본문 바로가기
KERD
논문KCI 등재

Metabolic Regulation of Longevity and Immune Response in Caenorhabditis elegans by Ingestion of Lacticaseibacillus rhamnosus IDCC 3201 Using Multi-Omics Analysis

2

조회

0

다운로드

0

인용

0

참고문헌

키워드

주제분류생물학

초록

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 wellestablished 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 wellknown 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.

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 wellestablished 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 wellknown 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.

참고문헌 (49)

  1. Kim B, "Complete genome and two plasmids sequences of Lactiplantibacillus plantarum L55 for probiotic potentials", J. Anim. Sci. Technol, 65, pp.1341~1344 (2023)
  2. Morelli L, "FAO", WHO guidelines on probiotics : 10 years later, 2012, pp.46, S1~S2
  3. Lee D, "Perspectives and advances in probiotics and the gut microbiome in companion animals", J. Anim. Sci. Technol, 64, pp.197~217 (2022)
  4. Yang S, "Complete genome sequence of Lactiplantibacillus plantarum ST, a potential probiotic strain with antibacterial properties", J. Anim. Sci. Technol, 64, pp.183~186 (2022)
  5. Kim B, "Complete genome sequence of Limosilactobacillus fermentum JNU532as a probiotic candidate for the functional food and feed supplements", J. Anim. Sci. Technol, 65, pp.271~274 (2023)
  6. Kim JY, "Immunostimulatory effects of dairy probiotic strains Bifidobacterium animalis ssp. HY8002 and Lactobacillus plantarum HY7717", J. Anim. Sci. Technol, 64, pp.1117~1131 (2022)
  7. Kang AN, "Culturomic-, metagenomic-, and transcriptomic-based characterization of commensal lactic acid bacteria isolated from domestic dogs using Caenorhabditis elegans as a model for aging", J. Anim. Sci, 100, pp.skac323~ (2022)
  8. Jaafar M, "Dairy based-LAB improved constipation via increasing fecal bulk and decreasing concentration of fecal threonine while preserving colonic goblet cell count", Jaafar M, 66, pp.178~203 (2024)
  9. Kaletta T, "Finding function in novel targets: C. elegans as a model organism", Nat. Rev. Drug discov, 5, pp.387~398 (2006)
  10. Mahesh R, "Probiotics interactions and the modulation of major signalling pathways in host model organism Caenorhabditis elegans", Indian J. Microbiol, 61, pp.404~416 (2021)
  11. Clark LC, "Commensals, probiotics and pathogens in the Caenorhabditis elegans model", Cell. Microbiol, 16, pp.27~38 (2014)
  12. Choi H, "Molecular characterization and functionality of rumen-derived extracellular vesicles using a Caenorhabditis elegans animal model", J. Anim. Sci. Technol, 65, pp.652~663 (2023)
  13. Kang A, "Dietary supplementation with probiotics promotes weight loss by reshaping the gut microbiome and energy metabolism in obese dogs", Microbiol. Spectr, 0, pp.e02552-02523~
  14. Anderson SM, "Immunometabolism in Caenorhabditis elegans", PLoS Pathog, 16, pp.e1008897~ (2020)
  15. Wan QL, "Metabolomic signature associated with reproduction-regulated aging in Caenorhabditis elegans", Aging(Albany NY), 9, pp.447~474 (2017)
  16. Kim H, "Evaluation of probiotic characteristics of newly isolated lactic acid bacteria from dry-aged Hanwoo beef", Food Sci. Anim. Resour, 41, pp.468~480 (2021)
  17. Park MR, "Probiotic Lactobacillus fermentum strain JDFM216 stimulates the longevity and immune response of Caenorhabditis elegans through a nuclear hormone receptor", Sci. Rep, 8, pp.7441~ (2018)
  18. Kim Y, "Caenorhabditis elegans immune conditioning with the probiotic bacterium Lactobacillus acidophilus strain NCFM enhances gram-positive immune responses", Infect. Immun, 80, pp.2500~2508 (2012)
  19. Shen P, "Effects of conjugated linoleic acid(CLA)on fat accumulation, activity, and proteomics analysis in Caenorhabditis elegans", Food Chem, 249, pp.193~201 (2018)
  20. Ryu S, "Bacterial quality, prevalence of pathogens, and molecular characterization of biofilm-producing Staphylococcus aureus from Korean dairy farm environments", Animals, 11, pp.1306~ (2021)
