotoxins produced by Alternaria eichhorniae. Appl Environ Microbiol 43:846–849Google Scholar
  11. Chen CQ, Fang LK, Liu JW, Zhang JW, Yang GG, Yang W (2010) Effects of marine fungal metabolites (1386A) from the South China Sea on proliferation, apoptosis and membrane potential of gastric cancer cell line MCG-803. Chin J Pathophysiol 26:1908–1912Google Scholar
  12. Chen WS, Hou JN, Guo YB, Yang HL, Xie CM, Lin YC, She ZG (2011) Bostrycin inhibits proliferation of human lung carcinoma A549 cells via downregulation of the Pl3K/Akt pathway. J Exp Clin Cancer Res 30:17.  https://doi.org/10.1186/1756-9966-30-17 CrossRefGoogle Scholar
  13. Cho YJ, Park JP, Hwang HJ, Kim SW, Choi JW, Yun JW (2002) Production of red pigment by submerged culture of Paecilomyces sinclairii. Lett Appl Microbiol 35:195–202.  https://doi.org/10.1046/j.1472-765X.2002.01168.x CrossRefGoogle Scholar
  14. Deshmukh SK, Verekar SA, Bhave SV (2014) Endophytic fungi: a reservoir of antibacterials. Front Microbiol 5:715.  https://doi.org/10.3389/fmicb.2014.00715 Google Scholar
  15. Devi S, Karuppan P (2015) Reddish brown pigment from Alternaria alternata for textile dyeing and printing. Indian J Fibre Text Res 40:315–319Google Scholar
  16. Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC, Ravishankar GA (2005) Microorganism and microalgae as source of pigments for food use: a scientific oddity or an industrial reality. Trends Food Sci Technol 16:389–406.  https://doi.org/10.1016/j.tifs.2005.02.006 CrossRefGoogle Scholar
  17. Dufossé L, Fouille M, Caro Y, Mapari SAS, Sutthiwong N (2014) Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr Opin Biotechnol 26:56–61.  https://doi.org/10.1016/j.copbio.2013.09.007 CrossRefGoogle Scholar
  18. Durán N, Teixeira MFS, Conti RD, Esposito E (2002) Ecological-friendly pigmentts from fungi. Crit Rev Food Sci Nutr 42:53–66.  https://doi.org/10.1080/10408690290825457 CrossRefGoogle Scholar
  19. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  20. Fuoillaud M, Venkatachalam M, Girard-Valenciennes E, Caro Y, Dufossé L (2016) Anthraquinones and derivatives from marine-derived fungi: structure diversity and selected biological activities. Mar Drugs 14:64.  https://doi.org/10.3390/md14040064 CrossRefGoogle Scholar
  21. Glass LN, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330Google Scholar
  22. Hailei W, Zhifang R, Ping L, Yanchang G, Guosheng L, Jianming Y (2011) Improvement of the production of a red pigment in Penicillium sp. HSD07B synthesized during co-culture with Candida tropicalis. Bioresour Technol 102:6082–6087.  https://doi.org/10.1016/j.biortech.2011.01.040 CrossRefGoogle Scholar
  23. Hernández VA, Galleguillos F, Thibaut R, Müller A (2019) Fungal dyes for textile applications: testing of industrial conditions for wool fabrics dyeing. J Text Inst 110:61–66.  https://doi.org/10.1080/00405000.2018.1460037 CrossRefGoogle Scholar
  24. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192CrossRefGoogle Scholar
  25. Hinsch EM, Chen HL, Weber G, Robinson SC (2015) Colorfastness of extracted wood-staining fungal pigments on fabrics: a new potential of textile dyes. J Text Appar Technol Manag 9:1–11Google Scholar
  26. Huang X, Sun X, Lin S, Xiao Z, Li H, Bo D, She Z (2014) Xylanthraquinone, a new anthraquinone from the fungus Xylaria sp. 2508 from the South China Sea. Nat Prod Res 28:111–114.  https://doi.org/10.1080/14786419.2013.850687 CrossRefGoogle Scholar
  27. Huang YH, Yang WJ, Cheng CY, Sung HM, Lin SF (2017) Bostrycin production by agro-industrial residues and its potential for food processing. Food Sci Biotechnol 26:715–721.  https://doi.org/10.1007/s10068-017-0082-6 CrossRefGoogle Scholar
  28. Joshi V, Attri D, Bala A, Bhushan S (2003) Microbial pigments. Indian J Biotechnol 2:362–369Google Scholar
