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Inhibitory effect of volatile organic compounds from Bacillus flexus TR-1 against Aspergillus flavus and aflatoxins in grains during storage

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Abstract

Aspergillus flavus infects stored grains and produces aflatoxins with highly toxic and carcinogenic properties, which are a threat to food safety and human health. Microbes and their bio-active compounds are considered effective agents to control A. flavus and aflatoxins during the pre- and post-harvest stages. Here, we reveal that Bacillus flexus strain TR-1 isolated from tea plant rhizosphere soil could efficiently inhibit the growth of A. flavus in dual culture tests through the production of antifungal volatiles. Additionally, these volatiles showed great inhibitory effects against A. flavus infection and aflatoxin production in maize and peanut with high water activity levels during storage. Scanning electron microscope analysis further proved that the conidia of A. flavus on the peanut surface treated with TR-1 volatiles could not germinate and were severely dehydrated and shrunken. Gas chromatography-tandem mass spectrometry revealed that five antifungal compounds were identified in the volatile profiles, including benzene, methyl thiolacetate, dimethyl disulfide, butanethioic acid S-methyl ester analogue, dimethyl trisulfide (DMTS), and S-methyl 3-methylbutanethioate. DMTS, with the best antagonistic effect, completely inhibited the growth of A. flavus at 10 μl−1 (compound volume/airspace volume). TR-1 also exhibited efficient and broad inhibitory effects against six other fungal pathogens. Overall, B. flexus strain TR-1 and its produced volatiles showed valid antifungal activity against phytopathogens. This study provides novel materials for the production of bioactive agents to control plant pathogens in stored grains.

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Funding

This work was supported by the National Natural Science Foundation of China [grant numbers 31701740], the National Natural Science Foundation of Henan [grant number 222300420519, 222301420111], Scientific and Technological Project in Henan Province [grant number 212102110447], and Nanhu Scholars Program for Young Scholars of XYNU. The authors would like to thank TopEdit (https://www.topeditsci.com) for its linguistic assistance during the preparation of this manuscript.

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Authors and Affiliations

  1. College of Life Science, Xinyang Normal University, Xinyang, 464000, China

    An-Dong Gong, Meng-Ge Song & Gao-Zhan Wang

  2. College of Forestry, Hebei Agricultural University, Baoding, 071000, China

    Hua-Ling Wang

  3. Laboratory of Quality & Safety Risk Assessment for Agro-Products (Shanghai), Ministry of Agriculture, Institute for Agro-Food Standards and Testing Technology, Shanghai Academy ofAgricultural Sciences, Shanghai, 201403, China

    Jian-Hua Wang

  4. Molecular Biotechnology Laboratory of Triticeae Crops, Huazhong Agricultural University, Wuhan, 430070, China

    Jing-Bo Zhang

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  1. An-Dong Gong
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Correspondence to An-Dong Gong.

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Supplementary Information

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10526_2023_10187_MOESM1_ESM.tif

Supplementary file1 (TIF 338 KB)—Mass spectrogram comparison between VOCs in TR-1 (RT=3.042 min) (up histogram) and benzene in the NIST 17 MS spectral database (down histogram). Horizontal axis indicates mass charge ratios, and peaks the relative abundance

10526_2023_10187_MOESM2_ESM.tif

Supplementary file2 (TIF 475 KB)—Mass spectrogram comparison between VOCs in TR-1 (RT=3.388 min) (up histogram) and methyl thiolacetate in the NIST 17 MS spectral database (down histogram). Horizontal axis indicates mass charge ratios, and peaks the relative abundance

10526_2023_10187_MOESM3_ESM.tif

Supplementary file3 (TIF 1109 KB)—Mass spectrogram comparison between VOCs in TR-1 (RT=4.389 min) (up histogram) and DMDS in the NIST 17 MS spectral database (down histogram). Horizontal axis indicates mass charge ratios, and peaks the relative abundance

10526_2023_10187_MOESM4_ESM.tif

Supplementary file4 (TIF 696 KB)—Mass spectrogram comparison between VOCs in TR-1 (RT=7.581 min) (up histogram) and butanethioic acid S-methyl ester in the NIST 17 MS spectral database (down histogram). Horizontal axis indicates mass charge ratios, and peaks the relative abundance

10526_2023_10187_MOESM5_ESM.tif

Supplementary file5 (TIF 1329 KB)—Mass spectrogram comparison between VOCs in TR-1 (RT=12.113 min) (up histogram) and DMTS in the NIST 17 MS spectral database (down histogram). Horizontal axis indicates mass charge ratios, and peaks the relative abundance

10526_2023_10187_MOESM6_ESM.tif

Supplementary file6 (TIF 1588 KB)—Broad spectrum antifungal activity of TR-1 against six important fungal pathogens. The fungi were inoculated in the center of a PDA plate and challenged with (control+TR-1) or without (control) TR-1, respectively. Fg: F. graminearum PH1, Fv: F. verticillioides 3056, Cg: C. graminicola M2, Cf: C. fructicola MG3, Aa: A. alternata TA133, and Bc: B. cinerea Y25

Supplementary file7 (DOCX 53 KB)

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Gong, AD., Song, MG., Wang, HL. et al. Inhibitory effect of volatile organic compounds from Bacillus flexus TR-1 against Aspergillus flavus and aflatoxins in grains during storage. BioControl 68, 181–190 (2023). https://doi.org/10.1007/s10526-023-10187-5

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