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.
Similar content being viewed by others
Data availability
The data supporting the findings are provided in the supplementary file.
6 References
Samanta AK, Agarwal P (2009) Application of natural dyes on textiles 34:384–399
Narsing Rao MP, Xiao M, Li WJ (2007) Fungal and bacterial pigments: secondary metabolites with wide applications. Front Microbiol 8:1113
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
Elliot AJ, Maier MA (2014) Color psychology: effects of perceiving color on psychological functioning in humans. Annu Rev Psychol 65:95–120
Mukherjee G, Mishra T, Deshmukh SK (2017) Fungal pigments: an overview. Dev Fungal Biol Appl Mycol 525–541
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
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
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”.
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
Durán N, Teixeira MF, De Conti R, Esposito E (2002) Ecological-friendly pigments from fungi. Crit Rev Food Sci Nutr 42(1):53–66
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
Atalla MM, Elkhrisy EAM, Youssef YA, Mohamed AA (2011) Production of textile reddish brown dyes by fungi. Malay J Microbiol 7(1):33–40
Meruvu H, Dos Santos JC (2021) Colors of life: a review on fungal pigments. Crit Rev Biotechnol 41(8):1153–1177
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
Feng Y, Shao Y, Zhou Y, Chen W, Chen F (2016) Monascus pigments. Ind Biotechnol Vit Biopigm Antioxidants 497–535
Mapari SA, Thrane U, Meyer AS (2010) Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol 28(6):300–307
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
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
Cenis JL (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20(9):2380
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
Ankenbrand MJ, Keller A, Wolf M, Schultz J, Förster F (2015) ITS2 database V: Twice as much. Mol Biol Evol 32(11):3030–3032
Schliep PKP (2011) phylogenetics analysis in R. Bioinformatics 27(4):592–593
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
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
Perez C (1990) Antibiotic assay by agar-well diffusion method. Acta Biol Med Exp 15:113–115
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
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
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
Gohel A, McCarthy MB, Gronowicz G (1999) Estrogen prevents glucocorticoid-induced apoptosis in osteoblasts in vivo and in vitro. Endocrinology 140(11):5339–5347
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
Kannathasan K, Kokila P (2021) Dyeing of cotton fabric by Caesalpinia sappan aqueous extract at different temperatures and mordants. Curr Bot 12:188–191
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
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
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
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
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
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
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
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
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
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
Narendrababu BN, Shishupala S (2017) Spectrophotometric detection of pigments from aspergillus and penicillium isolates. J Appl Biol Biotechnol 5(1):053–058
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
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
Singh N, Rajini PS (2004) Free radical scavenging activity of an aqueous extract of potato peel. Food Chem 85(4):611–616
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
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
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
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)
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
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
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
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
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)
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
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
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
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
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
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
Tyagi T, Agarwal M (2017) Research article antioxidant properties and phenolic compounds in methanolic extracts of Eichhornia crassipes. Res J Phytochem 11:85–89
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
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
Abed RM, Salman MD (2022) Chemical composition ethanol and methanol extract of lycoperdon pyriforme. Int J Health Sci 6(S1):13749–13760
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
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
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
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)
Aishwarya AD (2014) Extraction of natural dyes from fungus—an alternate for textile dyeing. J Natl Sci Res 4(7):1–7
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
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
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. No conflict of interest exits in the submission of this manuscript, and manuscript is approved by all authors for publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12088-024-01211-y