  29. Kaur S, Arora N, Kaur S (2017) Characterization of yellow pigments produced by Pencillium sp. under solid state cultivation. J Biotechnol Biomater 7(259).  https://doi.org/10.4172/2155-952X.1000259
  30. Kornerup A, Wanscher JH (1967) Methuen handbook of colour, 2nd edn. Eyre Methuen, LondonGoogle Scholar
  31. Kramar A, Ilic-Tomic T, Petkovic M, Radulović N, Kostic M, Jocic D, Nikodinovic-Runic J (2014) Crude bacterial extracts of two new Streptomyces sp. isolates as bio-colorants for textile dyeing. World J Mirobiol Biotechnol 30:2231–2240.  https://doi.org/10.1007/s11274-014-1644-x CrossRefGoogle Scholar
  32. Kumar A, Vishwakarma HS, Singh J, Dwivedi S, Kumar M (2015) Microbial pigments: production and their application in various industries. IJPCBS 5:203–212Google Scholar
  33. Latha BV, Jeevaratnam K (2010) Purification and characterization of the pigments from Rhodotorula glutinis DFR-PDY isolated from natural source. Global J Biotechnol Biochem 5:166–174Google Scholar
  34. Lebeau J, Venkatachlam M, Fouillaud M, Petit T, Vinale F, Dufossé CY (2017) Production and new extraction method of polyketide red pigments produced by ascomycetous fungi from terrestrial and marine habitats. J Fungi 3:34.  https://doi.org/10.3390/jof3030034 CrossRefGoogle Scholar
  35. Lin W, Fang LK, Liu JW, Cheng WQ, Yun M, Yang HL (2008) Inhibitory effects of marine fungal metabolites from the South China Sea on prostate cancer cell line DU-145. Int J Intern Med 35:562–564Google Scholar
  36. Mabrouk AM, El-Khrisy EAM, Youssef YA, Asem MA (2011) Production of textile reddish brown dyes by fungi. Malaysian J Microbiol 7:33–40Google Scholar
  37. Malik K, Tokkas J, Goyal S (2012) Microbial pigment: a review. Int J Microbial Resour Technol 1:361–365Google Scholar
  38. Mapari SAS, Nielsen KF, Larsen TO, Frisvad JC, Meyer AS, Thrane U (2005) Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol 16:231–238.  https://doi.org/10.1016/j.copbio.2005.03.004 CrossRefGoogle Scholar
  39. Méndez A, Pérez C, Montanéz JC, Martínez G, Aguilar CN (2011) Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J Zhejiang Univ Sci B 12:961–968.  https://doi.org/10.1631/jzus.B1100039 CrossRefGoogle Scholar
  40. Nagia FA, El-Mohamedy RSR (2007) Dyeing of wool with natural anthraquinone dyes from Fusarium oxysporum. Dyes Pigments 75:550–555.  https://doi.org/10.1016/j.dyepig.2006.07.002 CrossRefGoogle Scholar
  41. Narendrababu BN, Shishupala S (2017) Spectrophotometric detection of pigments from Aspergillus and Penicillium isolates. J Appl Biol Biotechnol 5:53–58.  https://doi.org/10.7324/JABB.2017.50109 CrossRefGoogle Scholar
  42. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044–2049.  https://doi.org/10.1073/pnas.95.5.2044
  43. Osman MY, Sharaf IA, Osman HM, El-Khouly ZA, Ahmed EI (2004) Synthetic organic food colouring agents and their degraded products: effects on human and rat cholinesterases. Br J Biomed Sci 61:128–132.  https://doi.org/10.1080/09674845.11732657 CrossRefGoogle Scholar
  44. Page RD (2001) TreeView. Glasgow University, GlasgowGoogle Scholar
  45. Palomino AME, Vega GSM, Chen HL, Robinson SC (2017) Wood-rotting fungal pigments as colorant coating on oil-based textile dyes. Coatings 7:152.  https://doi.org/10.3390/coatings7100152 CrossRefGoogle Scholar
  46. Pandey N, Jain R, Pandey A, Tamta S (2018) Optimisation and characterisation of the orange pigment produced by a cold adapted strain of Penicillium sp. (GBPI_P155) isolated from mountain ecosystem. Mycology 9:81–92.  https://doi.org/10.1080/21501203.2017.1423127 CrossRefGoogle Scholar
  47. Panesar R, Kaur S, Panesar PS (2015) Production of microbial pigments utilizing agro-industrial waste: a review. Curr Opin Food Sci 1:70–76.  https://doi.org/10.1016/j.cofs.2014.12.002 CrossRefGoogle Scholar
