Estragole Inhibits Growth and Aflatoxin Biosynthesis of by Affecting Reactive Oxygen Species Homeostasis

Overview

Journal Microbiol Spectr

Specialty Microbiology

Date 2023 Jun 8

PMID 37289093

Authors

Liuke Liang

Wei Zhang

Jing Hao

Yanyu Wang

Shan Wei

Shuaibing Zhang

Yuansen Hu

Yangyong Lv

Affiliations

Soon will be listed here.

Abstract

A variety of essential oils and edible compounds have been widely recognized for their antifungal activity in recent years. In this study, we explored the antifungal activity of estragole from Pimenta racemosa against Aspergillus flavus and investigated the underlying mechanism of action. The results showed that estragole had significant antifungal activity against A. flavus, with a minimum inhibitory concentration of 0.5 μL/mL against spore germination. Additionally, estragole inhibited the biosynthesis of aflatoxin in a dose-dependent manner, and aflatoxin biosynthesis was significantly inhibited at 0.125 μL/mL. Pathogenicity assays showed that estragole had potential antifungal activity against A. flavus in peanut and corn grains by inhibiting conidia and aflatoxin production. Transcriptomic analysis showed that the differentially expressed genes (DEGs) were mainly related to oxidative stress, energy metabolism, and secondary metabolite synthesis following estragole treatment. Importantly, we experimentally verified reactive oxidative species accumulation following downregulation of antioxidant enzymes, including catalase, superoxide dismutase, and peroxidase. These results suggest that estragole inhibits the growth and aflatoxin biosynthesis of A. flavus by modulating intracellular redox homeostasis. These findings expand our knowledge on the antifungal activity and molecular mechanisms of estragole, and provide a basis for estragole as a potential agent against A. flavus contamination. Aspergillus flavus contaminates crops and produces aflatoxins, carcinogenic secondary metabolites which pose a serious threat to agricultural production and animal and human health. Currently, control of A. flavus growth and mycotoxin contamination mainly relies on antimicrobial chemicals, agents with side effects such as toxic residues and the emergence of resistance. With their safety, environmental friendliness, and high efficiency, essential oils and edible compounds have become promising antifungal agents to control growth and mycotoxin biosynthesis in hazardous filamentous fungi. In this study, we explored the antifungal activity of estragole from against A. flavus and investigated its underlying mechanism. The results demonstrated that estragole inhibits the growth and aflatoxin biosynthesis of A. flavus by modulating intracellular redox homeostasis.

Citing Articles

Inhibition Mechanism of Leaf Essential Oil Against and Aflatoxins.

Liang H, Lv F, Xian M, Luo C, Zhang L, Yang M Foods. 2025; 14(4).

PMID: 40002124 PMC: 11853908. DOI: 10.3390/foods14040682.

Rhein Inhibits Cell Development and Aflatoxin Biosynthesis via Energy Supply Disruption and ROS Accumulation in .

Wang X, Sahibzada K, Du R, Lei Y, Wei S, Li N Toxins (Basel). 2024; 16(7).

PMID: 39057925 PMC: 11280830. DOI: 10.3390/toxins16070285.

References

Huang Z, Zhang S, Xu Y, Li L, Li Y . Metabolic Effects of the pksCT Gene on Monascus aurantiacus Li As3.4384 Using Gas Chromatography--Time-of-Flight Mass Spectrometry-Based Metabolomics. J Agric Food Chem. 2016; 64(7):1565-74. DOI: 10.1021/acs.jafc.5b06082. View

Basilico M, Basilico J . Inhibitory effects of some spice essential oils on Aspergillus ochraceus NRRL 3174 growth and ochratoxin A production. Lett Appl Microbiol. 1999; 29(4):238-41. DOI: 10.1046/j.1365-2672.1999.00621.x. View

Fontenelle R, Morais S, Brito E, Brilhante R, Cordeiro R, Nascimento N . Antifungal activity of essential oils of Croton species from the Brazilian Caatinga biome. J Appl Microbiol. 2008; 104(5):1383-90. DOI: 10.1111/j.1365-2672.2007.03707.x. View

Hadrich I, Amouri I, Neji S, Mahfoud N, Ranque S, Makni F . Genetic structure of Aspergillus flavus populations in human and avian isolates. Eur J Clin Microbiol Infect Dis. 2012; 32(2):277-82. DOI: 10.1007/s10096-012-1740-5. View

