Skip to main content
Log in

Lactobacillus plantarum HAC01 regulates gut microbiota and adipose tissue accumulation in a diet-induced obesity murine model

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The functional features of Lactobacillus plantarum HAC01 (HAC01), isolated from fermented Korean kimchi, were studied with regard to the fat mass, immunometabolic biomarkers and dysbiosis in a diet-induced obesity (DIO) murine model. L. rhamnosus GG (LGG) served as reference strain and a PBS-treated group as control. The administration of L. plantarum HAC01 resulted in reduction of the mesenteric adipose depot, the conjunctive tissue closely associated with the gastrointestinal tract, where lipid oxidative gene expression was upregulated compared to the control group. Metagenome analysis of intestinal microbiota showed that both strains HAC01 and LGG influenced specific bacterial families such as the Lachnospiraceae and Ruminococcaceae rather than the phyla Firmicutes and Bacteroidetes as a whole. The relative abundance of the Lachnospiraceae (phylum Firmicutes) was significantly higher in both LAB-treated groups than in the control. Comparing the impact of the two Lactobacillus strains on microbial composition in the gut also suggests strain-specific effects. The study emphasises the need for deeper studies into functional specificity of a probiotic organism at the strain level. Alleviation of obesity-associated dysbiosis by modulation of the gut microbiota appears to be associated with “indicator” bacterial taxa such as the family Lachnospiraceae. This may provide further insight into mechanisms basic to the mode of probiotic action against obesity and associated dysbiosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101(44):15718–15723. doi:10.1073/pnas.0407076101

    Article  PubMed  PubMed Central  Google Scholar 

  • Caricilli AM, Picardi PK, de Abreu LL, Ueno M, Prada PO, Ropelle ER, Hirabara SM, Castoldi Â, Vieira P, Camara NO (2011) Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. PLoS Biol 9(12):e1001212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll IM, Ringel-Kulka T, Siddle JP, Ringel Y (2012) Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol & Motility 24(6):521–e248

    Article  CAS  Google Scholar 

  • Consortium HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214

    Article  Google Scholar 

  • Cusi K (2010) The role of adipose tissue and lipotoxicity in the pathogenesis of type 2 diabetes. Curr Diabetes Rep 10(4):306–315

    Article  CAS  Google Scholar 

  • D’Argenio V, Salvatore F (2015) The role of the gut microbiome in the healthy adult status. Clin Chim Acta 451:97–102

    Article  PubMed  Google Scholar 

  • Gaspar JM, Thomas WK (2015) FlowClus: efficiently filtering and denoising pyrosequenced amplicons. BMC Bioinformatics 16:105. doi:10.1186/s12859-015-0532-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Gosalbes MJ, Durban A, Pignatelli M, Abellan JJ, Jimenez-Hernandez N, Perez-Cobas AE, Latorre A, Moya A (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 6(3):e17447. doi:10.1371/journal.pone.0017447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemarajata P, Versalovic J (2012) Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol 6(1):39–51. doi:10.1177/1756283X12459294

    Article  Google Scholar 

  • Holzapfel WH, Wood BJ (2014) Lactic acid bacteria: biodiversity and taxonomy. John Wiley & Sons, Chichester

    Book  Google Scholar 

  • Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155(7):1451–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji YS, Kim HN, Park HJ, Lee JE, Yeo SY, Yang JS, Park SY, Yoon HS, Cho GS, Franz CM, Bomba A, Shin HK, Holzapfel WH (2012) Modulation of the murine microbiome with a concomitant anti-obesity effect by Lactobacillus rhamnosus GG and Lactobacillus sakei NR28. Benef Microbes 3(1):13–22. doi:10.3920/BM2011.0046

    Article  CAS  PubMed  Google Scholar 

  • Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, Okano M, Kagoshima M, Tsuchida T (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64(6):636–643. doi:10.1038/ejcn.2010.19

    Article  CAS  PubMed  Google Scholar 

  • Kim B, Park K-Y, Ji Y, Park S, Holzapfel W, Hyun C-K (2016) Protective effects of Lactobacillus rhamnosus GG against dyslipidemia in high-fat diet-induced obese mice. Biochem Biophys Res Comm 473(2):530–536

    Article  CAS  PubMed  Google Scholar 

  • Kim S-W, Park K-Y, Kim B, Kim E, Hyun C-K (2013) Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Comm 431(2):258–263

    Article  CAS  PubMed  Google Scholar 

  • Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, Terasawa K, Kashihara D, Hirano K, Tani T, Takahashi T, Miyauchi S, Shioi G, Inoue H, Tsujimoto G (2013) The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun 4:1829. doi:10.1038/ncomms2852

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwok L, Guo Z, Zhang J, Wang L, Qiao J, Hou Q, Zheng Y, Zhang H (2015) The impact of oral consumption of Lactobacillus plantarum P-8 on faecal bacteria revealed by pyrosequencing. Benef Microbes 6(4):405–413

    Article  CAS  PubMed  Google Scholar 

  • Kwon H-K, So J-S, Lee C-G, Sahoo A, Yi H-J, Park J-N, S-y L, Hwang K-C, Jun C-D, Chun J-S (2008) Foxp3 induces IL-4 gene silencing by affecting nuclear translocation of NFκB and chromatin structure. Mol Immunol 45(11):3205–3212

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Yang S, Lin H, Huang J, Watkins PA, Moser AB, DeSimone C, Xy S, Diehl AM (2003) Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatol 37(2):343–350

    Article  CAS  Google Scholar 

  • Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maghbooli Z, Hossein-nezhad A (2015) Transcriptome and molecular endocrinology aspects of epicardial adipose tissue in cardiovascular diseases: a systematic review and meta-analysis of observational studies. Biomed Res Int 2015:926567 12 pages, http://dx.doi.org/10.1155/2015/926567

