Elsevier

Carbohydrate Polymers

Volume 130, 5 October 2015, Pages 191-197
Carbohydrate Polymers

Structural features of soluble cereal arabinoxylan fibers associated with a slow rate of in vitro fermentation by human fecal microbiota

https://doi.org/10.1016/j.carbpol.2015.04.041Get rights and content

Highlights

  • Alkali-solubilized arabinoxylans had a range of in vitro fecal fermentation rates.

  • All arabinoxylans were highly branched and substituted.

  • Complex wheat and corn arabinoxylans had slow initial but complete fermentation.

  • Fast fermenting rice and sorghum arabinoxylans had simple branched structures.

  • Terminal xylose and complex trisaccharide branches related to slow fermentation.

Abstract

Most soluble dietary fibers ferment rapidly in the proximal colon, potentially causing discomfort and poor tolerability. Alkali-extracted arabinoxylan isolates from corn, wheat, rice and sorghum brans were prepared, through hydrolysis (except sorghum) and ethanol fractionation, to have a broad range of initial fermentation rates, and their linkage patterns were determined to understand structural aspects related to slow fermentation rate. They were all highly branched polymers with degree of substitution greater than 64%. There was no relationship of molecular mass, arabinose:xylose ratio, or degree of substitution to fermentation rate patterns. Slow fermenting wheat and corn arabinoxylans had much higher amount of terminal xylose in branches than fast fermenting rice and sorghum arabinoxylans. The slowest fermenting wheat arabinoxylan additionally contained a complex trisaccharide side chain with two arabinoses linked at the O-2 and O-3 positions of an arabinose that is O-2 linked to the xylan backbone. Structural features were proposed for tolerable slowly fermentable arabinoxylan with possible beneficial fermentation function into the distal colon.

Introduction

The importance of the role of dietary fiber in human health has taken on a new emphasis due to recent research in the area of the gut microbiome. There is increasing interest in specific functions of fibers, amounts needed to create desired effects, and how to deliver functional fibers in an acceptable way to the consumer. On the latter point, the issues are product quality and tolerability. Many soluble fibers, both oligo- and polysaccharides, are relatively fast fermenting and can cause bloating and discomfort when consumed in even moderate amounts (Pedersen et al., 1997, Stone-Dorshow and Levitt, 1987). Here, we report on soluble dietary fibers with a broad range of initial rate of in vitro fecal fermentation, made from the arabinoxylans from cell walls of cereal bran from different sources, and associative structural features to their slow or fast rates of fermentation.

Arabinoxylans (or “heteroxylans” to account for their additional sugars of galactose and glucuronic acid), along with β-glucans and cellulose, are the major hemicelluloses found in cereal grains. Arabinoxylans are both water-extractable and unextractable, but the majority are the latter due to their bound state through diferulate crosslinks. When treated with alkali, which breaks the ester bonds of the crosslinks, the resulting soluble arabinoxylans from various cereal sources have been shown to differ in their rates of fecal fermentation (Rose, Patterson, & Hamaker, 2010). In particular, we showed that alkali-extractable corn arabinoxylan and its endoxylanase-hydrolyzate had a significantly slower rate of gas production in an in vitro fecal batch fermentation compared to fructooligosaccharides (Rumpagaporn, Kaur, Campanella, Patterson & Hamaker, 2012).

A desirable low bloating soluble dietary fiber should be one with a low initial rate of gas production, but that is fermented completely throughout the colon. Such controlled enzymatic hydrolysis of fermentable dietary fibers has been proposed as a solution to prevent or reduce the unfavorable symptoms associated with excess gas production (Grizard & Barthomeuf, 1999). Soluble fibers from brans of cereal grains might be desirable dietary fiber ingredients or supplements due to their slower rate of fermentation (Karppinen et al., 2000, Rose et al., 2010).

