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Unveiling the Bioprospecting Efficacy and Textile Dyeing of a Novel Endophytic Mycobial Red Pigment

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Abstract

Natural pigments are becoming increasingly popular owing of their reliability. Microbial pigments provide an alternative to natural colours. A total of 24 fungal cultures were collected from leaf bits of Senna auriculata, with one strain (FNG1) producing an extracellular red orange pigment. Nigrospora oryzae was confirmed by using physical criteria and molecular phylogenetic study by using ITS and β- tubulin analysis. In EtOAc, the crude red pigment was the most soluble. The TLC analysis was used to partly purify the natural pigment. The partially purified fungal pigment was used in successive bioprospecting studies. The antimicrobial activity of the partially purified sample was assessed against eight human pathogens, with Leucobacter AA7 showing the largest zone of inhibition (200–500 µg/mL). The compound's DPPH scavenging activity enhanced from 38.2 to 67.9%, with an IC50 value of 34.195 ± 2.33 µg/mL. Cancer cells were suppressed by partly pure fungal pigment, but non-cancerous HEK 293 cells were unaffected. The GC–MS analysis was used to characterize the molecule present in the partly purified pigment. In addition, the cotton textiles have the greatest staining capability for crude mycobial pigment, which dyes quickly and has a negative cytotoxicity.

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6 References

  1. Samanta AK, Agarwal P (2009) Application of natural dyes on textiles 34:384–399

  2. Narsing Rao MP, Xiao M, Li WJ (2007) Fungal and bacterial pigments: secondary metabolites with wide applications. Front Microbiol 8:1113

    Article  Google Scholar 

  3. Garber LL Jr, Hyatt EM, Nafees L (2016) The effects of food color on perceived flavor: a factorial investigation in India. J Food Prod Mark 22(8):930–948

    Article  Google Scholar 

  4. Elliot AJ, Maier MA (2014) Color psychology: effects of perceiving color on psychological functioning in humans. Annu Rev Psychol 65:95–120

    Article  PubMed  Google Scholar 

  5. Mukherjee G, Mishra T, Deshmukh SK (2017) Fungal pigments: an overview. Dev Fungal Biol Appl Mycol 525–541

  6. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM (2006) Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr 46(2):185–196

    Article  PubMed  CAS  Google Scholar 

  7. Babitha S, Soccol CR, Pandey A (2007) Effect of stress on growth, pigment production and morphology of Monascus sp. in solid cultures. J Basic Microbiol 47(2):118–126

    Article  PubMed  CAS  Google Scholar 

  8. Fouillaud M, Venkatachalam M, Girard-Valenciennes E, Caro Y, Dufossé L (2016) Marine-derived fungi producing red anthraquinones: new resources for natural colors?. In: 8th international conference of pigments in food, “coloured foods for health benefits”.

  9. Chen W, Chen R, Liu Q, He Y, He K, Ding X, Kang L, Guo X, Xie N, Zhou Y, Lu Y (2017) Orange, red, yellow: biosynthesis of azaphilone pigments in Monascus fungi. Chem Sci 8(7):4917–4925

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Durán N, Teixeira MF, De Conti R, Esposito E (2002) Ecological-friendly pigments from fungi. Crit Rev Food Sci Nutr 42(1):53–66

    Article  PubMed  Google Scholar 

  11. Ramesh C, Vinithkumar NV, Kirubagaran R, Venil C, Dufossé L (2019) Multifaceted applications of microbial pigments: current knowledge, challenges and future directions for public health implications. Microorganisms 7(7):186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Atalla MM, Elkhrisy EAM, Youssef YA, Mohamed AA (2011) Production of textile reddish brown dyes by fungi. Malay J Microbiol 7(1):33–40

    Google Scholar 

  13. Meruvu H, Dos Santos JC (2021) Colors of life: a review on fungal pigments. Crit Rev Biotechnol 41(8):1153–1177

    Article  PubMed  Google Scholar 

  14. Kunwar A, Adhikary B, Jayakumar S, Barik A, Chattopadhyay S, Raghukumar S, Priyadarsini KI (2021) Melanin, a promising radioprotector: Mechanisms of actions in a mice model. Toxicol Appl Pharmacol 264(2):202–211

    Article  Google Scholar 

  15. Feng Y, Shao Y, Zhou Y, Chen W, Chen F (2016) Monascus pigments. Ind Biotechnol Vit Biopigm Antioxidants 497–535

  16. Mapari SA, Thrane U, Meyer AS (2010) Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol 28(6):300–307

    Article  PubMed  CAS  Google Scholar 

  17. Venil CK, Velmurugan P, Dufossé L, Renuka Devi P, Veera Ravi A (2020) Fungal pigments: potential coloring compounds for wide ranging applications in textile dyeing. J Fungi 6(2):68

