Skip to main content
SpringerLink
Log in

Effects of bifidobacteria-produced exopolysaccharides on human gut microbiota in vitro

  • Biotechnological products and process engineering
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Exopolysaccharides (EPSs) are carbohydrate polymers that are synthesized and present on the surface of bifidobacteria. Due to their potential applications in diverse sectors, such as food, biotechnology, cosmetics, and medicine, EPSs synthesized by bifidobacteria have recently attracted more attention. EPS production not only has benefits in food and health but also has effects on probiotics in the microbial ecosystem. In this study, we investigated the interaction between bifidobacteria EPSs and human gut microbiota in vitro using thin-layer chromatography, 16S rDNA high-throughput sequencing, and gas chromatography. The results showed that human gut microbiota has the capacity to degrade EPSs, although the degradation rate was approximately 50% after fermenting for 48 h. On the other hand, EPSs regulate the human gut microbiota. Fermented samples in the VI_Bif group clustered together according to the bacterial community compared to the VI_Starch group, in which starch was added as a carbon source. The bifidobacteria EPS promoted the growth of phylum Deinococcus_Thermus, class Deinococci, order Deinococcales, and genus Coprococcus. EPSs also increased the production of propionic acid compared to the starch group. The detection results of Dionex ICS 5000 high-purity capillary ion chromatography system showed that EPSs had absorption peaks of fucose, rhamnose, galactose/acetyl glucosamine, glucose, and ribose, and the molecular proportion of these monosaccharides was approximately 2: 2: 440: 3: 53. The monosaccharide composition of this EPS appears to be more complex than previously reported for bifidobacteria EPS. Additional studies are needed to elucidate its structure and functions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen AP, Dinan TG, Clarke G, Cryan JF (2017) A psychology of the human brain-gut-microbiome axis. Soc Personal Psychol Compass 11:e12309

    Article  PubMed  PubMed Central  Google Scholar 

  • Arboleya S, Watkins C, Stanton C, Ross RP (2016) Gut bifidobacteria populations in human health and aging. Front Microbiol 7:1204

    Article  PubMed  PubMed Central  Google Scholar 

  • Arora T, Backhed F (2016) The gut microbiota and metabolic disease: current understanding and future perspectives. J Intern Med 280:339–349

    Article  CAS  PubMed  Google Scholar 

  • Bron PA, van Baarlen P, Kleerebezem M (2011) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10:66–78

    Article  CAS  PubMed  Google Scholar 

  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  CAS  PubMed  Google Scholar 

  • Coombes JL, Powrie F (2008) Dendritic cells in intestinal immune regulation. Nat Rev Immunol 8:435–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dennis KL, Wang Y, Blatner NR, Wang S, Saadalla A, Trudeau E, Roers A, Weaver CT, Lee JJ, Gilbert JA, Chang EB, Khazaie K (2013) Adenomatous polyps are driven by microbe-instigated focal inflammation and are controlled by IL-10-producing T cells. Cancer Res 73:5905–5913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duffy LC, Zielezny MA, Riepenhoff-Talty M, Dryja D, Sayahtaheri-Altaie S, Griffiths E, Ruffin D, Barrett H, Ogra PL (1994a) Reduction of virus shedding by B. bifidum in experimentally induced MRV infection. Statistical application for ELISA. Dig Dis Sci 39:2334–2340

    Article  CAS  PubMed  Google Scholar 

  • Duffy LC, Zielezny MA, Riepenhoff-Talty M, Dryja D, Sayahtaheri-Altaie S, Griffiths E, Ruffin D, Barrett H, Rossman J, Ogra PL (1994b) Effectiveness of Bifidobacterium bifidum in mediating the clinical course of murine rotavirus diarrhea. Pediatr Res 35:690–695

    Article  CAS  PubMed  Google Scholar 

  • Freitas F, Alves VD, Reis MA (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29:388–398

    Article  CAS  PubMed  Google Scholar 

  • Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T, Taylor TD, Itoh K, Kikuchi J, Morita H, Hattori M, Ohno H (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469:543–547

