Glycan complexity dictates microbial resource allocation in the large intestine

Authors: ROGOWSKI, ARTUR - Newcastle University; BRIGGS, JONATHON - Newcastle University; MORTIMER, JENNIFER - Cambridge University; TRYFONA, THEODORA - Cambridge University; TERRAPON, NICOLAS - Aix-Marseille University; LOWE, ELISABETH - Newcastle University; BASLE, ARNAUD - Newcastle University; DAY, ALISON - Newcastle University; ZHENG, HONGJUN - Newcastle University; ROGERS, THERESA - University Of Michigan; Yadav, Madhav; HENRISSAT, BERNARD - Aix-Marseille University; MARTENS, ERIC - University Of Michigan Medical School; DUPREE, PAUL - Cambridge University; GILBERT, HARRY - Newcastle University; BOLAM, DAVID - Newcastle University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/13/2015
Publication Date: 6/26/2015
Publication URL: https://handle.nal.usda.gov/10113/61635
Citation: Rogowski, A., Briggs, J.A., Mortimer, J.C., Tryfona, T., Terrapon, N., Lowe, E.C., Basle, A., Day, A.M., Zheng, H., Rogers, T.E., Yadav, M.P., Henrissat, B., Martens, E.C., Dupree, P., Gilbert, H.J., Bolam, D.N. 2015. Glycan complexity dictates microbial resource allocation in the large intestine. Nature Communications. 6:1-15. doi: 10.1038/ncomms8481.

Interpretive Summary: The human gut microbiota plays a key role in human physiology and health. Complex carbohydrates are the major nutrients for the growth of beneficial bacteria in the human gut. To initiate the growth of these useful bacteria in human gut there is a need of such complex carbohydrate in human food, which can be specifically utilized by them. The complex carbohydrate isolated from corn fiber is called corn arabinoxylan. Corn fiber is a low value by-products of corn milling process and is currently used as a component of low-value animal feeds. Corn arabinoxylan has a very branched structure, which can be degraded and fermented only by the beneficial bacteria in human gut. The cellular organization of the xylan degrading apparatus of these beneficial bacteria ensures that the sugars released from highly complex arabinoxylan are not shared significantly with other nonbeneficial members of the human gut microbiota. For this purpose, only these bacteria can make the enzymes, which can cleave the complex corn arabinoxylan and utilize it for food. The enzymes synthesized by these beneficial bacteria were identified and their actions are studied on corn arabinoxylan substrate. The utilization of these corn arabinoxylan isolated from corn processing by-product will benefit U.S. corn processors and corn growers. The generation and recovery of additional valuable product from corn milling by-products will also indirectly help to reduce overall cost of fuel ethanol produced from corn kernels.

Technical Abstract: The structure of the human gut microbiota, which impacts on the health of the host, is controlled by complex dietary carbohydrates and members of the Bacteroidetes phylum are the major contributors to the degradation of complex dietary carbohydrates. The extent to which complex dietary carbohydrates breakdown products are shared between key members of the human gut microbiota is unclear, but is crucial in the development of prebiotic strategies designed to modulate the HGM for the benefit of health. We show here, using xylan, a major complex dietary carbohydrate, as a model substrate, that sharing of complex dietary carbohydrate breakdown products with non-Bacteroidetes is dependent upon the complexity of the target glycan. The characterization of the xylan degrading loci in Bacteroides ovatus elucidates the mechanisms by which this bacterium determines resource allocation to other members of the microbiota during complex dietary carbohydrate breakdown.