Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate

Deoxynivalenol (DON) is a widely distributed mycotoxin that frequently occurs in various agricultural raw materials and feeds. DON acts as a virulence factor that accelerates the spread of plant diseases; moreover, its accumulation in grains causes yield loss and serious health problems to humans an...

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Main Authors: Yaoyao Zhai, Lei Zhong, Hui Gao, Zhaoxin Lu, Xiaomei Bie, Haizhen Zhao, Chong Zhang, Fengxia Lu
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02172/full
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spelling doaj-e1c2b8dcecae4f1292ef45db655293d22020-11-25T02:05:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-09-011010.3389/fmicb.2019.02172472027Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main IntermediateYaoyao ZhaiLei ZhongHui GaoZhaoxin LuXiaomei BieHaizhen ZhaoChong ZhangFengxia LuDeoxynivalenol (DON) is a widely distributed mycotoxin that frequently occurs in various agricultural raw materials and feeds. DON acts as a virulence factor that accelerates the spread of plant diseases; moreover, its accumulation in grains causes yield loss and serious health problems to humans and livestock. Biodegradation of DON into less- or non-toxic substances using naturally existing microorganisms is considered the best approach for DON detoxification. Although various single isolates and mixed cultures capable of detoxifying DON have been reported, details of the metabolic pathways and the degrading enzymes/coding genes involved are scarce. In this study, we aimed to isolate DON-degrading bacteria from soil samples and explore the mechanisms. Toward this end, 85 soil samples collected from different provinces in China were enriched under aerobic conditions with mineral media containing 50 μg/ml of DON as the sole carbon source. The bacterial consortium LZ-N1 exhibited highly efficient and steady DON-transforming activity. High-throughput sequencing was used to characterize the composition of the involved microflora, and analysis of 16S rRNA sequences indicated that LZ-N1 was composed of at least 11 bacterial genera, with Pseudomonas accounting for nearly half the relative abundance. Coincubation of a mixed culture of two novel strains from the LZ-N1 consortium, namely Pseudomonas sp. Y1 and Lysobacter sp. S1, showed sustained transformation of DON into the metabolite 3-epi-deoxynivalenol, with no degradation products detected after 72 h. The cell-free supernatant, lysate, and cell debris of the mixed culture possessed DON-degrading ability, with the supernatant reaching a DON degradation rate of 100% within 48 h with 50 μg/ml of DON. This is the first report of two-step enzymatic epimerization of DON by a mixed culture, which may provide a new insight into this pathway for future applications in detoxification of DON-contaminated cereals and feed.https://www.frontiersin.org/article/10.3389/fmicb.2019.02172/fulldeoxynivalenolenrichmentepimerizationbacterial consortiummixed culture PseudomonasLysobacter
collection DOAJ
language English
format Article
sources DOAJ
author Yaoyao Zhai
Lei Zhong
Hui Gao
Zhaoxin Lu
Xiaomei Bie
Haizhen Zhao
Chong Zhang
Fengxia Lu
spellingShingle Yaoyao Zhai
Lei Zhong
Hui Gao
Zhaoxin Lu
Xiaomei Bie
Haizhen Zhao
Chong Zhang
Fengxia Lu
Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
Frontiers in Microbiology
deoxynivalenol
enrichment
epimerization
bacterial consortium
mixed culture Pseudomonas
Lysobacter
author_facet Yaoyao Zhai
Lei Zhong
Hui Gao
Zhaoxin Lu
Xiaomei Bie
Haizhen Zhao
Chong Zhang
Fengxia Lu
author_sort Yaoyao Zhai
title Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
title_short Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
title_full Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
title_fullStr Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
title_full_unstemmed Detoxification of Deoxynivalenol by a Mixed Culture of Soil Bacteria With 3-epi-Deoxynivalenol as the Main Intermediate
title_sort detoxification of deoxynivalenol by a mixed culture of soil bacteria with 3-epi-deoxynivalenol as the main intermediate
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-09-01
description Deoxynivalenol (DON) is a widely distributed mycotoxin that frequently occurs in various agricultural raw materials and feeds. DON acts as a virulence factor that accelerates the spread of plant diseases; moreover, its accumulation in grains causes yield loss and serious health problems to humans and livestock. Biodegradation of DON into less- or non-toxic substances using naturally existing microorganisms is considered the best approach for DON detoxification. Although various single isolates and mixed cultures capable of detoxifying DON have been reported, details of the metabolic pathways and the degrading enzymes/coding genes involved are scarce. In this study, we aimed to isolate DON-degrading bacteria from soil samples and explore the mechanisms. Toward this end, 85 soil samples collected from different provinces in China were enriched under aerobic conditions with mineral media containing 50 μg/ml of DON as the sole carbon source. The bacterial consortium LZ-N1 exhibited highly efficient and steady DON-transforming activity. High-throughput sequencing was used to characterize the composition of the involved microflora, and analysis of 16S rRNA sequences indicated that LZ-N1 was composed of at least 11 bacterial genera, with Pseudomonas accounting for nearly half the relative abundance. Coincubation of a mixed culture of two novel strains from the LZ-N1 consortium, namely Pseudomonas sp. Y1 and Lysobacter sp. S1, showed sustained transformation of DON into the metabolite 3-epi-deoxynivalenol, with no degradation products detected after 72 h. The cell-free supernatant, lysate, and cell debris of the mixed culture possessed DON-degrading ability, with the supernatant reaching a DON degradation rate of 100% within 48 h with 50 μg/ml of DON. This is the first report of two-step enzymatic epimerization of DON by a mixed culture, which may provide a new insight into this pathway for future applications in detoxification of DON-contaminated cereals and feed.
topic deoxynivalenol
enrichment
epimerization
bacterial consortium
mixed culture Pseudomonas
Lysobacter
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02172/full
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