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Characterization and metabolomic profiling of two pigment producing fungi from infected fruits of Indian Gooseberry

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Abstract

Two pigment producing fungi, Talaromyces atroroseus and Penicillium choerospondiatis, were isolated and identified from infected fruits of Phyllanthus emblica L. based on amplification and sequencing of internal transcribed spacer region and beta-tubulin gene. This is the first occurrence report of these two fungi from fruits of P. emblica. Culture extract containing metabolites of T. atroroseus and P. choerospondiatis contained phenolics of 26.35 mg and 30.89 mg GAE/g dry extract respectively; whereas no significant amount of flavonoids and tannins were detected. P. choerospondiatis metabolites extract showed higher DPPH and ABTS activity with IC50 values of 21.94 mg/ml and 27.03 mg/ml respectively than T. atroroseus. LC-HRMS analysis of metabolites extract of T. atroroseus revealed presence of trimethyl-isopropyl-butanamide, perlolyrine, N-hexadecanoylpyrrolidine etc. whereas P. choerospondiatis displayed presence of tangeraxanthin, ugaxanthone, daphniphylline, etc. Therefore, fungal metabolites are rich natural sources of diversified compounds that can be utilized in dyeing industries, cosmetics and novel drug development.

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References

  • Afshari M, Shahidi F, Mortazavi SA, Tabatabai F, Es’ haghi Z (2015) Investigating the influence of pH, temperature and agitation speed on yellow pigment production by Penicillium aculeatum ATCC 10409. Nat Prod Res 29(14):1300–1306

    Article  CAS  PubMed  Google Scholar 

  • Anzai Y et al (2008) Functional analysis of MycCI and MycG, cytochrome P450 enzymes involved in biosynthesis of mycinamicin macrolide antibiotics. Chem Biol 15:950–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baliga MS, Prabhu AN, Prabhu DA, Shivashankara AR, Abraham A, Palatty PL (2013) Antidiabetic and cardioprotective effects of Amla (Emblica officinalis Gaertn) and its phytochemicals: preclinical observations. In: Bioactive food as dietary interventions for diabetes, pp 583–600

  • Bhattacharya E, Mandal Biswas S (2021) Role of tartaric acid in the ecology of a zoochoric fruit species, Tamarindus indica L. Int J Fruit Sci 21(1):819–825

    Article  Google Scholar 

  • Bills GF, Gloer JB (2016) Biologically active secondary metabolites from the fungi. Microbiol Spectr 4(6):4–6

    Article  Google Scholar 

  • Blake PM, Hurst GA, Terry TA (1987) Responses of vegetation and deer forage following application of hexazinone. S J Appl for 11(4):176–180

    CAS  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28(1):25–30

    Article  CAS  Google Scholar 

  • Burns RE (1971) Method for estimation of tannin in grain sorghum 1. Agron J 63(3):511–512

    Article  CAS  Google Scholar 

  • Cao MY, Ma BJ, Gu QX, Fu B, Lu HH (2022) Concise enantioselective total synthesis of daphenylline enabled by an intramolecular oxidative dearomatization. J Am Chem Soc 144(13):5750–5755

    Article  CAS  PubMed  Google Scholar 

  • Chávez R, Fierro F, García-Rico RO, Vaca I (2015) Filamentous fungi from extreme environments as a promising source of novel bioactive secondary metabolites. Front Microbiol 6:903

    Article  PubMed  PubMed Central  Google Scholar 

  • Dairi T, Hasegawa M (1989) Common biosynthetic feature of fortimicin-group antibiotics. J Antibiot 42(6):934–943

    Article  CAS  Google Scholar 

  • Dang A, Reddy AJ, Pokala V et al (2022) An analysis of the use of proparacaine in cataract surgery. Cureus 14(2):e22175. https://doi.org/10.7759/cureus.22175

    Article  PubMed  PubMed Central  Google Scholar 

  • Du G, Yang W, Liao X, Gao C, Yang J, Yang B (2022) Synthesis, characterization and thermal controlled release of 2-isopropyl-N,2,3-trimethylbutyramide with acyclic cucurbit [n] urils inclusion complexes. Chem Select 7(13):e202104390

    CAS  Google Scholar 

  • Dufossé L, Fouillaud M, Caro Y, Mapari SA, Sutthiwong N (2014) Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr Opin Biotechnol 26:56–61

    Article  PubMed  Google Scholar 

  • Dufossé L, Fouillaud M, Caro Y (2021) Fungi and fungal metabolites for the improvement of human and animal nutrition and health. J Fungi 7(4):274

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Shao Y, Chen F (2012) Monascus pigments. Appl Microbiol Biotechnol 96(6):1421–1440

    Article  CAS  PubMed  Google Scholar 

  • Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11(6):481–487

    Article  CAS  PubMed  Google Scholar 

  • Frisvad JC, Yilmaz N, Thrane U, Rasmussen KB, Houbraken J, Samson RA (2013) Talaromyces atroroseus, a new species efficiently producing industrially relevant red pigments. PLoS ONE 8(12):e84102

    Article  PubMed  PubMed Central  Google Scholar 

  • Gontia-Mishra I, Tripathi N, Tiwari S (2014) A simple and rapid DNA extraction protocol for filamentous fungi efficient for molecular studies. Indian J Biotechnol 13:536–539

    CAS  Google Scholar 

  • Hawkins JM, Moore PA (2002) Local anesthesia: advances in agents and techniques. Dental Clin 46(4):719–732

    Google Scholar 

  • Hazra A, Mahadani P, Das S, Bhattacharya S, Kumar R, Sengupta C, Das S (2021) Insight to the ancestral relations and varietal diversity of Indian tea [Camellia sinensis (L.) Kuntze] through plastid and nuclear phylogenetic markers. Genet Resour Crop Evol 68(2):773–783

