Bifidobacteria can protect from enteropathogenic infection through production of acetate (original) (raw)

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Gene Expression Omnibus

Data deposits

Microarray data have been deposited in the NCBI Gene Expression Omnibus under accession number GSE13061. Sequences for the B. longum genomes have been deposited in the DNA Data Bank of Japan, GenBank and the EMBL Nucleotide Sequence Database under accession numbers AP010888, AP010889, AP010890, AP010891 and AP010892.

References

  1. Picard, C. et al. Bifidobacteria as probiotic agents—physiological effects and clinical benefits. Aliment. Pharmacol. Ther. 22, 495–512 (2005)
    Article CAS Google Scholar
  2. Ventura, M. et al. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nature Rev. Microbiol. 7, 61–71 (2009)
    Article CAS Google Scholar
  3. Jia, W., Li, H., Zhao, L. & Nicholson, J. K. Gut microbiota: a potential new territory for drug targeting. Nature Rev. Drug Discov. 7, 123–129 (2008)
    Article CAS Google Scholar
  4. Mazmanian, S. K. & Kasper, D. L. The love–hate relationship between bacterial polysaccharides and the host immune system. Nature Rev. Immunol. 6, 849–858 (2006)
    Article CAS Google Scholar
  5. Saulnier, D. M., Spinler, J. K., Gibson, G. R. & Versalovic, J. Mechanisms of probiosis and prebiosis: considerations for enhanced functional foods. Curr. Opin. Biotechnol. 20, 135–141 (2009)
    Article CAS Google Scholar
  6. Sonnenburg, J. L., Chen, C. T. & Gordon, J. I. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol. 4, e413 (2006)
    Article Google Scholar
  7. Garmendia, J., Frankel, G. & Crepin, V. F. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect. Immun. 73, 2573–2585 (2005)
    Article CAS Google Scholar
  8. Tarr, P. I., Gordon, C. A. & Chandler, W. L. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365, 1073–1086 (2005)
    CAS PubMed Google Scholar
  9. Kitajima, H., Ida, S. & Fujimura, M. Daily bowel movements and Escherichia coli O157 infection. Arch. Dis. Child. 87, 335–336 (2002)
    Article CAS Google Scholar
  10. Eaton, K. A. et al. Pathogenesis of renal disease due to enterohemorrhagic Escherichia coli in germ-free mice. Infect. Immun. 76, 3054–3063 (2008)
    Article CAS Google Scholar
  11. Asahara, T. et al. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157:H7. Infect. Immun. 72, 2240–2247 (2004)
    Article CAS Google Scholar
  12. Gagnon, M., Kheadr, E. E., Dabour, N., Richard, D. & Fliss, I. Effect of Bifidobacterium thermacidophilum probiotic feeding on enterohemorrhagic Escherichia coli O157:H7 infection in BALB/c mice. Int. J. Food Microbiol. 111, 26–33 (2006)
    Article Google Scholar
  13. Yoshimura, K., Matsui, T. & Itoh, K. Prevention of Escherichia coli O157:H7 infection in gnotobiotic mice associated with Bifidobacterium strains. Antonie Van Leeuwenhoek 97, 107–117 (2010)
    Article CAS Google Scholar
  14. Li, J., Pircher, P. C., Schulman, I. G. & Westin, S. K. Regulation of complement C3 expression by the bile acid receptor FXR. J. Biol. Chem. 280, 7427–7434 (2005)
    Article CAS Google Scholar
  15. Laffitte, B. A. et al. LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl Acad. Sci. USA 98, 507–512 (2001)
    Article ADS CAS Google Scholar
  16. Antonio, V., Janvier, B., Brouillet, A., Andreani, M. & Raymondjean, M. Oxysterol and 9-_cis_-retinoic acid stimulate the group IIA secretory phospholipase A2 gene in rat smooth-muscle cells. Biochem. J. 376, 351–360 (2003)
    Article CAS Google Scholar
  17. Zelcer, N. & Tontonoz, P. Liver X receptors as integrators of metabolic and inflammatory signaling. J. Clin. Invest. 116, 607–614 (2006)
    Article CAS Google Scholar
  18. Sethi, S. et al. Oxidized omega-3 fatty acids in fish oil inhibit leukocyte–endothelial interactions through activation of PPARα. Blood 100, 1340–1346 (2002)
    Article CAS Google Scholar
  19. Staels, B. et al. Activation of human aortic smooth-muscle cells is inhibited by PPARα but not by PPARγ activators. Nature 393, 790–793 (1998)
    Article ADS CAS Google Scholar
  20. Delerive, P., Gervois, P., Fruchart, J. C. & Staels, B. Induction of IκBα expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-α activators. J. Biol. Chem. 275, 36703–36707 (2000)
    Article CAS Google Scholar
  21. Sela, D. A. et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl Acad. Sci. USA 105, 18964–18969 (2008)
    Article ADS CAS Google Scholar
  22. Schell, M. A. et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl Acad. Sci. USA 99, 14422–14427 (2002)
    Article ADS CAS Google Scholar