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J (2009) Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58:1509–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerhardt S, Mohajeri MH (2018) Changes of colonic bacterial composition in Parkinson’s disease and other neurodegenerative diseases. Nutrients 10(6):E708

    Article  CAS  PubMed  Google Scholar 

  • Gueimonde M, Margolles A, de los Reyes-Gavilan CG, Salminen S (2007) Competitive exclusion of enteropathogens from human intestinal mucus by Bifidobacterium strains with acquired resistance to bile--a preliminary study. Int J Food Microbiol 113:228–232

    Article  PubMed  Google Scholar 

  • Hidalgo-Cantabrana C, Lopez P, Gueimonde M, de Los Reyes-Gavilan CG, Suarez A, Margolles A, Ruas-Madiedo P (2012) Immune modulation capability of exopolysaccharides synthesised by lactic acid bacteria and bifidobacteria. Probiotics Antimicrob Proteins 4:227–237

    Article  CAS  PubMed  Google Scholar 

  • Hidalgo-Cantabrana C, Sanchez B, Milani C, Ventura M, Margolles A, Ruas-Madiedo P (2014) Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Appl Environ Microbiol 80:9–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosono A, Lee J, Ametani A, Natsume M, Hirayama M, Adachi T, Kaminogawa S (1997) Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101-4. Biosci Biotechnol Biochem 61:312–316

    Article  CAS  PubMed  Google Scholar 

  • Lebeer S, Vanderleyden J, De Keersmaecker SC (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8:171–184

    Article  CAS  PubMed  Google Scholar 

  • Lee IC, Caggianiello G, van S, Taverne N, Meijerink M, Bron PA, Spano G, Kleerebezem M (2016) Strain-specific features of extracellular polysaccharides and their impact on Lactobacillus plantarum-host interactions. Appl Environ Microbiol 82:3959–3970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei F, Yin Y, Wang Y, Deng B, Yu HD, Li L, Xiang C, Wang S, Zhu B, Wang X (2012) Higher-level production of volatile fatty acids in vitro by chicken gut microbiotas than by human gut microbiotas as determined by functional analyses. Appl Environ Microbiol 78:5763–5772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Yang H, Yin Z, Jiang X, Zhong H, Qiu D, Zhu F, Li R (2017) Remodeling of the gut microbiota and structural shifts in preeclampsia patients in South China. Eur J Clin Microbiol Infect Dis 36:713–719

    Article  CAS  PubMed  Google Scholar 

  • Moslemi M, Mazaheri Nezhad Fard R, Hosseini SM, Homayouni-Rad A, Mortazavian AM (2016) Incorporation of Propionibacteria in fermented milks as a probiotic. Crit Rev Food Sci Nutr 56:1290–1312

    Article  CAS  PubMed  Google Scholar 

  • O’Callaghan A, van Sinderen D (2016) Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 7:925

    PubMed  PubMed Central  Google Scholar 

  • Perdigon G, Alvarez S, Rachid M, Aguero G, Gobbato N (1995) Immune system stimulation by probiotics. J Dairy Sci 78:1597–1606

    Article  CAS  PubMed  Google Scholar 

  • Petrov VA, Saltykova IV, Zhukova IA, Alifirova VM, Zhukova NG, Dorofeeva YB, Tyakht AV, Kovarsky BA, Alekseev DG, Kostryukova ES, Mironova YS, Izhboldina OP, Nikitina MA, Perevozchikova TV, Fait EA, Babenko VV, Vakhitova MT, Govorun VM, Sazonov AE (2017) Analysis of gut microbiota in patients with Parkinson’s disease. Bull Exp Biol Med 162:734–737

    Article  CAS  PubMed  Google Scholar 

  • Picard C, Fioramonti J, Francois A, Robinson T, Neant F, Matuchansky C (2005) Review article: bifidobacteria as probiotic agents -- physiological effects and clinical benefits. Aliment Pharmacol Ther 22:495–512

    Article  CAS  PubMed  Google Scholar 

  • Rehm BH (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8:578–592

    Article  CAS  PubMed  Google Scholar 

  • Roberts CM, Fett WF, Osman SF, Eijey C, O’Connor JV, Hoover DG (1995) Exopolysaccharide production by Bifidobacterium longum BB-79. J Appl Bacteriol 78:463–468

