Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Metabolic Regulation of Longevity and Immune Response in Caenorhabditis elegans by Ingestion of Lacticaseibacillus rhamnosus IDCC 3201 Using Multi-Omics Analysis

  • Daniel Junpyo Lee (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Ju Young Eor (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Min-Jin Kwak (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Junbeom Lee (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • An Na Kang (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Daye Mun (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Hyejin Choi (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University) ;
  • Minho Song (Department of Animal Science and Biotechnology, Chungnam National University) ;
  • Jong Nam Kim (Department of Food Science & Nutrition, Dongseo University) ;
  • Jun-Mo Kim (Department of Animal Science and Technology, Chung-Ang University) ;
  • Jungwoo Yang (Department of Microbiology, College of Medicine, Dongguk University) ;
  • Hyung Wook Kim (College of Life Sciences, Sejong University) ;
  • Sangnam Oh (Department of Functional Food and Biotechnology, Jeonju University) ;
  • Younghoon Kim (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University)
  • Received : 2024.02.16
  • Accepted : 2024.03.27
  • Published : 2024.05.28
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Abstract

Probiotics, specifically Lacticaseibacillus rhamnosus, have garnered attention for their potential health benefits. This study focuses on evaluating the probiotic properties of candidate probiotics L. rhamnosus IDCC 3201 (3201) using the Caenorhabditis elegans surrogate animal model, a well-established in vivo system for studying host-bacteria interactions. The adhesive ability to the host's gastrointestinal tract is a crucial criterion for selecting potential probiotic bacteria. Our findings demonstrated that 3201 exhibits significantly higher adhesive capabilities compared with Escherichia coli OP50 (OP50), a standard laboratory food source for C. elegans and is comparable with the widely recognized probiotic L. rhamnosus GG (LGG). In lifespan assay, 3201 significantly increased the longevity of C. elegans compared with OP50. In addition, preconditioning with 3201 enhanced C. elegans immune response against four different foodborne pathogenic bacteria. To uncover the molecular basis of these effects, transcriptome analysis elucidated that 3201 modulates specific gene expression related to the innate immune response in C. elegans. C-type lectin-related genes and lysozyme-related genes, crucial components of the immune system, showed significant upregulation after feeding 3201 compared with OP50. These results suggested that preconditioning with 3201 may enhance the immune response against pathogens. Metabolome analysis revealed increased levels of fumaric acid and succinic acid, metabolites of the citric acid cycle, in C. elegans fed with 3201 compared with OP50. Furthermore, there was an increase in the levels of lactic acid, a well-known antimicrobial compound. This rise in lactic acid levels may have contributed to the robust defense mechanisms against pathogens. In conclusion, this study demonstrated the probiotic properties of the candidate probiotic L. rhamnosus IDCC 3201 by using multi-omics analysis.

Keywords

Acknowledgement

This study was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET-321037-5) and by a National Research Foundation of Korea Grant funded by the Korean government (MEST) (NRF-2021R1A2C3011051) and "Cooperative Research Program for Agriculture Science & Technology Development (Project No. RS-2023-00225838)" Rural Development Administration, Republic of Korea.

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