Sanchez Armengol E, Harmanci M, Laffleur F . Current strategies to determine antifungal and antimicrobial activity of natural compounds. Microbiol Res. 2021; 252:126867. DOI: 10.1016/j.micres.2021.126867. View

Hayyan M, Hashim M, AlNashef I . Superoxide Ion: Generation and Chemical Implications. Chem Rev. 2016; 116(5):3029-85. DOI: 10.1021/acs.chemrev.5b00407. View

Liu J, Yang L, Hou Y, Soteyome T, Zeng B, Su J . Transcriptomics Study on Biofilm Under Low Concentration of Ampicillin. Front Microbiol. 2018; 9:2413. PMC: 6218852. DOI: 10.3389/fmicb.2018.02413. View

Hu L, Ban F, Li H, Qian P, Shen Q, Zhao Y . Thymol Induces Conidial Apoptosis in Aspergillus flavus via Stimulating K Eruption. J Agric Food Chem. 2018; 66(32):8530-8536. DOI: 10.1021/acs.jafc.8b02117. View

Walsh C, Fischbach M . Inhibitors of sterol biosynthesis as Staphylococcus aureus antibiotics. Angew Chem Int Ed Engl. 2008; 47(31):5700-2. PMC: 2603329. DOI: 10.1002/anie.200801801. View

10.

Mota A, Martins M, Arantes S, Lopes V, Bettencourt E, Pombal S . Antimicrobial activity and chemical composition of the essential oils of Portuguese Foeniculum vulgare fruits. Nat Prod Commun. 2015; 10(4):673-6. View

11.

Natarajan S, Balachandar D, Senthil N, Velazhahan R, Paranidharan V . Volatiles of antagonistic soil yeasts inhibit growth and aflatoxin production of Aspergillus flavus. Microbiol Res. 2022; 263:127150. DOI: 10.1016/j.micres.2022.127150. View

12.

Yao L, Ban F, Peng S, Xu D, Li H, Mo H . Exogenous Iron Induces NADPH Oxidases-Dependent Ferroptosis in the Conidia of . J Agric Food Chem. 2021; 69(45):13608-13617. DOI: 10.1021/acs.jafc.1c04411. View

13.

Eom T, Moon H, Yu J, Park H . Characterization of the velvet regulators in Aspergillus flavus. J Microbiol. 2018; 56(12):893-901. DOI: 10.1007/s12275-018-8417-4. View

14.

Fujiwara M, Ichinomiya M, Motoyama T, Horiuchi H, Ohta A, Takagi M . Evidence that the Aspergillus nidulans class I and class II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J Biochem. 2000; 127(3):359-66. DOI: 10.1093/oxfordjournals.jbchem.a022616. View

15.

Klich M . Aspergillus flavus: the major producer of aflatoxin. Mol Plant Pathol. 2010; 8(6):713-22. DOI: 10.1111/j.1364-3703.2007.00436.x. View

16.

Ikai N, Nakazawa N, Hayashi T, Yanagida M . The reverse, but coordinated, roles of Tor2 (TORC1) and Tor1 (TORC2) kinases for growth, cell cycle and separase-mediated mitosis in Schizosaccharomyces pombe. Open Biol. 2012; 1(3):110007. PMC: 3352084. DOI: 10.1098/rsob.110007. View

17.

Bezerra A, Rodrigues Bezerra S, Silva Macedo N, de Sousa Silveira Z, Rodrigues Dos Santos Barbosa C, de Freitas T . Effect of estragole over the RN4220 Staphylococcus aureus strain and its toxicity in Drosophila melanogaster. Life Sci. 2020; 264:118675. DOI: 10.1016/j.lfs.2020.118675. View

18.

Turna N, Wu F . Risk assessment of aflatoxin-related liver cancer in Bangladesh. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2019; 36(2):320-326. DOI: 10.1080/19440049.2019.1567941. View

19.

da Costa R, Rocha J, de Freitas T, Pereira R, Pereira Junior F, de Oliveira M . Evaluation of antibacterial activity and reversal of the NorA and MepA efflux pump of estragole against Staphylococcus aureus bacteria. Arch Microbiol. 2021; 203(6):3551-3555. DOI: 10.1007/s00203-021-02347-x. View

20.

Shen Q, Zhou W, Li H, Hu L, Mo H . ROS Involves the Fungicidal Actions of Thymol against Spores of Aspergillus flavus via the Induction of Nitric Oxide. PLoS One. 2016; 11(5):e0155647. PMC: 4872997. DOI: 10.1371/journal.pone.0155647. View