The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces

Bacillus cereus is a well-characterized human pathogen that produces toxins associated with diarrheal and emetic foodborne diseases. To investigate the possible transmission of B. cereus on lettuce farms in China and determine its enterotoxicity, (I) a total of 524 samples (lettuce: 332, soil: 69, w...

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Main Authors: Yang Qu, Chao Wei, Xiaohang Dai, Yalong Bai, Xin Zhao, Qingkuo Lan, Wenbo Wang, Yuanjuan Wu, Min Gao, Weihao Tang, Changyan Zhou, Yujuan Suo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.746632/full
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author Yang Qu
Yang Qu
Chao Wei
Xiaohang Dai
Yalong Bai
Xin Zhao
Qingkuo Lan
Wenbo Wang
Yuanjuan Wu
Min Gao
Weihao Tang
Changyan Zhou
Changyan Zhou
Yujuan Suo
Yujuan Suo
author_facet Yang Qu
Yang Qu
Chao Wei
Xiaohang Dai
Yalong Bai
Xin Zhao
Qingkuo Lan
Wenbo Wang
Yuanjuan Wu
Min Gao
Weihao Tang
Changyan Zhou
Changyan Zhou
Yujuan Suo
Yujuan Suo
author_sort Yang Qu
collection DOAJ
description Bacillus cereus is a well-characterized human pathogen that produces toxins associated with diarrheal and emetic foodborne diseases. To investigate the possible transmission of B. cereus on lettuce farms in China and determine its enterotoxicity, (I) a total of 524 samples (lettuce: 332, soil: 69, water: 57, manure: 57, pesticide: 9) were collected from 46 lettuce farms in five Chinese provinces, (II) multilocus sequence typing (MLST) was used to classify B. cereus isolates and for trace analysis, and (III) the presence of toxin genes and enterotoxins (Hbl and Nhe) was detected in 68 strains. The results showed that one hundred and sixty-one lettuce samples (48.5%) tested positive for B. cereus at levels ranging from 10 to 5.3 × 104 CFU/g. Among the environmental sample categories surveyed, the highest positive rate was that of the pesticide samples at 55.6%, followed by soil samples at 52.2% and manure samples at 12.3%. Moreover, one hundred isolates of B. cereus yielded 68 different sequence types (STs) and were classified into five phylogenetic clades. Furthermore, Nhe toxin genes (nheA, nheB, nheC) were broadly distributed and identified in all 68 strains (100%), while Hbl toxin genes (hblA, hblC, hblD) were present in 61 strains (89.7%), entFM was detected in 62 strains (91.2%), and cytK was found in 29 strains (42.6%). All strains were negative for ces. As for the enterotoxin, Nhe was observed in all 68 isolates carrying nheB, while Hbl was present in 76.5% (52/68) of the strains harboring hblC. This study is the first report of possible B. cereus transmission and of its potential enterotoxicity on lettuce farms in China. The results showed that soil and pesticides are the main sources of B. cereus on lettuce farms in China, and the possible transmission routes are as follows: soil-lettuce, manure-lettuce, pesticide-lettuce, manure-soil-lettuce, and water-manure-soil-lettuce. Furthermore, the B. cereus isolates, whether from lettuce or the environment, pose a potential risk to health.
