Novel insights into biofilm formation and the key differentially expressed genes in Yersinia enterocolitica from meat: Implications for food safety and disease prevention

IF 5 1区 农林科学 Q1 FOOD SCIENCE & TECHNOLOGY
Xiuqin Lou , Yue Wu , Zongzong Chen , Qian Zhang , Xiao Xiao , Zhiguo Fang
{"title":"Novel insights into biofilm formation and the key differentially expressed genes in Yersinia enterocolitica from meat: Implications for food safety and disease prevention","authors":"Xiuqin Lou ,&nbsp;Yue Wu ,&nbsp;Zongzong Chen ,&nbsp;Qian Zhang ,&nbsp;Xiao Xiao ,&nbsp;Zhiguo Fang","doi":"10.1016/j.ijfoodmicro.2024.110914","DOIUrl":null,"url":null,"abstract":"<div><p><em>Yersinia enterocolitica</em> is an important foodborne pathogen that can cause a zoonotic disease known as yersiniosis, which causes symptoms such as acute diarrhea, mesenteric adenitis, terminal ileum inflammation, pseudo appendicitis, sepsis, and other complications. The mechanism of biofilm formation in <em>Y. enterocolitica</em> remains poorly understood, with limited research available on this topic. This study systematically examined the distribution characteristics and biofilm formation ability of <em>Y. enterocolitica</em> isolated from poultry and livestock related samples. Analysis of food samples collected indicated significant presence of <em>Y. enterocolitica</em> (207/670, 30.9 %), particularly in frozen duck meat (7/11, 63.6 %). Majority of the isolated strains did not demonstrate biofilm-forming ability (52.7 %), while a notable percentage exhibited moderate (6.8 %) to strong (11.6 %) biofilm-forming ability. Additionally, a significant percentage of strains (16/207, 7.7 %) displayed extremely high optical density/cut-off OD (OD/ODC) ratios (the average OD value of each sample divided by the average OD value of the negative controls of each 96-well plate plus 3 standard deviations) (exceeding 10). Time-course analysis of biofilm formation in 10 isolates revealed three distinct patterns: (i) rapid increase from 6 h to 12 h, with gradual peak between 48 and 72 h followed by a slight decline and stabilization; (ii) little biofilm formation at 24 h with a gradual increase up to 96 h, maintaining this level until 120 h; and (iii) complete absence of biofilm formation throughout the experiment. Subsequent examination of differentially expressed genes (DEGs) in planktonic cells and biofilms of two strains with distinct biofilm formation capabilities identified seven metabolic pathways, including ribosome, photosynthesis, fatty acid degradation, valine, leucine, and isoleucine degradation, as well as pinene, camphor, and geraniol degradation. Significantly elevated expression levels of genes associated with flagellar assembly, bacterial chemotaxis, and quorum sensing (partially) were observed exclusively in planktonic cells of the selected strain with stronger biofilm-forming ability, implying that the heightened expression of flagellar assembly and bacterial chemotaxis-related genes is an important but not sole determinant of biofilm formation. The study contributes to the elucidation of the underlying mechanisms governing biofilm formation in <em>Y. enterocolitica</em> and may offer valuable insights for the advancement of novel food safety strategies.</p></div>","PeriodicalId":14095,"journal":{"name":"International journal of food microbiology","volume":"426 ","pages":"Article 110914"},"PeriodicalIF":5.0000,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"International journal of food microbiology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0168160524003581","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"FOOD SCIENCE & TECHNOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Yersinia enterocolitica is an important foodborne pathogen that can cause a zoonotic disease known as yersiniosis, which causes symptoms such as acute diarrhea, mesenteric adenitis, terminal ileum inflammation, pseudo