    Article  Google Scholar 

  • Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2007) Endophytic fungi from Nerium oleander L. (Apocynaceae): main constituents and antioxidant activity. World J Microbiol Biotechnol 23:1253–1263

    Article  CAS  Google Scholar 

  • Kirti K, Amita S, Priti S, Jyoti S (2014) Colorful world of microbes: carotenoids and their applications. Adv Biol 2014:1–13

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopchuk JM (2019) Imide natural products. In: Imides. Elsevier, pp 255–334

  • Meyer V, Basenko EY, Philipp Benz J, Braus GH, Caddick MX, Csukai M, Vries RP, Endy D, Frisvad JC, Gunde-Cimerman N (2020) Growing a circular economy with fungal biotechnology: a white paper. Fungal Biol Biotechnol 7(1):1–23

    Article  Google Scholar 

  • Nagai C, Noda K, Kirihara A, Tomita Y, Murata M (2019) A low-molecular weight Maillard pigment from beer was identified as perlolyrine, a Maillard reaction product from tryptophan. Food Sci Technol Res 25(1):81–88

    Article  CAS  Google Scholar 

  • Nair B (2001) Final report on the safety assessment of benzyl alcohol, benzoic acid, and sodium benzoate. Int J Toxicol 20:23–50

    Article  PubMed  Google Scholar 

  • Oishi S (2002) Effects of butyl paraben on the male reproductive system in mice. Arch Toxicol 76(7):423–429

    Article  CAS  PubMed  Google Scholar 

  • Pombeiro-Sponchiado SR, Sousa GS, Andrade JC, Lisboa HF, Gonçalves RC (2017) Production of melanin pigment by fungi and its biotechnological applications. Melanin 47–75

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9–10):1231–1237

    Article  CAS  PubMed  Google Scholar 

  • Sajid S, Akbar N (2018) 1. Applications of fungal pigments in biotechnology. Pure Appl Biol PAB 7(3):922–930

    CAS  Google Scholar 

  • Salim RG, Fadel M, Youssef YA, Taie HA, Abosereh NA, El-Sayed GM, Marzouk M (2022) A local Talaromyces atroroseus TRP-NRC isolate: isolation, genetic improvement, and biotechnological approach combined with LC/HRESI-MS characterization, skin safety, and wool fabric dyeing ability of the produced red pigment mixture. J Genet Eng Biotechnol 20(1):1–22

    Article  Google Scholar 

  • Satoi S, Muto N, Hayashi M, Fujii T, Otani M (1980) Mycinamicins, new macrolide antibiotics. I. Taxonomy, production, isolation, characterization and properties. J Antibiot 33(4):364–376

    Article  CAS  Google Scholar 

  • Sengupta P, Sen S, Mukherjee K, Acharya K (2020) Postharvest diseases of Indian gooseberry and their management: a review. Int J Fruit Sci 20(2):178–190

    Article  Google Scholar 

  • Singh E, Sharma S, Pareek A, Dwivedi J, Yadav S, Sharma S (2011) Phytochemistry, traditional uses and cancer chemopreventive activity of Amla (Phyllanthus emblica): the sustainer. J Appl Pharm Sci 02(01):176–183

    Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16(3):144–158

    CAS  Google Scholar 

  • Takahashi JA, Barbosa BV, Martins BDA, Guirlanda PC, Moura AFM (2020) Use of the versatility of fungal metabolism to meet modern demands for healthy aging, functional foods, and sustainability. J Fungi 6(4):223

    Article  CAS  Google Scholar 

  • Tian X, Yu Q, Yao D, Shao L, Liang Z, Jia F, Dai R (2018) New insights into the response of metabolome of Escherichia coli O157: H7 to ohmic heating. Front Microbiol 9:2936

    Article  PubMed  PubMed Central  Google Scholar 

  • Viggiano A, Salo O, Ali H, Szymanski W, Lankhorst PP, Nygård Y, Driessen AJ (2018) Pathway for the biosynthesis of the pigment chrysogine by Penicillium chrysogenum. Appl Environ Microbiol 84(4):e02246-e2317

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang XC, Chen K, Zeng ZQ, Zhuang WY (2017) Phylogeny and morphological analyses of Penicillium section Sclerotiora (Fungi) lead to the discovery of five new species. Sci Rep 7(1):1–14

    PubMed  PubMed Central  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

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Acknowledgements

We are privileged to convey our sincere gratitude to our respected Director, Prof. Sanghamitra Bandhopadhyay for providing laboratory facilities and financial support for performing this research work. We are indebted to Prof-in-Charge, Biological Sciences Division; Head, Agricultural and Ecological Research Unit, Indian Statistical Institute, for their affectionate encouragement, valuable advice and enormous laboratory facilities.

Funding

Funding was provided by Indian Statistical Institute, Kolkata (Grant no. 5521F).

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Contributions

MD—design of the experiment, investigation, collection of test data, formal analysis, drafting the article; AH—design of the experiment, investigation, formal analysis, revision of manuscript; EB—design of the experiment, investigation, formal analysis, revision of manuscript; RB—design of the experiment, investigation, formal analysis, revision of manuscript; SMB—critical revision, funding acquisition, project administration, validation, supervision.

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Correspondence to Madhurima Dutta or Suparna Mandal Biswas.

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The authors who have engaged in this study declared that they have no conflict of interests among them regarding the publication of this paper.

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Communicated by Yusuf Akhter.

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Dutta, M., Hazra, A., Bhattacharya, E. et al. Characterization and metabolomic profiling of two pigment producing fungi from infected fruits of Indian Gooseberry. Arch Microbiol 205, 141 (2023). https://doi.org/10.1007/s00203-023-03483-2

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