    Article  CAS  Google Scholar 

  18. Sundaresan N, Jagan EG, Kathamuthu G, Pandi M (2019) Internal transcribed spacer 2 (ITS2) molecular morphometric analysis based species delimitation of foliar endophytic fungi from Aglaia elaeagnoidea, Flacourtia inermis and Premna serratifolia. PLoS ONE 14(4):e0215024

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Cenis JL (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20(9):2380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols Guide Methods Appl 18(1):315–322

    Google Scholar 

  21. Ankenbrand MJ, Keller A, Wolf M, Schultz J, Förster F (2015) ITS2 database V: Twice as much. Mol Biol Evol 32(11):3030–3032

    Article  PubMed  CAS  Google Scholar 

  22. Schliep PKP (2011) phylogenetics analysis in R. Bioinformatics 27(4):592–593

    Article  MathSciNet  PubMed  CAS  Google Scholar 

  23. Raj KG, Manikandan R, Arulvasu C, Pandi M (2015) Anti-proliferative effect of fungal taxol extracted from Cladosporium oxysporum against human pathogenic bacteria and human colon cancer cell line HCT 15. Spectrochim Acta Part A Mol Biomol Spectrosc 138:667–674

    Article  ADS  Google Scholar 

  24. 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

    Article  PubMed  CAS  Google Scholar 

  25. Perez C (1990) Antibiotic assay by agar-well diffusion method. Acta Biol Med Exp 15:113–115

    Google Scholar 

  26. Nuerxiati R, Abuduwaili A, Mutailifu P, Wubulikasimu A, Rustamova N, Jingxue C, Aisa HA, Yili A (2019) Optimization of ultrasonic-assisted extraction, characterization and biological activities of polysaccharides from Orchis chusua D. Don (Salep). Int J Biol Macromol 141:431–443

    Article  PubMed  CAS  Google Scholar 

  27. Oyaizu M (1986) Studies on products of browning reaction antioxidative activities of products of browning reaction prepared from glucosamine. Jpn J Nutrit Dietet 44(6):307–315

    Article  CAS  Google Scholar 

  28. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1–2):55–63

    Article  PubMed  CAS  Google Scholar 

  29. Gohel A, McCarthy MB, Gronowicz G (1999) Estrogen prevents glucocorticoid-induced apoptosis in osteoblasts in vivo and in vitro. Endocrinology 140(11):5339–5347

    Article  PubMed  CAS  Google Scholar 

  30. Kim HW, Wang M, Leber CA, Nothias LF, Reher R, Kang KB, Cottrell GW (2021) NPClassifier: A deep neural network-based structural classification tool for natural products. J Natl Prod 84(11):2795–2807

    Article  CAS  Google Scholar 

  31. Kannathasan K, Kokila P (2021) Dyeing of cotton fabric by Caesalpinia sappan aqueous extract at different temperatures and mordants. Curr Bot 12:188–191

    Article  CAS  Google Scholar 

  32. Westphal KR, Wollenberg RD, Herbst FA, Sørensen JL, Sondergaard TE, Wimmer R (2018) Enhancing the production of the fungal pigment aurofusarin in Fusarium graminearum. Toxins 10(11):485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Nille GC, Mishra SK, Chaudhary AK, Reddy KRC (2021) Ethnopharmacological, phytochemical, pharmacological, and toxicological review on Senna auriculata (L) Roxb: a special insight to antidiabetic property. Front Pharmacol 2180

  34. 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. Carbohyd Polym 79(2):262–268

    Article  CAS  Google Scholar 

  35. Arumugam GK, Srinivasan SK, Joshi G, Gopal D, Ramalingam K (2015) Production and characterization of bioactive metabolites from piezotolerant deep sea fungus Nigrospora sp. in submerged fermentation. J Appl Microbiol 118(1):99–111

    Article  PubMed  CAS  Google Scholar 

  36. Torres FAE, Zaccarim BR, de Lencastre Novaes LC, Jozala AF, Santos CAD, Teixeira MFS, Santos-Ebinuma VC (2016) Natural colorants from filamentous fungi. Appl Microbiol Biotechnol 100:2511–2521

    Article  PubMed  CAS  Google Scholar 

  37. Lebeau J, Venkatachalam M, Fouillaud M, Petit T, Vinale F, Dufossé L, Caro Y (2017) Production and new extraction method of polyketide red pigments produced by ascomycetous fungi from terrestrial and marine habitats. J Fungi 3(3):34

    Article  Google Scholar 

  38. Suwannarach N, Kumla J, Nishizaki Y, Sugimoto N, Meerak J, Matsui K, Lumyong S (2019) 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. Appl Microbiol Biotechnol 103:6973–6987

