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Novel carbohydrate binding modules in the surface anchored α‐amylase of Eubacterium rectale provide a molecular rationale for the range of starches used by this organism in the human gut

Journal Article · · Molecular Microbiology
DOI:https://doi.org/10.1111/mmi.13881· OSTI ID:1410833
 [1];  [2];  [2];  [2];  [3];  [4];  [2]
  1. Department of Microbiology and Immunology University of Michigan Medical School Ann Arbor MI 48109 USA, Department of Food Science Pennsylvania State University, University Park PA 16802 USA
  2. Department of Microbiology and Immunology University of Michigan Medical School Ann Arbor MI 48109 USA
  3. Life Sciences Collaborative Access Team (LS‐CAT), Advanced Photon Source Argonne National Laboratory, 9700 S. Cass Avenue Argonne IL 60439 USA
  4. Architecture et Fonction des Macromolécules Biologiques, CNRS, Aix‐Marseille University Marseille F‐13288 France, Institut National de la Recherche Agronomique, USC1408 Architecture et Fonction des Macromolécules Biologiques Marseille F‐13288 France, Department of Biological Sciences King Abdulaziz University Jeddah 21589 Saudi Arabia

Summary

Gut bacteria recognize accessible glycan substrates within a complex environment. Carbohydrate binding modules (CBMs) of cell surface glycoside hydrolases often drive binding to the target substrate. Eubacterium rectale , an important butyrate‐producing organism in the gut, consumes a limited range of substrates, including starch. Host consumption of resistant starch increases the abundance of E. rectale in the intestine, likely because it successfully captures the products of resistant starch degradation by other bacteria. Here, we demonstrate that the cell wall anchored starch‐degrading α‐amylase, Amy13K of E. rectale harbors five CBMs that all target starch with differing specificities. Intriguingly these CBMs efficiently bind to both regular and high amylose corn starch (a type of resistant starch), but have almost no affinity for potato starch (another type of resistant starch). Removal of these CBMs from Amy13K reduces the activity level of the enzyme toward corn starches by ∼40‐fold, down to the level of activity toward potato starch, suggesting that the CBMs facilitate activity on corn starch and allow its utilization in vivo . The specificity of the Amy13K CBMs provides a molecular rationale for why E. rectale is able to only use certain starch types without the aid of other organisms.

Sponsoring Organization:
USDOE
Grant/Contract Number:
NONE; AC02-06CH11357
OSTI ID:
1410833
Alternate ID(s):
OSTI ID: 1419064
Journal Information:
Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 2 Vol. 107; ISSN 0950-382X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
FAO
Language:
English

References (71)

