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The implication of viability and pathogenicity by truncated lipopolysaccharide in Yersinia enterocolitica

  • Applied Genetics and Molecular Biotechnology
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Abstract

The fast envelope stress responses play a key role in the transmission and pathogenesis of Yersinia enterocolitica, one of the most common foodborne pathogens. Our previous study showed that deletion of the waaF gene, essential for the biosynthesis of lipopolysaccharide (LPS) core polysaccharides, led to the formation of a truncated LPS structure and induced cell envelope stress. This envelope stress may disturb the intracellular signal transduction, thereby affecting the physiological functions of Y. enterocolitica. In this study, truncated LPS caused by waaF deletion was used as a model of envelope stress in Y. enterocolitica. We investigated the mechanisms of envelope stress responses and the cellular functions affected by truncated LPS. Transcriptome analysis and phenotypic validation showed that LPS truncation reduced flagellar assembly, bacterial chemotaxis, and inositol phosphate metabolism, presenting lower pathogenicity and viability both in vivo and in vitro environments. Further 4D label-free phosphorylation analysis confirmed that truncated LPS perturbed multiple intracellular signal transduction pathways. Specifically, a comprehensive discussion was conducted on the mechanisms by which chemotactic signal transduction and Rcs system contribute to the inhibition of chemotaxis. Finally, the pathogenicity of Y. enterocolitica with truncated LPS was evaluated in vitro using IPEC-J2 cells as models, and it was found that truncated LPS exhibited reduced adhesion, invasion, and toxicity of Y. enterocolitica to IPEC-J2 cells. Our research provides an understanding of LPS in the regulation of Y. enterocolitica viability and pathogenicity and, thus, opening new avenues to develop novel food safety strategies or drugs to prevent and control Y. enterocolitica infections.

Key points

• Truncated LPS reduces flagellar assembly, chemotaxis, and inositol phosphate metabolism in Y. enterocolitica.

• Truncated LPS reduces adhesion, invasion, and toxicity of Y. enterocolitica to IPEC-J2 cells.

• Truncated LPS regulates intracellular signal transduction of Y. enterocolitica.

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Data availability

All data included in this study are available upon request by contact with the corresponding author.

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Acknowledgements

We gratefully acknowledge the excellent research facilities and support provided by the Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, throughout this study.

Funding

The study was funded by the China Postdoctoral Science Foundation-funded project (2021M703439).

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Authors and Affiliations

  1. Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, College of Bioengineering, Tianjin University of Science and Technology, Tianjin, 300457, China

    Fan Wu & Xixian Xie

  2. Laboratory of Nutrient Resources and Synthetic Biology, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Science, Tianjin, 300308, China

    Fengyun Ren, Jiao Meng & Xin Wu

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  1. Fan Wu
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  2. Fengyun Ren
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  3. Xixian Xie
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  4. Jiao Meng
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Contributions

MJ, XXX, and WX conceived the study, designed experiments, and analyzed data. WF, RFY, and MJ performed experiments and/or analyzed data. WF and RFY wrote the manuscript. WX provided the key revisions to the article. All authors reviewed and commented on the final version of the manuscript.

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Correspondence to Xixian Xie or Jiao Meng.

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Wu, F., Ren, F., Xie, X. et al. The implication of viability and pathogenicity by truncated lipopolysaccharide in Yersinia enterocolitica. Appl Microbiol Biotechnol 107, 7165–7180 (2023). https://doi.org/10.1007/s00253-023-12785-w

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