Abstract
Resistant starch (RS) in the diet reaches the large intestine and is fermented by the gut microbiota, providing beneficial effects on human health. The human gut bacterium FMB-CY1 was isolated and identified as a new species closest to Ruminococcus bromii. Ruminococcus sp. FMB-CY1 completely degraded RS including commercial RS types 2, 3, and 4, and generated glucose and maltose; however, it did not assimilate glucose. Genome analysis revealed 15 amylolytic enzymes (Amy) present in FMB-CY1. The evolutionary trees revealed that the Amys were well divided each other. All Amys (4, 9, 10, 12, and 16) containing cohesin and/or dockerin and scaffolding proteins known to be involved in constituting the amylosome, were identified. A new species of Ruminococcus, strain FMB-CY1, was considered to have the ability to form amylosomes for the degradation of RS. This new RS-degrading Ruminococcus species provides insights into the mechanism(s) underlying RS degradation in the human gut.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10068-021-01027-2/MediaObjects/10068_2021_1027_Fig1_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10068-021-01027-2/MediaObjects/10068_2021_1027_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10068-021-01027-2/MediaObjects/10068_2021_1027_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10068-021-01027-2/MediaObjects/10068_2021_1027_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10068-021-01027-2/MediaObjects/10068_2021_1027_Fig5_HTML.png)
Similar content being viewed by others
References
Armenteros JJA, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology. 37: 420-423 (2019)
Bello‐Perez LA, Flores‐Silva PC, Agama‐Acevedo E, Tovar J. Starch digestibility: past, present, and future. Journal of the Science of Food and Agriculture. 100: 5009-5016 (2020)
Blaak E, Canfora E, Theis S, Frost G, Groen A, Mithieux G, Nauta A, Scott K, Stahl B, van Harsselaar J. Short chain fatty acids in human gut and metabolic health. Beneficial Microbes. 11: 411-455 (2020)
Blake AW, McCartney L, Flint JE, Bolam DN, Boraston AB, Gilbert HJ, Knox JP. Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. Journal of Biological Chemistry. 281: 29321-29329 (2006)
Boos W, Shuman H. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiology and Molecular Biology Reviews. 62: 204-229 (1998)
Bren A, Park JO, Towbin BD, Dekel E, Rabinowitz JD, Alon U. Glucose becomes one of the worst carbon sources for E. coli on poor nitrogen sources due to suboptimal levels of cAMP. Scientific Reports. 6: 1-10 (2016)
Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics. 25: 119-120 (2008)
Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods. 10: 563 (2013)
DeMartino P, Cockburn DW. Resistant starch: impact on the gut microbiome and health. Current Opinion in Biotechnology. 61: 66-71 (2020)
Doster E, Lakin SM, Dean CJ, Wolfe C, Young JG, Boucher C, Belk KE, Noyes NR, Morley PS. MEGARes 2.0: a database for classification of antimicrobial drug, biocide and metal resistance determinants in metagenomic sequence data. Nucleic Acids Research. 40: D561-D569 (2019)
Flint HJ. The impact of nutrition on the human microbiome. Nutrition Reviews. 70: S10-S13 (2012)
Fuentes‐Zaragoza E, Sánchez‐Zapata E, Sendra E, Sayas E, Navarro C, Fernández‐López J, Pérez‐Alvarez JA. Resistant starch as prebiotic: a review. Starch‐Stärke. 63: 406-415 (2011)
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Research. 36: W5-W9 (2008)
Jung D-H, Seo D-H, Kim G-Y, Nam Y-D, Song E-J, Yoon S and Park C-S, The effect of resistant starch (RS) on the bovine rumen microflora and isolation of RS-degrading bacteria. Applied Microbiology and Biotechnology. 102:4927-4936 (2018).