Dysbiosis of fecal microbiota in Crohnʼs disease patients as revealed by a custom phylogenetic microarray journal January 2010
The starch-binding domain family CBM41-An in silico analysis of evolutionary relationships : Carbohydrate-binding Module Family 41 journal May 2017
Recent Advances in Knowledge of Starch Structure journal January 1991
Atomic Structures of the Human Immunophilin FKBP-12 Complexes with FK506 and Rapamycin journal January 1993
Characterization of two forms of glucoamylase from aspergillus niger journal January 1982
Structure and function of α-glucan debranching enzymes journal May 2016
The Sus operon: a model system for starch uptake by the human gut Bacteroidetes journal May 2016
Butyrate Enhances Intestinal Epithelial Barrier Function via Up-Regulation of Tight Junction Protein Claudin-1 Transcription journal June 2012
Assay of reducing sugars in the nanomole range with 2,2′-bicinchoninate journal September 1987
Thermodynamics of hydrolysis of oligosaccharides journal April 1991
Quantitative Approaches to The Analysis of Carbohydrate-Binding Module Function book January 2012
Basic local alignment search tool journal October 1990
Degradation of the starch components amylopectin and amylose by barley α-amylase 1: Role of surface binding site 2 journal December 2012
The activity of barley α-amylase on starch granules is enhanced by fusion of a starch binding domain from Aspergillus niger glucoamylase journal February 2006
Binding interactions of α-amylase with starch granules: The influence of supramolecular structure and surface area journal August 2011
Pullulan: An exopolysaccharide and its various applications journal June 2013
A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility journal November 2016
Surface binding sites in amylase have distinct roles in recognition of starch structure motifs and degradation journal April 2015
The Structural Basis of α-Glucan Recognition by a Family 41 Carbohydrate-binding Module from Thermotoga maritima journal January 2007
The gut microbial community in metabolic syndrome patients is modified by diet journal January 2016
Starch Catabolism by a Prominent Human Gut Symbiont Is Directed by the Recognition of Amylose Helices journal July 2008
A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate journal June 2012
From the gut to the peripheral tissues: the multiple effects of butyrate journal October 2010
α-Glucan Recognition by a New Family of Carbohydrate-Binding Modules Found Primarily in Bacterial Pathogens journal December 2004
Two Secondary Carbohydrate Binding Sites on the Surface of Barley α-Amylase 1 Have Distinct Functions and Display Synergy in Hydrolysis of Starch Granules journal August 2009
13 C Nuclear Magnetic Relaxation Study of Segmental Dynamics of the Heteropolysaccharide Pullulan in Dilute Solutions journal December 2001
Comparative Study of Small Linear and Branched α-Glucans Using Size Exclusion Chromatography and Static and Dynamic Light Scattering # journal January 2005
First Principles Insight into the α-Glucan Structures of Starch: Their Synthesis, Conformation, and Hydration journal April 2010
Gut microbiome composition is linked to whole grain-induced immunological improvements journal October 2012
Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon journal February 2012
A metagenome-wide association study of gut microbiota in type 2 diabetes journal September 2012
Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota journal December 2015
Privateer: software for the conformational validation of carbohydrate structures journal November 2015
The effect of short-chain fatty acids on human monocyte-derived dendritic cells journal November 2015
Glucoamylase starch-binding domain of Aspergillus niger B1: molecular cloning and functional characterization journal June 2003
Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects journal August 2010
Multidomain Carbohydrate-binding Proteins Involved in Bacteroides thetaiotaomicron Starch Metabolism journal August 2012
A Structural and Functional Analysis of α-Glucan Recognition by Family 25 and 26 Carbohydrate-binding Modules Reveals a Conserved Mode of Starch Recognition journal October 2005
Influence of orally and rectally administered propionate on cholesterol and glucose metabolism in obese rats journal August 1996
The contribution of the large intestine to energy supplies in man journal February 1984
Measurement of Resistant Starch journal May 2002
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
JPred4: a protein secondary structure prediction server journal April 2015
Colonic Health: Fermentation and Short Chain Fatty Acids journal January 2006
Phylogenetic Analysis of Dysbiosis in Ulcerative Colitis During Remission journal January 2013
Cell-associated  -amylases of butyrate-producing Firmicute bacteria from the human colon journal November 2006
Phaser crystallographic software journal July 2007
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Overview of the CCP 4 suite and current developments journal March 2011
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM journal March 2011
Data processing and analysis with the autoPROC toolbox journal March 2011
Towards automated crystallographic structure refinement with phenix.refine journal March 2012
How good are my data and what is the resolution? journal June 2013
Carbohydrate-binding module 74 is a novel starch-binding domain associated with large and multidomain α-amylase enzymes journal May 2016
Selective colonization of insoluble substrates by human faecal bacteria journal March 2007
Towards the human intestinal microbiota phylogenetic core journal October 2009
Association between specific mucosa-associated microbiota in Crohn's disease at the time of resection and subsequent disease recurrence: A pilot study: Microbiota in Crohn's disease journal January 2015
Molecular details of a starch utilization pathway in the human gut symbiont E ubacterium rectale : Starch utilization by journal December 2014
Systemic availability and metabolism of colonic-derived short-chain fatty acids in healthy subjects: a stable isotope study: Short-chain fatty acid systemic availability and metabolism in humans journal September 2016
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice journal September 2013
Degradation of Granular Starch by the Bacterium Microbacterium aurum Strain B8.A Involves a Modular α-Amylase Enzyme System with FNIII and CBM25 Domains journal July 2015
Predominant Gram-Positive Bacteria in Human Feces: Numbers, Variety, and Persistence journal January 1974
The Gut Microbiome Modulates Colon Tumorigenesis journal November 2013
Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. journal September 1980
Feeding the microbiota: transducer of nutrient signals for the host journal June 2017
Butyrate ingestion improves hepatic glycogen storage in the re-fed rat journal January 2008
Variable responses of human microbiomes to dietary supplementation with resistant starch journal June 2016
Resistant Starches Types 2 and 4 Have Differential Effects on the Composition of the Fecal Microbiota in Human Subjects journal November 2010
Disrupted Intestinal Microbiota and Intestinal Inflammation in Children with Cystic Fibrosis and Its Restoration with Lactobacillus GG: A Randomised Clinical Trial journal February 2014
Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health journal February 2016
Resistant Starch: Promise for Improving Human Health journal November 2013

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