  23. Parche, S. et al. Sugar transport systems of Bifidobacterium longum NCC 2705. J. Mol. Microbiol. Biotechnol. 12, 9–19 (2007)
    Article CAS Google Scholar
  24. Yuan, J. et al. A proteome reference map and proteomic analysis of Bifidobacterium longum NCC 2705. Mol. Cell. Proteomics 5, 1105–1118 (2006)
    Article CAS Google Scholar
  25. Annison, G., Illman, R. J. & Topping, D. L. Acetylated, propionylated or butyrylated starches raise large bowel short-chain fatty acids preferentially when fed to rats. J. Nutr. 133, 3523–3528 (2003)
    Article CAS Google Scholar
  26. Tedelind, S., Westberg, F., Kjerrulf, M. & Vidal, A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J. Gastroenterol. 13, 2826–2832 (2007)
    Article CAS Google Scholar
  27. Kles, K. A. & Chang, E. B. Short-chain fatty acids impact on intestinal adaptation, inflammation, carcinoma, and failure. Gastroenterology 130, S100–S105 (2006)
    Article CAS Google Scholar
  28. Maslowski, K. M. et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282–1286 (2009)
    Article ADS CAS Google Scholar
  29. Kurokawa, K. et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 14, 169–181 (2007)
    Article CAS Google Scholar
  30. Kongmuang, U., Honda, T. & Miwatani, T. Enzyme-linked immunosorbent assay to detect Shiga toxin of Shigella dysenteriae and related toxins. J. Clin. Microbiol. 25, 115–118 (1987)
    CAS PubMed PubMed Central Google Scholar
  31. Morita, T., Tanabe, H., Takahashi, K. & Sugiyama, K. Ingestion of resistant starch protects endotoxin influx from the intestinal tract and reduces d-galactosamine-induced liver injury in rats. J. Gastroenterol. Hepatol. 19, 303–313 (2004)
    Article CAS Google Scholar
  32. Hase, K. et al. Activation-induced cytidine deaminase deficiency causes organ-specific autoimmune disease. PLoS ONE 3, e3033 (2008)
    Article ADS Google Scholar
  33. Hase, K. et al. Distinct gene expression profiles characterize cellular phenotypes of follicle-associated epithelium and M cells. DNA Res. 12, 127–137 (2005)
    Article CAS Google Scholar
  34. Irizarry, R. A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003)
    Article Google Scholar
  35. Hijikata, A. et al. Construction of an open-access database that integrates cross-reference information from the transcriptome and proteome of immune cells. Bioinformatics 23, 2934–2941 (2007)
    Article CAS Google Scholar
  36. Tian, C. et al. Top-down phenomics of Arabidopsis thaliana: metabolic profiling by one- and two-dimensional nuclear magnetic resonance spectroscopy and transcriptome analysis of albino mutants. J. Biol. Chem. 282, 18532–18541 (2007)
    Article CAS Google Scholar
  37. Fukuda, S. et al. Evaluation and characterization of bacterial metabolic dynamics with a novel profiling technique, real-time metabolotyping. PLoS ONE 4, e4893 (2009)
    Article ADS Google Scholar
  38. Kikuchi, J., Shinozaki, K. & Hirayama, T. Stable isotope labeling of Arabidopsis thaliana for an NMR-based metabolomics approach. Plant Cell Physiol. 45, 1099–1104 (2004)
    Article CAS Google Scholar
  39. Sekiyama, Y., Chikayama, E. & Kikuchi, J. Profiling polar and semi-polar plant metabolites throughout extraction processes using a combined solution-state and HR-MAS NMR approach. Anal. Chem. 82, 1643–1652 (2010)
    Article CAS Google Scholar
  40. Akiyama, K. et al. PRIMe: a Web site that assembles tools for metabolomics and transcriptomics. In Silico Biol. 8, 339–345 (2008)
    CAS PubMed Google Scholar
  41. Chikayama, E. et al. Statistical indices for simultaneous large-scale metabolite detections for a single NMR spectrum. Anal. Chem. 82, 1653–1658 (2010)
    Article CAS Google Scholar
  42. Schuller, S., Frankel, G. & Phillips, A. D. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell. Microbiol. 6, 289–301 (2004)
    Article Google Scholar
  43. Gordon, D., Desmarais, C. & Green, P. Automated finishing with Autofinish. Genome Res. 11, 614–625 (2001)
    Article CAS Google Scholar
  44. Delcher, A. L., Harmon, D., Kasif, S., White, O. & Salzberg, S. L. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27, 4636–4641 (1999)
    Article CAS Google Scholar
  45. Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964 (1997)
    Article CAS Google Scholar
  46. Nakamura, T. et al. Cloned cytosine deaminase gene expression of Bifidobacterium longum and application to enzyme/pro-drug therapy of hypoxic solid tumors. Biosci. Biotechnol. Biochem. 66, 2362–2366 (2002)
    Article CAS Google Scholar
  47. Yasui, K. et al. Improvement of bacterial transformation efficiency using plasmid artificial modification. Nucleic Acids Res. 37, e3 (2009)
    Article Google Scholar