    Article  PubMed  CAS  Google Scholar 

  39. Mishra R, Kalra R, Dilawari R, Deshmukh SK, Barrow CJ, Goel M (2021) Characterization of an endophytic strain Talaromyces assiutensis, CPEF04 with evaluation of production medium for extracellular red pigments having antimicrobial and anticancer properties. Front Microbiol 12:665702

    Article  PubMed  PubMed Central  Google Scholar 

  40. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium, Fungal Barcoding Consortium Author List, Bolchacova E, Voigt K (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109(16):6241–6246

    Article  ADS  Google Scholar 

  41. da Costa N, Souza P, Luiza Bim Grigoletto T, Beraldo A, de Moraes L, Abreu LM, Henrique Souza Guimarães L, Santos C, Ribeiro Galvão L, Gomes Cardoso P (2016) Production and chemical characterization of pigments in filamentous fungi. Microbiology 162(1):12–22

    Article  Google Scholar 

  42. Narendrababu BN, Shishupala S (2017) Spectrophotometric detection of pigments from aspergillus and penicillium isolates. J Appl Biol Biotechnol 5(1):053–058

    Article  CAS  Google Scholar 

  43. El-Sayed ESR, Gach J, Olejniczak T, Boratyński F (2022) A new endophyte Monascus ruber SRZ112 as an efficient production platform of natural pigments using agro-industrial wastes. Sci Rep 12(1):12611

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  44. Pawle G, Singh SK (2014) Antimicrobial, antioxidant activity and phytochemical analysis of an endophytic species of Nigrospora isolated from living fossil Ginkgo biloba. Curr Res Environ Appl Mycol 4(1):1–9

    Article  Google Scholar 

  45. Singh N, Rajini PS (2004) Free radical scavenging activity of an aqueous extract of potato peel. Food Chem 85(4):611–616

    Article  CAS  Google Scholar 

  46. Khalil D, El-Zayat SA, El-Sayed MA (2020) Phytochemical screening and antioxidant potential of endophytic fungi isolated from Hibiscus sabdariffa. J Appl Biotechnol Rep 7(2):116–124

    CAS  Google Scholar 

  47. Xing R, Yu H, Liu S, Zhang W, Zhang Q, Li Z, Li P (2005) Antioxidant activity of differently regioselective chitosan sulfates in vitro. Bioorg Med Chem 13(4):1387–1392

    Article  PubMed  CAS  Google Scholar 

  48. Salvador-Reyes LA, Engene N, Paul VJ, Luesch H (2015) Targeted natural products discovery from marine cyanobacteria using combined phylogenetic and mass spectrometric evaluation. J Nat Prod 78(3):486–492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Elkhouly HI, Hamed AA, El Hosainy AM, Ghareeb MA, Sidkey NM (2021) Bioactive secondary metabolite from endophytic Aspergillus tubenginses ASH4 isolated from Hyoscyamus muticus: antimicrobial, antibiofilm, antioxidant and anticancer activity. Pharmacognosy J 13(2)

  50. Lu Y, Chen C, Chen H, Zhang J, Chen W (2012) Isolation and identification of endophytic fungi from Actinidia macrosperma and investigation of their bioactivities. Evidence-based complementary and alternative medicine

  51. Taritla S, Kumari M, Kamat S, Bhat SG, Jayabaskaran C (2021) Optimization of physicochemical parameters for production of cytotoxic secondary metabolites and apoptosis induction activities in the culture extract of a marine algal-derived endophytic fungus Aspergillus sp. Front Pharmacol 12:542891

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Navya PN, Kaphle A, Srinivas SP, Bhargava SK, Rotello VM, Daima HK (2019) Current trends and challenges in cancer management and therapy using designer nanomaterials. Nano Convergence 6:1–30

    Article  CAS  Google Scholar 

  53. Polapally R, Mansani M, Rajkumar K, Burgula S, Hameeda B, Alhazmi A, Bantun F, Almalki AH, Haque S, El Enshasy HA, Sayyed RZ (2022) Melanin pigment of Streptomyces puniceus RHPR9 exhibits antibacterial, antioxidant and anticancer activities. PLoS ONE 17(4):e0266676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Aji N, Kumala S, Mumpuni E, Rahmat D (2022) Antibacterial activity and active fraction of Zingiber officinale Roscoe, Zingiber montanum (J. Koenig) link ex A., and Zingiber zerumbet (L.) roscoe ex sm against propionibacterium acnes. Pharmacognosy J 14(1)

  55. Olasehinde TA, Odjadjare EC, Mabinya LV, Olaniran AO, Okoh AI (2019) Chlorella sorokiniana and Chlorella minutissima exhibit antioxidant potentials, inhibit cholinesterases and modulate disaggregation of β-amyloid fibrils. Electron J Biotechnol 40:1–9

