Characterization and mechanism of simultaneous degradation of aflatoxin B1 and zearalenone by an edible fungus of Agrocybe cylindracea GC-Ac2

Changying Guo; Lixia Fan; Qingqing Yang; Mingxiao Ning; Bingchun Zhang; Xianfeng Ren

doi:10.3389/fmicb.2024.1292824

Characterization and mechanism of simultaneous degradation of aflatoxin B₁ and zearalenone by an edible fungus of Agrocybe cylindracea GC-Ac2

Front Microbiol. 2024 Feb 13:15:1292824. doi: 10.3389/fmicb.2024.1292824. eCollection 2024.

Authors

Changying Guo^#^{1

2}, Lixia Fan^#^{1

2}, Qingqing Yang^#³, Mingxiao Ning^{1

2}, Bingchun Zhang^{1

2}, Xianfeng Ren^{1

2}

Affiliations

¹ Institute of Quality Standard and Testing Technology for Agro-products, Shandong Academy of Agricultural Sciences, Jinan, China.
² Shandong Provincial Key Laboratory of Test Technology on Food Quality and Safety, Jinan, China.
³ School of Agricultural Engineering and Food Science, Shandong University of Technology, Zibo, China.

^# Contributed equally.

Abstract

Contamination with multiple mycotoxins is a major issue for global food safety and trade. This study focused on the degradation of aflatoxin B₁ (AFB₁) and zearalenone (ZEN) by 8 types of edible fungi belonging to 6 species, inclulding Agaricus bisporus, Agrocybe cylindracea, Cyclocybe cylindracea, Cyclocybe aegerita, Hypsizygus marmoreus and Lentinula edodes. Among these fungi, Agrocybe cylindracea strain GC-Ac2 was shown to be the most efficient in the degradation of AFB₁ and ZEN. Under optimal degradation conditions (pH 6.0 and 37.4°C for 37.9 h), the degradation rate of both AFB₁ and ZEN reached over 96%. Through the analysis of functional detoxification components, it was found that the removal of AFB₁ and ZEN was primarily degraded by the culture supernatant of the fungus. The culture supernatant exhibited a maximum manganese peroxidase (MnP) activity of 2.37 U/mL. Interestingly, Agrocybe cylindracea strain GC-Ac2 also showed the capability to degrade other mycotoxins in laboratory-scale mushroom substrates, including 15A-deoxynivalenol, fumonisin B₁, B₂, B₃, T-2 toxin, ochratoxin A, and sterigmatocystin. The mechanism of degradation of these mycotoxins was speculated to be catalyzed by a complex enzyme system, which include MnP and other ligninolytic enzymes. It is worth noting that Agrocybe cylindracea can degrade multiple mycotoxins and produce MnP, which is a novel and significant discovery. These results suggest that this candidate strain and its enzyme system are expected to become valuable biomaterials for the simultaneous degradation of multiple mycotoxins.

Keywords: aflatoxin B1; edible fungi; manganese peroxidase; simultaneous degradation; zearalenone.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (Grant no. 32202208), the Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (Grant no. CXGC2023G11 and CXGC2023A25) and the Natural Science Foundation of Shandong (Grant no. ZR2022QC074). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.