The effect of resistant starch (RS) on the bovine rumen microflora and isolation of RS-degrading bacteria

  • Dong-Hyun Jung
  • Dong-Ho Seo
  • Ga-Young Kim
  • Young-Do Nam
  • Eun-Ji Song
  • Shawn Yoon
  • Cheon-Seok Park
Applied microbial and cell physiology

Abstract

Resistant starch (RS) in the diet reaches the large intestine without degradation, where it is decomposed by the commensal microbiota. The fermentation of RS produces secondary metabolites including short-chain fatty acids (SCFAs), which have been linked to a variety of physiological and health effects. Therefore, the availability of RS as a prebiotic is a current issue. The objectives of this study were (1) to use metagenomics to observe microbial flora changes in Bos taurus coreanae rumen fluid in the presence of RS and (2) to isolate RS-degrading microorganisms. The major microbial genus in a general rumen fluid was Succiniclasticum sp., whereas Streptococcus sp. immediately predominated after the addition of RS into the culture medium and was then drastically replaced by Lactobacillus sp. The presence of Bifidobacterium sp. was also observed continuously. Several microorganisms with high RS granule-degrading activity were identified and isolated, including B. choerinum FMB-1 and B. pseudolongum FMB-2. B. choerinum FMB-1 showed the highest RS-hydrolyzing activity and degraded almost 60% of all substrates tested. Coculture experiments demonstrated that Lactobacillus brevis ATCC 14869, which was isolated from human feces, could grow using reducing sugars generated from RS by B. choerinum FMB-1. These results suggest that Bifidobacterium spp., especially B. choerinum FMB-1, are the putative primary degrader of RS in rumen microbial flora and could be further studied as probiotic candidates.

Keywords

Bovine rumen Granular starch-degrading bacteria Resistant starch Bifidobacterium 

Notes

Acknowledgments

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MEST) (no. 2017R1A2B4004218). Additionally, this research was partly supported by Main Research Programs (grant number E0170602-02) of the Korea Food Research Institute funded by the Ministry of Science and ICT.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2018_8971_MOESM1_ESM.pdf (548 kb)
ESM 1 (PDF 548 kb)