Jung D-H, Chung W-H, Seo D-H, Kim Y-J, Nam Y-D, Park C-S. Complete genome sequence of Bifidobacterium adolescentis P2P3, a human gut bacterium possessing strong resistant starch-degrading activity. 3 Biotech. 10: 1-9 (2020)
Jung D-H, Kim G-Y, Kim I-Y, Seo D-H, Nam Y-D, Kang H, Song Y, Park C-S. Bifidobacterium adolescentis P2P3, a human gut bacterium having strong non-gelatinized resistant starch-degrading activity. Journal of Microbiology and Biotechnology. 29:1904-1915 (2019)
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547 (2018)
La Reau AJ, Meier-Kolthoff JP, Suen G. Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association. Microbial Genomics. 2 (2016)
Le Leu RK, Brown IL, Hu Y, Bird AR, Jackson M, Esterman A, Young GP. A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. The Journal of Nutrition. 135: 996-1001 (2005)
Le Leu RK, Hu Y, Brown IL, Young GP. Effect of high amylose maize starches on colonic fermentation and apoptotic response to DNA-damage in the colon of rats. Nutrition & Metabolism. 6: 1-9 (2009)
Lee I, Kim YO, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. International Journal of Systematic and Evolutionary Microbiology. 66: 1100-1103 (2016)
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Research. 45: D200-D203 (2017)
Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC. Carbohydrate analysis by a phenol–sulfuric acid method in microplate format. Analytical Biochemistry. 339: 69-72 (2005)
Maziarz MP, Preisendanz S, Juma S, Imrhan V, Prasad C, Vijayagopal P. Resistant starch lowers postprandial glucose and leptin in overweight adults consuming a moderate-to-high-fat diet: a randomized-controlled trial. Nutrition Journal. 16: 14 (2017)
Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry. 31: 426-428 (1959)
Mukhopadhya I, Moraïs S, Laverde‐Gomez J, Sheridan PO, Walker AW, Kelly W, Klieve AV, Ouwerkerk D, Duncan SH, Louis P. Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii. Environmental Microbiology. 20: 324-336 (2018)
Molinero N, Conti E, Sánchez B, Walker AW, Margolles A, Duncan SH, Delgado S. Ruminococcoides bili gen. nov., sp. nov., a bile-resistant bacterium from human bile with autolytic behavior. International Journal of Systematic and Evolutionary Microbiology. 71: 004960 (2021)
Raigond P, Ezekiel R, Raigond B. Resistant starch in food: a review. Journal of the Science of Food and Agriculture. 95: 1968-1978 (2015)
Sandberg JC, Björck IM, Nilsson AC. Effects of whole grain rye, with and without resistant starch type 2 supplementation, on glucose tolerance, gut hormones, inflammation and appetite regulation in an 11–14.5 hour perspective; a randomized controlled study in healthy subjects. Nutrition Journal. 16: 25 (2017)
Shaikh F, Ali TM, Mustafa G, Hasnain A. Comparative study on effects of citric and lactic acid treatment on morphological, functional, resistant starch fraction and glycemic index of corn and sorghum starches. International Journal of Biological Macromolecules. 135: 314-327 (2019)
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology. 7: 539 (2011)
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Research. 44: 6614-6624 (2016)
Ze X, Ben David Y, Laverde-Gomez JA, Dassa B, Sheridan PO, Duncan SH, Louis P, Henrissat B, Juge N, Koropatkin NM. Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic Firmicutes bacterium Ruminococcus bromii. mBio. 6: e01058–15 (2015)
Ze X, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. The ISME journal. 6: 1535-1543 (2012)
Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Research. 46: W95-W101 (2018)
Acknowledgements
This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (2021R1A4A1023437).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of human derivatives were followed. The study of human derivatives was approved by the Institutional Review Board of Kyung Hee University (KHSIRB-17–004).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hong, YS., Jung, DH., Chung, WH. et al. Human gut commensal bacterium Ruminococcus species FMB-CY1 completely degrades the granules of resistant starch. Food Sci Biotechnol 31, 231–241 (2022). https://doi.org/10.1007/s10068-021-01027-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10068-021-01027-2