Genomic characteristics and virulence of common but overlooked Yersinia intermedia, Y. frederiksenii, and Y. kristensenii in food

Zexun Lü; Li Su; Mengting Han; Xiaoqi Wang; Mei Li; Siyue Wang; Shenghui Cui; Jia Chen; Baowei Yang

doi:10.1016/j.ijfoodmicro.2024.111052

Genomic characteristics and virulence of common but overlooked Yersinia intermedia, Y. frederiksenii, and Y. kristensenii in food

Int J Food Microbiol. 2025 Jan 3:430:111052. doi: 10.1016/j.ijfoodmicro.2024.111052. Online ahead of print.

Authors

Zexun Lü¹, Li Su¹, Mengting Han¹, Xiaoqi Wang¹, Mei Li¹, Siyue Wang¹, Shenghui Cui², Jia Chen³, Baowei Yang⁴

Affiliations

¹ College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100, China.
² National Institutes for Food and Drug Control, Beijing 100050, China. Electronic address: cuishenghui@aliyun.com.
³ Shijiazhuang University, Shijiazhuang 050035, China. Electronic address: chenjia_0311@163.com.
⁴ College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100, China. Electronic address: ybw090925@163.com.

PMID: 39798383
DOI: 10.1016/j.ijfoodmicro.2024.111052

Abstract

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_A 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_TEM-116 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.

Keywords: Comparative genomics; Pathogenicity; Y. frederiksenii; Y. intermedia; Y. kristensenii.