References

  1. Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW (2012) Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9:425–426CrossRefPubMedGoogle Scholar
  2. Canani RB, Di Costanzo M, Leone L, Pedata M, Meli R, Calignano A (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17:1519–1528CrossRefPubMedPubMedCentralGoogle Scholar
  3. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cockburn DW, Orlovsky NI, Foley MH, Kwiatkowski KJ, Bahr CM, Maynard M, Demeler B, Koropatkin NM (2015) Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol Microbiol 95:209–230CrossRefPubMedGoogle Scholar
  5. Crittenden R, Laitila A, Forssell P, Mättö J, Saarela M, Mattila-Sandholm T, Myllärinen P (2001) Adhesion of bifidobacteria to granular starch and its implications in probiotic technologies. Appl Environ Microbiol 67:3469–3475CrossRefPubMedPubMedCentralGoogle Scholar
  6. DuBois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  7. Ellis RP, Cochrane MP, Dale MFB, Duffus CM, Lynn A, Morrison IM, Prentice RDM, Swanston JS, Tiller SA (1998) Starch production and industrial use. J Sci Food Agric 77:289–311CrossRefGoogle Scholar
  8. Ferguson LR, Tasman-Jones C, Englyst H, Harris PJ (2000) Comparative effects of three resistant starch preparations on transit time and short-chain fatty acid production in rats. Nutr Cancer 36:230–237CrossRefPubMedGoogle Scholar
  9. Fuentes-Zaragoza E, Sánchez-Zapata E, Sendra E, Sayas E, Navarro C, Fernández-López J, Pérez-Alvarez JA (2011) Resistant starch as prebiotic: a review. Starch-Stärke 63:406–415CrossRefGoogle Scholar
  10. Keenan MJ, Zhou J, McCutcheon KL, Raggio AM, Bateman HG, Todd E, Jones CK, Tulley RT, Melton S, Martin RJ (2006) Effects of resistant starch, a non-digestible fermentable fiber, on reducing body fat. Obesity 14:1523–1534CrossRefPubMedGoogle Scholar
  11. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821CrossRefPubMedPubMedCentralGoogle Scholar
  12. Le Leu RK, Brown IL, Hu Y, Bird AR, Jackson M, Esterman A, Young GP (2005) A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. J Nutr 135:996–1001CrossRefPubMedGoogle Scholar
  13. Le Leu RK, Hu Y, Brown IL, Young GP (2009) Effect of high amylose maize starches on colonic fermentation and apoptotic response to DNA-damage in the colon of rats. Nutr Metab 6:11CrossRefGoogle Scholar
  14. Liu S, Ren F, Zhao L, Jiang L, Hao Y, Jin J, Zhang M, Guo H, Lei X, Sun E (2015) Starch and starch hydrolysates are favorable carbon sources for bifidobacteria in the human gut. BMC Microbiol 15:54CrossRefPubMedPubMedCentralGoogle Scholar
  15. Mao S, Zhang M, Liu J, Zhu W (2015) Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci Rep 5:16116CrossRefPubMedPubMedCentralGoogle Scholar
  16. Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC (2005) Carbohydrate analysis by a phenol–sulfuric acid method in microplate format. Anal Biochem 339:69–72CrossRefPubMedGoogle Scholar
  17. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618CrossRefPubMedGoogle Scholar
  18. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428CrossRefGoogle Scholar
  19. Niderman-Meyer O, Zeidman T, Shimoni E, Kashi Y (2010) Mechanisms involved in governing adherence of Vibrio cholerae to granular starch. Appl Environ Microbiol 76:1034–1043CrossRefPubMedGoogle Scholar
  20. Ørskov E (1986) Starch digestion and utilization in ruminants. J Anim Sci 63:1624–1633CrossRefPubMedGoogle Scholar
  21. Phillips J, Muir JG, Birkett A, Lu ZX, Jones GP, O'Dea K, Young GP (1995) Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. Am J Clin Nutr 62:121–130CrossRefPubMedGoogle Scholar
  22. Qian W, Li Z, Ao W, Zhao G, Li G, Wu J (2017) Bacterial community composition and fermentation in the rumen of Xinjiang brown cattle (Bos taurus), Tarim red deer (Cervus elaphus yarkandensis), and karakul sheep (Ovis aries). Can J Microbiol 63:375–383CrossRefPubMedGoogle Scholar
  23. Ramakrishna B, Venkataraman S, Srinivasan P, Dash P, Young GP, Binder HJ (2000) Amylase-resistant starch plus oral rehydration solution for cholera. N Engl J Med 342:308–313CrossRefPubMedGoogle Scholar
  24. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A (2014) Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. Peer J 2:e545CrossRefPubMedPubMedCentralGoogle Scholar
  25. Robertson MD, Bickerton AS, Dennis AL, Vidal H, Frayn KN (2005) Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am J Clin Nutr 82:559–567CrossRefPubMedGoogle Scholar
  26. Rosin PM, Lajolo FM, Menezes EW (2002) Measurement and characterization of dietary starches. J Food Compos Anal 15:367–377CrossRefGoogle Scholar
  27. Salyers AA, Leedle J, Hentges D (1983) Carbohydrate metabolism in the human colon—human intestinal microflora in health and disease, 1st edn. Elsevier Academic Press, New York, pp 129–144CrossRefGoogle Scholar
  28. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864CrossRefPubMedPubMedCentralGoogle Scholar
  29. Umu ÖC, Frank JA, Fangel JU, Oostindjer M, Da Silva CS, Bolhuis EJ, Bosch G, Willats WG, Pope PB, Diep DB (2015) Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations. Microbiome 3:16CrossRefPubMedPubMedCentralGoogle Scholar
  30. Walker AW, Duncan SH, Leitch ECM, Child MW, Flint HJ (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71:3692–3700CrossRefPubMedPubMedCentralGoogle Scholar
  31. Young GP, Hu Y, Le Leu RK, Nyskohus L (2005) Dietary fibre and colorectal cancer: a model for environment–gene interactions. Mol Nutr Food Res 49:571–584CrossRefPubMedGoogle Scholar
  32. Ze X, Duncan SH, Louis P, Flint HJ (2012) Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6:1535–1543CrossRefPubMedPubMedCentralGoogle Scholar
  33. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of Biotechnology and Institute of Life Science and ResourcesKyung Hee UniversityYonginRepublic of Korea
  2. 2.Gut Microbiome Research GroupKorea Food Research InstituteSungnamRepublic of Korea
  3. 3.Department of Food BiotechnologyKorea University of Science and TechnologyDaejeonRepublic of Korea
  4. 4.Global Research and Technology, Ingredion IncorporatedBridgewaterUSA

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