appendicitis, sepsis, and other complications. The mechanism of biofilm formation in Y. enterocolitica remains poorly understood, with limited research available on this topic. This study systematically examined the distribution characteristics and biofilm formation ability of Y. enterocolitica isolated from poultry and livestock related samples. Analysis of food samples collected indicated significant presence of Y. enterocolitica (207/670, 30.9 %), particularly in frozen duck meat (7/11, 63.6 %). Majority of the isolated strains did not demonstrate biofilm-forming ability (52.7 %), while a notable percentage exhibited moderate (6.8 %) to strong (11.6 %) biofilm-forming ability. Additionally, a significant percentage of strains (16/207, 7.7 %) displayed extremely high optical density/cut-off OD (OD/ODC) ratios (the average OD value of each sample divided by the average OD value of the negative controls of each 96-well plate plus 3 standard deviations) (exceeding 10). Time-course analysis of biofilm formation in 10 isolates revealed three distinct patterns: (i) rapid increase from 6 h to 12 h, with gradual peak between 48 and 72 h followed by a slight decline and stabilization; (ii) little biofilm formation at 24 h with a gradual increase up to 96 h, maintaining this level until 120 h; and (iii) complete absence of biofilm formation throughout the experiment. Subsequent examination of differentially expressed genes (DEGs) in planktonic cells and biofilms of two strains with distinct biofilm formation capabilities identified seven metabolic pathways, including ribosome, photosynthesis, fatty acid degradation, valine, leucine, and isoleucine degradation, as well as pinene, camphor, and geraniol degradation. Significantly elevated expression levels of genes associated with flagellar assembly, bacterial chemotaxis, and quorum sensing (partially) were observed exclusively in planktonic cells of the selected strain with stronger biofilm-forming ability, implying that the heightened expression of flagellar assembly and bacterial chemotaxis-related genes is an important but not sole determinant of biofilm formation. The study contributes to the elucidation of the underlying mechanisms governing biofilm formation in Y. enterocolitica and may offer valuable insights for the advancement of novel food safety strategies.

关于肉类中小肠结肠耶尔森菌生物膜形成和关键差异表达基因的新见解:对食品安全和疾病预防的影响
小肠结肠耶尔森菌是一种重要的食源性病原体,可引起人畜共患病--耶尔森菌病,导致急性腹泻、肠系膜腺炎、回肠末端炎症、假性阑尾炎、败血症和其他并发症。人们对小肠结肠炎耶尔森菌形成生物膜的机制仍知之甚少,相关研究也十分有限。本研究系统研究了从家禽和家畜相关样本中分离出的小肠结肠炎病毒的分布特征和生物膜形成能力。对收集到的食品样本进行的分析表明,存在大量的小肠结肠炎病毒(207/670,30.9%),尤其是在冷冻鸭肉中(7/11,63.6%)。大部分分离出的菌株没有表现出生物膜形成能力(52.7%),但也有相当一部分菌株表现出中等(6.8%)到较强(11.6%)的生物膜形成能力。此外,相当一部分菌株(16/207,7.7%)显示出极高的光密度/截留光密度比(每个样本的平均光密度值除以每个 96 孔板阴性对照的平均光密度值再加上 3 个标准差)(超过 10)。对 10 个分离株生物膜形成的时程分析表明了三种不同的模式:(i) 生物膜形成从 6 小时到 12 小时迅速增加,在 48 小时到 72 小时之间逐渐达到高峰,随后略有下降并趋于稳定;(ii) 生物膜形成在 24 小时内很少,在 96 小时内逐渐增加,在 120 小时内保持这一水平;(iii) 在整个实验过程中完全没有生物膜形成。随后对两种具有不同生物膜形成能力的菌株的浮游细胞和生物膜中的差异表达基因(DEGs)进行了检测,发现了七种代谢途径,包括核糖体、光合作用、脂肪酸降解、缬氨酸、亮氨酸和异亮氨酸降解,以及蒎烯、樟脑和香叶醇降解。在生物膜形成能力较强的所选菌株的浮游细胞中,只观察到与鞭毛组装、细菌趋化和法定量感应(部分)相关的基因表达水平显著升高,这意味着鞭毛组装和细菌趋化相关基因的高表达是生物膜形成的一个重要而非唯一的决定因素。这项研究有助于阐明小肠结肠炎病毒生物膜形成的基本机制,并为推进新型食品安全战略提供有价值的见解。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
International journal of food microbiology
International journal of food microbiology 工程技术-食品科技
CiteScore
10.40
自引率
5.60%
发文量
322
审稿时长
65 days
期刊介绍: The International Journal of Food Microbiology publishes papers dealing with all aspects of food microbiology. Articles must present information that is novel, has high impact and interest, and is of high scientific quality. They should provide scientific or technological advancement in the specific field of interest of the journal and enhance its strong international reputation. Preliminary or confirmatory results as well as contributions not strictly related to food microbiology will not be considered for publication.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信