  48. Perumal K, Stalin V, Chandrasekarenthiran S, Sumathi E, Saravanakumar A (2009) Extraction and characterization of pigment from Sclerotinia sp. and its use in dyeing cotton. Text Res J 79:1178–1187.  https://doi.org/10.1177/0040517508087680 CrossRefGoogle Scholar
  49. Poorniammal R, Manickam P, Gunasekaran S, Murugesan R, Thilagavathi G (2010) Natural dye production from Thermomyces sp. fungi for textile application. Indian J Fibre Text Res 38:276–279Google Scholar
  50. Pradeep FS, Begam MS, Palaniswamy M, Pradeep BV (2013) Influence of culture media on growth and pigment production by Fusarium moniliforme KUMBF1201 isolated from paddy field soil. World Appl Sci J 22:70–77.  https://doi.org/10.5829/idosi.wasj.2013.22.01.7265 Google Scholar
  51. Qui M, Xie R, Shi Y, Chen H, Wen Y, Gao Y, Hu X (2010) Isolation and identification of endophytic fungus SX01, a red pigment producer from Ginkgo biloba L. World J Microbiol Biotechnol 26:993–998.  https://doi.org/10.1007/s11274-009-0261-6 CrossRefGoogle Scholar
  52. Robinson SC, Tudor D, Zhang WR, Ng S, Cooper PA (2013) Ability of three yellow pigment producing fungi to colour wood under controlled conditions. Int Wood Prod J 5:103–107.  https://doi.org/10.1179/2042645313Y.0000000060 CrossRefGoogle Scholar
  53. Robinson SC, Hinsch E, Weber G, Freitas S (2014) Method of extraction and resolubilisation of pigments from Chlorociboria aeruginosa and Scytalidium cuboideum, two prolific spalting fungi. Color Technol 130:221–225.  https://doi.org/10.1111/cote.12080 CrossRefGoogle Scholar
  54. Rokade MT, Pethe DAS (2016) Isolation and identification of chromogenic bacteria from various sources. EJPMR 3:295–299Google Scholar
  55. Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefGoogle Scholar
  56. Sastrawidana IDK, Maryam SY, Sukarta IN (2016) Natural dyeing of silk and cotton fabric with red pigment from Penicillium purpurogenus which is isolated from goat milk contaminated soil. J Nat Sci Res 6:32–37Google Scholar
  57. Sharma D, Gupta C, Aggarwal S, Nagpal N (2012) Pigment extraction from fungus for textile dyeing. Indian J Fiber Text Res 37:68–73Google Scholar
  58. Souza PNC, Grigoletto TLB, de Moraes LAB, Abreu LM, Guimarães LHS, Santos C, Galvão LR, Cardoso PG (2016) Production and chemical characterization of pigments in filamentous fungi. Microbiology 162:12–22.  https://doi.org/10.1099/mic.0.000168 CrossRefGoogle Scholar
  59. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefGoogle Scholar
  60. Suemitsu R, Nakamura A (1981) Isolation and identification of altersolanol a from the culture liquid of Alternaria porri (Ellis) Ciferri. Agric Biol Chem 45:2363–2364.  https://doi.org/10.1080/00021369.1981.10864889 Google Scholar
  61. Thomson RH (1987) Naturally occurring Quinones III: recent advances. Chapman and Hall, LondonGoogle Scholar
  62. Torres FAE, Zaccarim BR, Novaes LCL, Jozala AF, Santos CA, Teixeira MFS, Santos-Ebinuma VC (2016) Natural colorants from filamentous fungi. Appl Microbial Biotechnol 100:2511–2521.  https://doi.org/10.1007/s00253-015-7274-x CrossRefGoogle Scholar
  63. Trisuwan K, Khamthong N, Rukachaisirikul V, Phongpaichit S, Preedanon S, Sakayaroj J (2010) Anthraquinone cyclopentanone and naphthoquinone derivatives from the sae fan-derived fungi Fusarium spp. PSU-F14 and PSU-F135. J Nat Prod 73:1507–1511.  https://doi.org/10.1021/np100282k CrossRefGoogle Scholar
  64. Tseng YY, Chen MT, Lin CF (2000) Growth, pigment production and protease activity of Monascus purpureus as affected by salt, sodium nitrite, polyphosphate and various sugars. J Appl Microbiol 88:31–37.  https://doi.org/10.1046/j.1365-2672.2000.00821.x
  65. Tudor D, Robinson SC, Cooper PA (2013) The influence of pH on pigment formation by lignicolous fungi. Int Biodeterior Biodegradation 80:22–28.  https://doi.org/10.1016/j.ibiod.2012.09.013 CrossRefGoogle Scholar