    Article  PubMed  PubMed Central  Google Scholar 

  • Masood MI, Qadir MI, Shirazi JH, Khan IU (2011) Beneficial effects of lactic acid bacteria on human beings. Crit Rev Microbiol 37(1):91–98

    Article  PubMed  Google Scholar 

  • Miyoshi M, Ogawa A, Higurashi S, Kadooka Y (2014) Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice. Europ J Nutr 53(2):599–606

    Article  Google Scholar 

  • O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7(7):688–693. doi:10.1038/sj.embor.7400731

    Article  PubMed  PubMed Central  Google Scholar 

  • Oda N, Imamura S, Fujita T, Uchida Y, Inagaki K, Kakizawa H, Hayakawa N, Suzuki A, Takeda J, Horikawa Y (2008) The ratio of leptin to adiponectin can be used as an index of insulin resistance. Metabolism 57(2):268–273

    Article  CAS  PubMed  Google Scholar 

  • Park S, Ji Y, Park H, Lee K, Park H, Beck BR, Shin H, Holzapfel WH (2016) Evaluation of functional properties of lactobacilli isolated from Korean white kimchi. Food Control 69:5–12. doi:10.1016/j.foodcont.2016.04.037

    Article  CAS  Google Scholar 

  • Parvez S, Malik K, Ah Kang S, Kim HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100(6):1171–1185

    Article  CAS  PubMed  Google Scholar 

  • Perez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A, Eismann K, Otto W, Rojo D, Bargiela R, von Bergen M, Neulinger SC, Daumer C, Heinsen FA, Latorre A, Barbas C, Seifert J, dos Santos VM, Ott SJ, Ferrer M, Moya A (2013) Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 62(11):1591–1601. doi:10.1136/gutjnl-2012-303184

    Article  CAS  PubMed  Google Scholar 

  • Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, Stombaugh J, Knight R, Ley RE, Leibel RL (2012) Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity (Silver Spring) 20(4):738–747. doi:10.1038/oby.2011.111

    Article  CAS  Google Scholar 

  • Richardson VR, Smith KA, Carter AM (2013) Adipose tissue inflammation: feeding the development of type 2 diabetes mellitus. Immunobiol 218(12):1497–1504

    Article  CAS  Google Scholar 

  • Ritze Y, Bárdos G, Claus A, Ehrmann V, Bergheim I, Schwiertz A, Bischoff SC (2014) Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice. PLoS One 9(1):e80169

    Article  PubMed  PubMed Central  Google Scholar 

  • Roos S, Dicksved J, Tarasco V, Locatelli E, Ricceri F, Grandin U, Savino F (2013) 454 pyrosequencing analysis on faecal samples from a randomized DBPC trial of colicky infants treated with Lactobacillus reuteri DSM 17938. PLoS One 8(2):e56710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanz Y, Rastmanesh R, Agostonic C (2013) Understanding the role of gut microbes and probiotics in obesity: how far are we? Pharmacol Res 69(1):144–155

    Article  PubMed  Google Scholar 

  • Sethi JK, Vidal-Puig AJ (2007) Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res 48(6):1253–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Rev Microbiol 9(4):279–290

    Article  CAS  Google Scholar 

  • Wang J, Tang H, Zhang C, Zhao Y, Derrien M, Rocher E, van- Hylckama Vlieg JE, Strissel K, Zhao L, Obin M, Shen J (2015) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J 9(1):1–15. doi:10.1038/ismej.2014.99

    Article  PubMed  Google Scholar 

  • Xu H (2013) Obesity and metabolic inflammation. Drug Discovery Today: Disease Mechanisms 10(1):e21–e25

    Article  Google Scholar 

  • Zeng J, Li YQ, Zuo XL, Zhen YB, Yang J, Liu CH (2008) Clinical trial: effect of active lactic acid bacteria on mucosal barrier function in patients with diarrhoea-predominant irritable bowel syndrome. Alim Pharmacol Therap 28(8):994–1002

  • Zhang C, Zhang M, Pang X, Zhao Y, Wang L, Zhao L (2012) Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J 6(10):1848–1857. doi:10.1038/ismej.2012.27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the Korea Institute of Planning and Evaluation Technology in the Ministry of Food, Agriculture, Forestry and Fisheries (IPET), as part of the research project “Modulation of the microbiome with a concomitant anti-obesity effect by Kimchi originated probiotic feeding” (911053-1). We also gratefully acknowledge support from the Bio- and Medical Technology Development Program of the National Research Foundation (NRF) funded by the Ministry of Science, ICT and Future Planning (2016M3A9A5923160).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wilhelm H. Holzapfel.

Ethics declarations

All applicable international, national and institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Ethical approval

All animal experiments and protocols were approved by the Committee on the Ethics of Animal Experiments of Handong Global University and were in agreement with the guidelines set forth by the Korean Association for Laboratory Animals.

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

WH was funded by Ministry of Food, Agriculture, Forestry and Fisheries (IPET), as part of the research project “Modulation of the microbiome with a concomitant anti-obesity effect by Kimchi originated probiotic feeding” (911053-1).

Electronic supplementary material

ESM 1

(PDF 168 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, S., Ji, Y., Jung, HY. et al. Lactobacillus plantarum HAC01 regulates gut microbiota and adipose tissue accumulation in a diet-induced obesity murine model. Appl Microbiol Biotechnol 101, 1605–1614 (2017). https://doi.org/10.1007/s00253-016-7953-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7953-2

Keywords

Navigation