Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea

Lettuce wraps are popular in Korean cuisine for their high nutritional value and versatility as healthy additions to multiple dishes. Microbial contamination of lettuce is a major concern, as lettuce is consumed fresh without cooking. Among foodborne pathogens, the spore-forming, facultative anaerob...

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Main Authors: Nagendran Rajalingam, Jieun Jung, Seung-Mi Seo, Hyun-Sook Jin, Bo-Eun Kim, Myeong-In Jeong, Dawoon Kim, Jae-Gee Ryu, Kyoung-Yul Ryu, Kwang Kyo Oh
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.906040/full
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author Nagendran Rajalingam
Jieun Jung
Seung-Mi Seo
Hyun-Sook Jin
Bo-Eun Kim
Myeong-In Jeong
Dawoon Kim
Jae-Gee Ryu
Kyoung-Yul Ryu
Kwang Kyo Oh
author_facet Nagendran Rajalingam
Jieun Jung
Seung-Mi Seo
Hyun-Sook Jin
Bo-Eun Kim
Myeong-In Jeong
Dawoon Kim
Jae-Gee Ryu
Kyoung-Yul Ryu
Kwang Kyo Oh
author_sort Nagendran Rajalingam
collection DOAJ
description Lettuce wraps are popular in Korean cuisine for their high nutritional value and versatility as healthy additions to multiple dishes. Microbial contamination of lettuce is a major concern, as lettuce is consumed fresh without cooking. Among foodborne pathogens, the spore-forming, facultative anaerobic bacterium, Bacillus cereus is one of the frequently detected pathogen in lettuce in Korea. In this study, we investigated the prevalence and distribution of Bacillus cereus strains in lettuce production farms and further evaluated the enterotoxin gene profiles, antibiotic susceptibility, multidrug resistance pattern, and genetic differences among the B. cereus group isolates. Of the 140 samples isolated from 10 lettuce production farms, 30 samples (21.42%) were positive for B. cereus in which 19 (31.6%) and 10 (23.25%) were from soil and lettuce, respectively. The enterotoxin patterns A (hblCDA, nheABC, entFM, and cytK genes) and B (hblCDA, nheABC, and entFM genes) accounted for 50% and 20% of all the isolates, whereas the emetic gene cesB was not detected in any of the B. cereus group isolates. Antibiotic susceptibility testing of the B. cereus group isolates revealed that all the strains were predominantly resistant to β-lactam antibiotics except imipenem and generally susceptible to most of the non β-lactam antibiotics, including gentamycin, streptomycin, chloramphenicol, and tetracycline. ERIC-PCR and MLST analysis revealed high genetic diversity among the 30 B. cereus group isolates, which belonged to 26 different sequence types (STs) and seven new STs. Moreover, isolates with identical STs exhibited similar patterns of antibiotic resistance and enterotoxin profiles. Results of this study indicate a high prevalence of B. cereus group isolates in lettuce production farms in the Republic of Korea.
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spelling doaj.art-e8a7404f2b2849da8c7678f10e3e79702022-12-22T04:02:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.906040906040Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in KoreaNagendran Rajalingam0Jieun Jung1Seung-Mi Seo2Hyun-Sook Jin3Bo-Eun Kim4Myeong-In Jeong5Dawoon Kim6Jae-Gee Ryu7Kyoung-Yul Ryu8Kwang Kyo Oh9Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaFunctional Food and Nutrition Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaPlanning and Coordination Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaMicrobial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, South KoreaLettuce wraps are popular in Korean cuisine for their high nutritional value and versatility as healthy additions to multiple dishes. Microbial contamination of lettuce is a major concern, as lettuce is consumed fresh without cooking. Among foodborne pathogens, the spore-forming, facultative anaerobic bacterium, Bacillus cereus is one of the frequently detected pathogen in lettuce in Korea. In this study, we investigated the prevalence and distribution of Bacillus cereus strains in lettuce production farms and further evaluated the enterotoxin gene profiles, antibiotic susceptibility, multidrug resistance pattern, and genetic differences among the B. cereus group isolates. Of the 140 samples isolated from 10 lettuce production farms, 30 samples (21.42%) were positive for B. cereus in which 19 (31.6%) and 10 (23.25%) were from soil and lettuce, respectively. The enterotoxin patterns A (hblCDA, nheABC, entFM, and cytK genes) and B (hblCDA, nheABC, and entFM genes) accounted for 50% and 20% of all the isolates, whereas the emetic gene cesB was not detected in any of the B. cereus group isolates. Antibiotic susceptibility testing of the B. cereus group isolates revealed that all the strains were predominantly resistant to β-lactam antibiotics except imipenem and generally susceptible to most of the non β-lactam antibiotics, including gentamycin, streptomycin, chloramphenicol, and tetracycline. ERIC-PCR and MLST analysis revealed high genetic diversity among the 30 B. cereus group isolates, which belonged to 26 different sequence types (STs) and seven new STs. Moreover, isolates with identical STs exhibited similar patterns of antibiotic resistance and enterotoxin profiles. Results of this study indicate a high prevalence of B. cereus group isolates in lettuce production farms in the Republic of Korea.https://www.frontiersin.org/articles/10.3389/fmicb.2022.906040/fullBacillus cereuslettucetoxin profilingantimicrobial resistanceERIC-PCRMLST
spellingShingle Nagendran Rajalingam
Jieun Jung
Seung-Mi Seo
Hyun-Sook Jin
Bo-Eun Kim
Myeong-In Jeong
Dawoon Kim
Jae-Gee Ryu
Kyoung-Yul Ryu
Kwang Kyo Oh
Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
Frontiers in Microbiology
Bacillus cereus
lettuce
toxin profiling
antimicrobial resistance
ERIC-PCR
MLST
title Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
title_full Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
title_fullStr Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
title_full_unstemmed Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
title_short Prevalence, distribution, enterotoxin profiles, antimicrobial resistance, and genetic diversity of Bacillus cereus group isolates from lettuce farms in Korea
title_sort prevalence distribution enterotoxin profiles antimicrobial resistance and genetic diversity of bacillus cereus group isolates from lettuce farms in korea
topic Bacillus cereus
lettuce
toxin profiling
antimicrobial resistance
ERIC-PCR
MLST
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.906040/full
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