  66. Unagul P, Wongsa P, Kittakoop P, Intamas S, Srikitikulchai P, Tanticharoen M (2005) Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis BCC1869. J Ind Microbiol Biotechnol 32:135–140.  https://doi.org/10.1007/s10295-005-0213-6 CrossRefGoogle Scholar
  67. van Eijk GW (1975) Bostrycin, a tetrahydroanthraquinone pigment and some other metabolites from the fungus Arthrinium phaeospermum. Experientia 31:783–784CrossRefGoogle Scholar
  68. Velmurugan P, Kamala-Kannan S, Balachandar V, Lakshmanaperumalsamy P, Chae JC, Oh BT (2010) Natural pigment extraction from five filamentous fungi for industrial applications and dyeing of leather. Carbohydr Polym 79:262–268.  https://doi.org/10.1016/j.carbpol.2009.07.058 CrossRefGoogle Scholar
  69. Venil CK, Lakshmanaperumalsamy P (2009) An insightful overview on microbial pigment, prodigiosin. Electron J Biol 5:49–61Google Scholar
  70. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246.  https://doi.org/10.1128/jb.172.8.4238-4246.1990
  71. Wang M, Lui F, Crous PW, Cai L (2017) Phylogenitic reassessment of Nigrospora: ubiquitous endophytes, plant and human pathogens. Persoonia 39:118–142.  https://doi.org/10.3767/persoonia.2017.39.06 CrossRefGoogle Scholar
  72. Wheeler MM, Wheeler DMS, Peterson GW (1975) Anthraquinone pigments from the phytopathogen Phomopsis juniperovora hahn. Phytochemistry 14:288–289.  https://doi.org/10.1016/0031-9422(75)85060-6 CrossRefGoogle Scholar
  73. White TJ, Burns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. in: Innis MA, Gelfand DH, Sninsky JJ, Whitish TJ (Eds.) PCR protocols, a guide to methods and applications. Academic Press, San Diego.  https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  74. Wolf S, Schmidt S, Müller-Hannemann M, Neumann S (2010) In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics 11:148.  https://doi.org/10.1186/1471-2105-11-148 CrossRefGoogle Scholar
  75. Wongjewboot I, Kongruang S (2011) pH stability of ultrasonic Thai isolated Monascus purpureus pigments. IJBBB 1:79–83CrossRefGoogle Scholar
  76. Xia X, Li Q, Li J, Shao C, Zhang J, Zhang Y, Liu X, Lin Y, Liu C, She Z (2011) Two new derivatives of griseofulvin from the mangrove endophytic fungus Nigrospora sp. (strain no. 1403) from Kandelia candel (L.) Druce. Planta Med 77:1735–1738.  https://doi.org/10.1055/s-0030-1271040 CrossRefGoogle Scholar
  77. Yagi A, Okamura N, Haraguchi H, Abo T, Hashimoto K (1993) Antimicrobial tetrahydroanthraquinones from a strain of Alternaria silani. Phytochemistry 33:87–91.  https://doi.org/10.1016/0031-9422(93)85401-C CrossRefGoogle Scholar
  78. Yang WJ, Yang CS, Huang CJ, Chen KS, Lin SF (2012) Bostrycin, a novel coupling agent protein immobilization and prevention of biomaterial-cantered infection produced by Nigrospora sp. Enzym Microb Technol 50(407):287–292.  https://doi.org/10.1016/j.enzmictec.2012.02.002 CrossRefGoogle Scholar
  79. Zhou Z, Guo H, Xie C (2015) Effect of culture conditions on production of red pigment and citrinin by fermentation of Monascus ruber. Chem Eng Trans 46:1363–1368.  https://doi.org/10.3303/CET1546228 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nakarin Suwannarach
    • 1
    • 2
  • Jaturong Kumla
    • 1
    • 2
  • Yuzo Nishizaki
    • 3
  • Naoki Sugimoto
    • 3
  • Jomkwan Meerak
    • 1
  • Kenji Matsui
    • 4
  • Saisamorn Lumyong
    • 1
    • 2
    • 5
    Email author
  1. 1.Department of Biology, Faculty of ScienceChiang Mai UniversityChiang MaiThailand
  2. 2.Center of Excellence in Microbial Diversity and Sustainable UtilizationChiang Mai UniversityChiang MaiThailand
  3. 3.Division of Food AdditivesNational Institute of Health SciencesKanagawaJapan
  4. 4.Graduate School of Science and Technology for Innovation, Faculty of AgricultureYamaguchi UniversityYamaguchiJapan
  5. 5.The Royal Society of ThailandAcademy of ScienceBangkokThailand

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