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spelling doaj.art-60f86d5eb5584b9c8303445f085122bc2022-12-21T19:07:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-10-011210.3389/fmicb.2021.746632746632The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese ProvincesYang Qu0Yang Qu1Chao Wei2Xiaohang Dai3Yalong Bai4Xin Zhao5Qingkuo Lan6Wenbo Wang7Yuanjuan Wu8Min Gao9Weihao Tang10Changyan Zhou11Changyan Zhou12Yujuan Suo13Yujuan Suo14Laboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute for Agro-Food Standards and Testing Technology, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Co-Elite Agro-Food Testing Service Co., Ltd., Shanghai, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute of Quality Standard and Testing Technology for Agro-Products of Sichuan Academy of Agricultural Sciences, Chengdu, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute of Quality Standard and Testing Technology for Agro-Products of Sichuan Academy of Agricultural Sciences, Chengdu, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute for Agro-Food Standards and Testing Technology, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaInstitute of Germplasm Resources and Biotechnology, Tianjin Academy of Agricultural Sciences, Tianjin, ChinaInstitute of Germplasm Resources and Biotechnology, Tianjin Academy of Agricultural Sciences, Tianjin, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute of Agricultural Standards and Testing Technology for Agri-Products, Shandong Academy of Agricultural Sciences, Jinan, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute of Agricultural Standards and Testing Technology for Agri-Products, Shandong Academy of Agricultural Sciences, Jinan, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products Processing of Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences (CAAS), Beijing, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products Processing of Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences (CAAS), Beijing, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute for Agro-Food Standards and Testing Technology, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Co-Elite Agro-Food Testing Service Co., Ltd., Shanghai, ChinaLaboratory of Quality and Safety Risk Assessment for Agro-Products of Ministry of Agriculture and Rural Affairs, Institute for Agro-Food Standards and Testing Technology, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Co-Elite Agro-Food Testing Service Co., Ltd., Shanghai, ChinaBacillus cereus is a well-characterized human pathogen that produces toxins associated with diarrheal and emetic foodborne diseases. To investigate the possible transmission of B. cereus on lettuce farms in China and determine its enterotoxicity, (I) a total of 524 samples (lettuce: 332, soil: 69, water: 57, manure: 57, pesticide: 9) were collected from 46 lettuce farms in five Chinese provinces, (II) multilocus sequence typing (MLST) was used to classify B. cereus isolates and for trace analysis, and (III) the presence of toxin genes and enterotoxins (Hbl and Nhe) was detected in 68 strains. The results showed that one hundred and sixty-one lettuce samples (48.5%) tested positive for B. cereus at levels ranging from 10 to 5.3 × 104 CFU/g. Among the environmental sample categories surveyed, the highest positive rate was that of the pesticide samples at 55.6%, followed by soil samples at 52.2% and manure samples at 12.3%. Moreover, one hundred isolates of B. cereus yielded 68 different sequence types (STs) and were classified into five phylogenetic clades. Furthermore, Nhe toxin genes (nheA, nheB, nheC) were broadly distributed and identified in all 68 strains (100%), while Hbl toxin genes (hblA, hblC, hblD) were present in 61 strains (89.7%), entFM was detected in 62 strains (91.2%), and cytK was found in 29 strains (42.6%). All strains were negative for ces. As for the enterotoxin, Nhe was observed in all 68 isolates carrying nheB, while Hbl was present in 76.5% (52/68) of the strains harboring hblC. This study is the first report of possible B. cereus transmission and of its potential enterotoxicity on lettuce farms in China. The results showed that soil and pesticides are the main sources of B. cereus on lettuce farms in China, and the possible transmission routes are as follows: soil-lettuce, manure-lettuce, pesticide-lettuce, manure-soil-lettuce, and water-manure-soil-lettuce. Furthermore, the B. cereus isolates, whether from lettuce or the environment, pose a potential risk to health.https://www.frontiersin.org/articles/10.3389/fmicb.2021.746632/fullBacillus cereuslettuce farmmultilocus sequence typing (MLST)tracing analysisenterotoxicity
spellingShingle Yang Qu
Yang Qu
Chao Wei
Xiaohang Dai
Yalong Bai
Xin Zhao
Qingkuo Lan
Wenbo Wang
Yuanjuan Wu
Min Gao
Weihao Tang
Changyan Zhou
Changyan Zhou
Yujuan Suo
Yujuan Suo
The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
Frontiers in Microbiology
Bacillus cereus
lettuce farm
multilocus sequence typing (MLST)
tracing analysis
enterotoxicity
title The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
title_full The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
title_fullStr The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
title_full_unstemmed The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
title_short The Possible Transmission and Potential Enterotoxicity of Bacillus cereus on Lettuce Farms in Five Chinese Provinces
title_sort possible transmission and potential enterotoxicity of bacillus cereus on lettuce farms in five chinese provinces
topic Bacillus cereus
lettuce farm
multilocus sequence typing (MLST)
tracing analysis
enterotoxicity
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.746632/full
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