    Article  CAS  Google Scholar 

  56. Ren J, Wang J, Karthikeyan S, Liu H, Cai J (2019) Natural anti-phytopathogenic fungi compound phenol, 2, 4-bis (1, 1-dimethylethyl) from Pseudomonas fluorescens TL-1. Indian J Biochem Biophys 56(2):162–168

    CAS  Google Scholar 

  57. Arokiyaraj S, Bharanidharan R, Agastian P, Shin H (2018) Chemical composition, antioxidant activity and antibacterial mechanism of action from Marsilea minuta leaf hexane: methanol extract. Chem Cent J 12(1):1–11

    Article  Google Scholar 

  58. El-Fayoumy EA, Shanab SM, Gaballa HS, Tantawy MA, Shalaby EA (2021) Evaluation of antioxidant and anticancer activity of crude extract and different fractions of Chlorella vulgaris axenic culture grown under various concentrations of copper ions. BMC Complem Med Therapies 21(1):1–16

    Article  Google Scholar 

  59. Eid K, El-Sayed AN, Shoala T (2018) Gas chromatography-mass spectrometry (GC-MS) analysis of sugar beet leaf extracts in response to exogenous application of resistance inducers to manage sugar beet powdery mildew. Egypt J Phytopathol 46(1):257–277

    Article  Google Scholar 

  60. Ganesh M, Mohankumar M (2017) Extraction and identification of bioactive components in Sida cordata (Burm. f.) using gas chromatography–mass spectrometry. J Food Sci Technol 54:3082–3091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Tyagi T, Agarwal M (2017) Research article antioxidant properties and phenolic compounds in methanolic extracts of Eichhornia crassipes. Res J Phytochem 11:85–89

    Article  CAS  Google Scholar 

  62. Salim SA (2018) In vitro induction of callus from different explants ofterminalia arjuna (roxb) Wight and arn. And detection of its active secondary metabolites using gc-ms analysis. Plant Arch 18(2):2519–2527

    Google Scholar 

  63. Mannaa M, Kim KD (2018) Biocontrol activity of volatile-producing Bacillus megaterium and Pseudomonas protegens against Aspergillus and Penicillium spp. predominant in stored rice grains: study II. Mycobiology 46(1):52–63

    Article  PubMed  PubMed Central  Google Scholar 

  64. Abed RM, Salman MD (2022) Chemical composition ethanol and methanol extract of lycoperdon pyriforme. Int J Health Sci 6(S1):13749–13760

    Google Scholar 

  65. Sami SA (2022) New insights into the identification of bioactive compounds from Willughbeia edulis Roxb. through GC–MS analysis. Beni-Suef Univ J Basic Appl Sci 11(1):89

    Article  MathSciNet  Google Scholar 

  66. Zubairu A, Mshelia YM (2015) Effects of selected mordants on the application of natural dye from onion skin (Allium cepa). Sci Technol 5(2):26–32

    Google Scholar 

  67. 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 Natl Sci Res 6:32–37

    Google Scholar 

  68. Hinsch EM, Weber G, Chen HL, Robinson SC (2015) Colorfastness of extracted wood-staining fungal pigments on fabrics: a new potential for textile dyes. J Textile Apparel Technol Manag 9(3)

  69. Aishwarya AD (2014) Extraction of natural dyes from fungus—an alternate for textile dyeing. J Natl Sci Res 4(7):1–7

    Google Scholar 

  70. Devi S, Karuppan P (2015) Reddish brown pigments from Alternaria alternata for textile dyeing and printing. Indian J Fibre Text Res 40(3):315–319

    Google Scholar 

  71. 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

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Mr. S. Suresh Kumar, Fungal and Cancer Biology Lab, School of Biotechnology, Madurai Kamaraj University, for his support for the work. The authors acknowledge “DST-PURSE and RUSA” Madurai Kamaraj University, Madurai, India for the instrument facility. Also, the authors acknowledge King Saud University, Riyadh, Saudi Arabia, for funding this research through Researchers Supporting Project No: RSPR2023/11.

Funding

This work was supported by grants from the RUSA” Madurai Kamaraj University, Madurai, India.

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IM: Investigation, methodology, conceptualization, writing—original draft & editing. MT: investigation, methodology, conceptualization, writing—review & editing. ASB: investigation and methodology. JXS, RR, AA, NP: Writing—review & editing. MP: Supervision, conceptualization, Writing—review & editing.

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Correspondence to Mohan Pandi.

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Mani, I., Thangavel, M., Surendrababu, A. et al. Unveiling the Bioprospecting Efficacy and Textile Dyeing of a Novel Endophytic Mycobial Red Pigment. Indian J Microbiol (2024). https://doi.org/10.1007/s12088-024-01211-y

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