Download references

Acknowledgements

We thank H. Kitamura and M. E. Mariotti-Ferrandiz for discussions and for reading the manuscript; T. Morita for suggestions; and C. Nishigaki, M. Ohmae, Y. Chiba, T. Kato, H. Shima, A. Nakano, K. Sakaguchi, K. Furuya, C. Yoshino, H. Inaba, E. Iioka, K. Motomura and Y. Hattori for technical support. This research was supported in part by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan: a Grant-in-Aid for Scientific Research on Priority Areas ‘Comprehensive Genomics’ (M.H.), ‘Membrane Traffic’ (H.O.) and ‘Matrix of Infectious Phenomena’ (K.H.); Young Scientists (S.F., K.H. and J.K.); Challenging Exploratory Research (J.K.); Scientific Research (H.O.); and Scientific Research on Innovative Areas ‘Intracellular Logistics’ (H.O.). This work was also supported in part by a RIKEN President’s Special Research Grant (J.K.); a RIKEN DRI Research Grant (S.F.); a CREST grant from the Japan Science and Technology Agency (J.K.); the Danone Institute of Japan (H.O.); the Institute for Fermentation, Osaka (S.F.); the Kieikai Research Foundation (S.F.); the Naito Foundation (S.F.); the Nestlé Nutrition Council, Japan (S.F.); the Sasakawa Scientific Research Grant from the Japan Science Society (S.F. and Y.N.); the Yakult Bio-Science Foundation (S.F.); the Academic Frontier Project for Private Universities (Matching Fund Subsidy (H.M.)); and the Private University Scientific Foundation (H.M.).

Author information

Authors and Affiliations

  1. Laboratory for Epithelial Immunobiology, RIKEN Research Center for Allergy and Immunology, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan ,
    Shinji Fukuda, Koji Hase, Yumiko Nakanishi & Hiroshi Ohno
  2. Graduate School of Nanobioscience, Yokohama City University, 1-7-29 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan ,
    Shinji Fukuda, Yumiko Nakanishi, Jun Kikuchi & Hiroshi Ohno
  3. MetaSystems Research Team, RIKEN Advanced Science Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan ,
    Hidehiro Toh & Todd D. Taylor
  4. Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan ,
    Kenshiro Oshima & Masahira Hattori
  5. Advanced NMR Metabomics Research Team, RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan ,
    Yumiko Nakanishi & Jun Kikuchi
  6. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan ,
    Kazutoshi Yoshimura & Kikuji Itoh
  7. Graduate School of Medicine, Osaka University, 2-2 Yamada-oka, Suita, Osaka 565-0871, Japan ,
    Toru Tobe
  8. Preventative Health National Research Flagship, CSIRO Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia ,
    Julie M. Clarke & David L. Topping
  9. The United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan ,
    Tohru Suzuki
  10. Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan ,
    Jun Kikuchi
  11. School of Veterinary Medicine, Azabu University, 1-17-71 Fuchinobe, Sagamihara, Kanagawa 229-8501, Japan ,
    Hidetoshi Morita
  12. Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan ,
    Hiroshi Ohno

Authors

  1. Shinji Fukuda
  2. Hidehiro Toh
  3. Koji Hase
  4. Kenshiro Oshima
  5. Yumiko Nakanishi
  6. Kazutoshi Yoshimura
  7. Toru Tobe
  8. Julie M. Clarke
  9. David L. Topping
  10. Tohru Suzuki
  11. Todd D. Taylor
  12. Kikuji Itoh
  13. Jun Kikuchi
  14. Hidetoshi Morita
  15. Masahira Hattori
  16. Hiroshi Ohno

Contributions

S.F., K.I., M.H. and H.O. conceived and designed the experiments. S.F., Y.N., K.H., K.Y., K.O., H.M. and K.I. performed the experiments. S.F., H.T. and Y.N. analysed the data. T.T., J.M.C., D.L.T., T.S., T.D.T., J.K. and M.H. contributed reagents, materials and analysis tools. S.F., H.T., K.H., T.D.T., M.H. and H.O. wrote the paper.

Corresponding authors

Correspondence toMasahira Hattori or Hiroshi Ohno.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

PowerPoint slides

Rights and permissions

About this article

Cite this article

Fukuda, S., Toh, H., Hase, K. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate.Nature 469, 543–547 (2011). https://doi.org/10.1038/nature09646

Download citation