Lü Zexun, Su Li, Han Mengting, Wang Xiaoqi, Li Mei, Wang Siyue, Cui Shenghui, Chen Jia, Yang Baowei
College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100, China.
National Institutes for Food and Drug Control, Beijing 100050, China.
Int J Food Microbiol. 2025 Feb 16;430:111052. doi: 10.1016/j.ijfoodmicro.2024.111052. Epub 2025 Jan 3.
Yersinia intermedia, Y. frederiksenii, and Y. kristensenii are a group of pathogens that are commonly found in food and are often overlooked in terms of their pathogenic potential. This study conducted a systematic and comprehensive genomic analysis of 114 Y. intermedia genomes, 20 Y. frederiksenii genomes, and 65 Y. kristensenii genomes from public database and our previous study. The results showed that these species were most frequently detected in Europe (56.28 %, 112/199), followed by in Asia (20.6 %, 41/199). Additionally, 33.17 % (66/199) genomes were isolated from food. Y. intermedia were grouped into Bayesian analysis of population structure (Baps) groups 3 and 4, demonstrating significant genomic diversity. This species has a high proportion of accessory genes (79.43 %), approximately 50 % of which have unknown functions, indicating a high degree of genomic plasticity. The three species carried a large number of mobile genetic elements (MGEs), including plasmids such as ColRNAI_1, ColE10_1, Col440II_1, Col440I_1, and Col (Ye4449) _1; insertion sequences (ISs) like MITEYpe1, MITEEc1, and IS1635; genomic islands (GIs); and prophages. In Y. intermedia, the following antibiotics resistance genes (ARGs) were detected: qnrD1 in 3.51 % (4/114), aph(3')-Ia in 2.63 % (3/114), bla in 1.75 % (2/114), and catA1, vat(F), and tet(C) each in 0.88 % (1/114). In Y. kristensenii, vat(F) was present in 98.46 % (64/65), bla in 7.69 % (5/65), and aph(3')-Ia in 1.54 % (1/65). However, only one Y. frederiksenii genome carried vat(F). There were differences in the virulence gene composition of the three species, with Y. kristensenii having the highest number of virulence genes, particularly its complete cytotoxic genes (yaxA and yaxB) and flagellar motor proteins genes (motA and motB). The pathogenic mechanisms of Y. intermedia and Y. frederiksenii were more similar, especially in the carriage of O-antigen related genes. Y. frederiksenii's unique mechanisms also include the yapC gene, which encodes the autotransporter protein YapC from Y. pestis. After co-cultured with human colonic epithelial cell lines Caco-2 and HT-29, Y. intermedia and Y. kristensenii demonstrated different adhesive and invasive capabilities, particularly the Y. intermedia strain y7, which exhibited stronger adhesion and invasion in both cell lines. In strains y118 and y119 of Y. intermedia, an Arg378del mutation in the UreC protein was identified, resulting in the loss of urease activity. Therefore, this study revealed the pathogenic potential of Y. intermedia, Y. frederiksenii, and Y. kristensenii. Future research should focus on identifying their unknown virulence genes and strengthening public food safety measures to mitigate potential risks.
中间耶尔森菌、费氏耶尔森菌和克里斯滕森耶尔森菌是一组常见于食物中的病原体，其致病潜力往往被忽视。本研究对来自公共数据库和我们之前研究的114个中间耶尔森菌基因组、20个费氏耶尔森菌基因组和65个克里斯滕森耶尔森菌基因组进行了系统全面的基因组分析。结果表明，这些菌种在欧洲的检出频率最高（56.28%，112/199），其次是亚洲（20.6%，41/199）。此外，33.17%（66/199）的基因组是从食物中分离出来的。中间耶尔森菌被归入群体结构贝叶斯分析（Baps）的第3组和第4组，显示出显著的基因组多样性。该菌种的辅助基因比例很高（79.43%），其中约50%功能未知，表明其基因组可塑性程度很高。这三个菌种携带大量可移动遗传元件（MGEs），包括ColRNAI_1、ColE10_1、Col440II_1、Col440I_1和Col(Ye4449)_1等质粒；MITEYpe1、MITEEc1和IS1635等插入序列（ISs）；基因组岛（GIs）；以及原噬菌体。在中间耶尔森菌中，检测到以下抗生素抗性基因（ARGs）：3.51%（4/114）含有qnrD1，2.63%（3/114）含有aph(3')-Ia，1.75%（2/114）含有bla，0.88%（1/114）分别含有catA1、vat(F)和tet(C)。在克里斯滕森耶尔森菌中，98.46%（64/65）含有vat(F)，7.69%（5/65）含有bla，1.54%（1/65）含有aph(3')-Ia。然而，只有一个费氏耶尔森菌基因组携带vat(F)。这三个菌种的毒力基因组成存在差异，克里斯滕森耶尔森菌的毒力基因数量最多，尤其是其完整的细胞毒素基因（yaxA和yaxB）和鞭毛运动蛋白基因（motA和motB）。中间耶尔森菌和费氏耶尔森菌的致病机制更为相似，特别是在携带O抗原相关基因方面。费氏耶尔森菌的独特机制还包括yapC基因，该基因编码来自鼠疫耶尔森菌的自转运蛋白YapC。与人类结肠上皮细胞系Caco-2和HT-29共培养后，中间耶尔森菌和克里斯滕森耶尔森菌表现出不同的黏附及侵袭能力，特别是中间耶尔森菌菌株y7，在两种细胞系中均表现出更强的黏附和侵袭能力。在中间耶尔森菌的y118和y119菌株中，鉴定出UreC蛋白中的Arg378del突变，导致脲酶活性丧失。因此，本研究揭示了中间耶尔森菌、费氏耶尔森菌和克里斯滕森耶尔森菌的致病潜力。未来的研究应侧重于鉴定其未知的毒力基因，并加强公共食品安全措施以降低潜在风险。