    Article  CAS  Google Scholar 

  • Ruiz L, Delgado S, Ruas-Madiedo P, Sanchez B, Margolles A (2017) Bifidobacteria and their molecular communication with the immune system. Front Microbiol 8:2345

    Article  PubMed  PubMed Central  Google Scholar 

  • Russell DA, Ross RP, Fitzgerald GF, Stanton C (2011) Metabolic activities and probiotic potential of bifidobacteria. Int J Food Microbiol 149:88–105

    Article  CAS  PubMed  Google Scholar 

  • Rycroft CE, Jones MR, Gibson GR, Rastall RA (2001) Fermentation properties of gentio-oligosaccharides. Lett Appl Microbiol 32:156–161

    Article  CAS  PubMed  Google Scholar 

  • Salazar N, Gueimonde M, Hernandez-Barranco AM, Ruas-Madiedo P, de los Reyes-Gavilan CG (2008) Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Appl Environ Microbiol 74:4737–4745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salazar N, Ruas-Madiedo P, Kolida S, Collins M, Rastall R, Gibson G, de Los Reyes-Gavilan CG (2009) Exopolysaccharides produced by Bifidobacterium longum IPLA E44 and Bifidobacterium animalis subsp. lactis IPLA R1 modify the composition and metabolic activity of human faecal microbiota in pH-controlled batch cultures. Int J Food Microbiol 135:260–267

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Xu J, Li Z, Huang Y, Yuan Y, Wang J, Zhang M, Hu S, Liang Y (2018) Analysis of gut microbiota diversity and auxiliary diagnosis as a biomarker in patients with schizophrenia: a cross-sectional study. Schizophr Res 197:470–477

    Article  PubMed  Google Scholar 

  • van de Guchte M, Blottiere HM, Dore J (2018) Humans as holobionts: implications for prevention and therapy. Microbiome 6:81

    Article  PubMed  PubMed Central  Google Scholar 

  • Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20:467–476

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu MH, Pan TM, Wu YJ, Chang SJ, Chang MS, Hu CY (2010) Exopolysaccharide activities from probiotic Bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol 144:104–110

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of exopolysaccharide fractions from Bifidobacterium animalis RH. Anaerobe 17:226–231

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Bian G, Su Y, Zhu W (2014) Comparison of faecal microbial community of lantang, bama, erhualian, meishan, xiaomeishan, duroc, landrace, and yorkshire sows. As-Aust. J Anim Sci 27:898–906

    CAS  Google Scholar 

  • Zhang Z, Xie J, Zhang F, Linhardt RJ (2007) Thin-layer chromatography for the analysis of glycosaminoglycan oligosaccharides. Anal Biochem 371:118–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank LetPub (www.letpub.com) for providing linguistic assistance during the preparation of this manuscript.

Funding

This study was funded by the Key Research and Development Plan of Zhejiang Province (2017C02G4010648), the Hunan Natural Science Foundation (No. 2018JJ3200), and the National Nature Science Foundation of China (No. 31741109).

Author information

Authors and Affiliations

  1. College of Food and Biological Engineering, Zhejiang Gongshang University, Hangzhou, Zhejiang, China

    Guiyang Liu & Qing Gu

  2. State Key Laboratory of Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China

    Guiyang Liu, Huahai Chen, Junkui Chen, Xin Wang & Yeshi Yin

  3. Key Laboratory of Comprehensive Utilization of Advantage Plants Resources in Hunan South, College of Chemistry and Bioengineering, Hunan University of Science and Engineering, Yongzhou, Hunan, China

    Huahai Chen & Yeshi Yin

Authors
  1. Guiyang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huahai Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junkui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qing Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yeshi Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qing Gu or Yeshi Yin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Zhejiang Gongshang University research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 940 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, G., Chen, H., Chen, J. et al. Effects of bifidobacteria-produced exopolysaccharides on human gut microbiota in vitro. Appl Microbiol Biotechnol 103, 1693–1702 (2019). https://doi.org/10.1007/s00253-018-9572-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9572-6

Keywords

Search

Navigation