  21. Bolger AM, "Trimmomatic : a flexible trimmer for Illumina sequence data", Bioinformatics, 30, pp.2114~2120 (2014)
  22. Kim D, "HISAT : a fast spliced aligner with low memory requirements", Nat. Methods, 12, pp.357~360 (2015)
  23. Liao Y, "featureCounts : an efficient general purpose program for assigning sequence reads to genomic features", Bioinformatics, 30, pp.923~930 (2014)
  24. Robinson MD, "edgeR : a Bioconductor package for differential expression analysis of digital gene expression data", Bioinformatics, 26, pp.139~140 (2010)
  25. Yoo J, "Enhanced γ-aminobutyric acid and sialic acid in fermented deer antler velvet and immune promoting effects", J. Anim. Sci. Technol, 64, pp.166~182 (2022)
  26. Williams NT, "Probiotics", Am. J. Health Syst. Pharm, 67, pp.449~458 (2010)
  27. Oh YJ, "Complete genome sequence of probiotic Lactobacillus johnsonii 7409N31isolated from a healthy Hanwoo calf", J. Anim. Sci. Technol, 65, pp.890~893 (2023)
  28. Hammes WP, "The genera of lactic acid bacteria", pp.19~54 (1995), Springer
  29. Vasquez R, "Gut microbiome-produced metabolites in pigs : a review on their biological functions and the influence of probiotics", J. Anim. Sci. Technol, 64, pp.671~695 (2022)
  30. Grompone G, "Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans", PLoS One, 7, pp.e52493~ (2012)
  31. Oh S, "Lactobacillus rhamnosus strain GG influences on the longevity and immune response of Caenorhabditis elegans to foodborne pathogens with stimulating microRNAs", FASEB J, 29, pp.853~ (2015)
  32. Monteagudo-Mera A, "Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health", Appl. Microbiol. Biotechnol, 103, pp.6463~6472 (2019)
  33. Poupet C, "Lactobacillus rhamnosus Lcr35 as an effective treatment for preventing Candida albicans infection in the invertebrate model Caenorhabditis elegans : first mechanistic insights", PLoS One, 14, pp.e0216184~ (2019)
  34. Shtonda BB, "Dietary choice behavior in Caenorhabditis elegans", J. Exper. Biol, 209, pp.89~102 (2006)
  35. Kim YJ, "Effects of different Bacillus licheniformis and Bacillus subtilis ratios on nutrient digestibility, fecal microflora, and gas emissions of growing pigs", J. Anim. Sci. Technol, 64, pp.291~301 (2022)
  36. Pees B, "Effector and regulator: diverse functions of C. elegans C-type lectinlike domain proteins", PLoS Pathog, 17, pp.e1009454~ (2021)
  37. Schulenburg H, "Specificity of the innate immune system and diversity of Ctype lectin domain(CTLD)proteins in the nematode Caenorhabditis elegans", Immunobiology, 213, pp.237~250 (2008)
  38. O’Rourke D, "Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum", Genome Res, 16, pp.1005~1016 (2006)
  39. Leippe M, "Antimicrobial and cytolytic polypeptides of amoeboid protozoa-effector molecules of primitive phagocytes", Dev. Comp. Immunol, 23, pp.267~279 (1999)
  40. Ciancio A, "Invertebrate Bacteriology", pp.205~239 (2016), Springer
  41. Amador-Noguez D, "Gene expression profile of long-lived Ames dwarf mice and Little mice", Aging Cell, 3, pp.423~441 (2004)
  42. Perron JT, "Maintenance of tricarboxylic acid cycle kinetics in Brown–Norway Fischer 344 rats may translate to longevity", Neurosc. Lett, 281, pp.91~94 (2000)
  43. Edwards CB, "Malate and fumarate extend lifespan in Caenorhabditis elegans", PLoS One, 8, pp.e58345~ (2013)
  44. Zarse K, "Impaired respiration is positively correlated with decreased life span in Caenorhabditis elegans models of Friedreich Ataxia", FASEB J, 21, pp.1271~1275 (2007)
  45. Ryu S, "Complete genome sequences of Lactococcus lactis JNU 534, a potential food and feed preservative", J. Anim. Sci. Technol, 64, pp.599~602 (2022)
  46. Fernández MF, "Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract", J. Appl. Microbiol, 94, pp.449~455 (2003)
  47. Dinev T, "Antimicrobial activity of Lactobacillus plantarum against pathogenic and food spoilage microorganisms: a review", Bulg. J. Vet. Med, 21 (2018)[DOI]
  48. Shu Q, "Immune protection mediated by the probiotic Lactobacillus rhamnosus HN001(DR20™)against Escherichia coli O157 : H7 infection in mice", FEMS Immunol. Med. Microbiol, 34, pp.59~64 (2002)

관련 논문AI추천

Probiotic Potential of Enterococcus faecium Isolated from Chicken Cecum with Immunomodulating Activity and Promoting Longevity in Caenorhabditis elegans고종호, 권가영, 박근태, 심인숙, 임영희한국미생물·생명공학회 · Journal of Microbiology and Biotechnology2018 · 제28권 제6호Lactobacillus rhamnosus CBT-LR5 Improves Lipid Metabolism by Enhancing Vitamin AbsorptionChung Myung Jun, Kim Dong-Jin, Kim Tai Yeub, Ryu Yongku, Yoon Yeo-Sang한국미생물·생명공학회 · 한국미생물·생명공학회지2022 · 제50권 제4호Increased Amino Acid Absorption Mediated by Lacticaseibacillus rhamnosus IDCC 3201 in High-Protein Diet-Fed MiceJeon Hyeon Ji, Jung Young Hoon, Kim Hayoung, Kim Jungyeon, Lee Minjee, Moon Jin Seok, Yang Jungwoo한국미생물·생명공학회 · Journal of Microbiology and Biotechnology2023 · 제33권 제4호Bacillus licheniformis Isolated from Korean Traditional Food Sources Enhances the Resistance of Caenorhabditis elegans to Infection by Staphylococcus aureus고광웅, 김종남, 박미리, 송민호, 오상남, 윤현선, 조호성, Do-Youn Jeong, Ju Hee Heo, Nag-Jin Choi, Seok Jun Son, Seung-Wha Jo, Young Hoon Kim한국미생물·생명공학회 · Journal of Microbiology and Biotechnology2014 · 제24권 제8호Transcriptional Response and Enhanced Intestinal Adhesion Ability of Lactobacillus rhamnosus GG after Acid Stress고혁진, 방미선, 오세종, 용청충, 최인걸한국미생물·생명공학회 · Journal of Microbiology and Biotechnology2018 · 제28권 제10호Modulation of the Gut Microbiome and Metabolomes by Fermentation Using a Probiotic Complex in a Dysbiosis-Associated Fecal ModelBang Won Yeong, Jeong Hye Min, Jeon Hyeon Ji, Jung Young Hoon, Kim Hayoung, Kwon Hyeji, Lee Han Bin, Lee Jongkyun, Lee Kyu-Shik, Moon Jin Seok, Yang Jungwoo한국미생물·생명공학회 · Journal of Microbiology and Biotechnology2025 · 제35권

이 간행물의 다른 논문 (19건)