Structural characteristics of arabinoxylans have been shown to drive different degradation patterns by the colonic bacteria. In a study using pigs, water-extractable rye arabinoxylan with low degree of xylan backbone substitution was readily fermented, whereas rye arabinoxylan with comparably high mono- and di-substitution, terminal xylose, and non-terminal arabinose was more difficult to degrade (Glitsø, Gruppen, Schols, Højsgaard, & Sandström, 1999). The fermentability of more highly branched arabinoxylans from wheat bran was lower than that of a slightly branched one from wheat aleurone cells (Amrein, Grönicher, Arrigoni, & Amado, 2003). Our laboratory reported that the alkali-solubilized fraction from corn bran was fermented in vitro at a relatively slow rate, with a higher production of short-chain fatty acids (SCFAs) at 24 h of fermentation, compared to the same fraction from wheat or rice brans (Rose et al., 2010). Complexity of branch structures was implicated as a reason for these observed differences in rate of fermentation. We thought a more detailed understanding of the structural properties of the cereal arabinoxylans that drive rate of fermentation would allow for strategies to be developed to identify or develop fermentable dietary fibers, including oligosaccharides, that are well tolerated and which would ferment into the distal colon. With this in mind, soluble arabinoxylans were obtained from corn, wheat, rice and sorghum brans; and native polymer and hydrolyzate fractions were isolated and chosen to have a broad range of initial rates of fermentation, but with complete fermentation by the end of the 24 h in vitro period. Their structural features were then determined and compared to fecal fermentation rates.

Section snippets

Materials

Corn bran was obtained from Bunge Milling (St. Louis, MO, USA). Wheat and rice bran products (Now Foods, Bloomingdale, IL, USA) were purchased from a local store. Sorghum bran was obtained by decorticating grain, from the Purdue Agronomy Center for Research and Education, using an abrasive dehuller. Bran (300 g) was defatted by mixing with hexane twice [bran:hexane, 1:7 (w/v)] at room temperature for 60 min each. Alpha-Amylase (EC 3.2.1.1) from Bacillus licheniformis (Type XII-A) and protease

Results and discussion

Among the collection of arabinoxylans tested, which were specifically chosen to provide a range of initial rates of fermentation (as well as molecular size and A/X ratio), certain linkage patterns were found associated with slow fermentation. Interestingly, the slow fermenting arabinoxylans (WH, CAX, and CH) all showed a two-stage fermentation profile where a pronounced slow initial fermentation was observed in the first four hours followed by a faster and complete fermentation of the remaining

Conclusion

This is the first report of specific linkage features of arabinoxylans associated with the rate of in vitro fermentation by fecal microbiota. Given that all arabinoxylan samples in this study were fairly highly substituted, the major structural factor that related to slow fermentation was type of linkage of the branch constituents. Overall, the slowly fermented arabinoxylans (WH, CAX, CH) had high amounts of branches with single xylose units that are postulated to be a determinant of slow

Acknowledgements

The authors gratefully acknowledge Anton Terekhov for assisting with gas chromatography analysis. We thank Madhuvanti Kale, David Petros and Amy Hui-Mei Lin for assistance with the HPSEC-MALS-RI analysis. Velena Lindley at the Department of Animal Science, Purdue University is also acknowledged for support during the in vitro fermentation experiment.

References (37)

  • L. Saulnier et al.

    Cell wall polysaccharide interactions in maize bran

    Carbohydrate Polymers

    (1995)
  • L. Saulnier et al.

    Isolation and partial characterization of feruloylated oligosaccharides from maize bran

    Carbohydrate Research

    (1995)
  • M.E.F. Schooneveld-Bergmans et al.

    Structural features of (glucurono)arabinoxylans extracted from wheat bran by barium hydroxide

    Journal of Cereal Science

    (1999)
  • T. Stone-Dorshow et al.

    Gaseous response to ingestion of a poorly absorbed fructo-oligosaccharide sweetener

    American Journal of Clinical Nutrition

    (1987)
  • D.P. Sweet et al.

    Quantitative analysis by various g.l.c. response-factor theories for partially methylated and partially ethylated alditol acetates

    Carbohydrate Research

    (1975)
  • M.A. Verbruggen et al.

    The selective extraction of glucuronoarabinoxylans from sorghum endosperm cell walls using barium and potassium hydroxide solutions

    Journal of Cereal Science

    (1995)
  • S. Zhou et al.

    Comparison of the immunological activities of arabinoxylans from wheat bran with alkali and xylanase-aided extraction

    Carbohydrate Polymers

    (2010)
  • J.M. Brillouet et al.

    Isolation, purification, and characterization of a complex heteroxylan from industrial wheat bran

    Journal of Agricultural and Food Chemistry

    (1982)
  • Cited by (114)

    View all citing articles on Scopus
    1

    Present address: Department of Food Science and Technology, Faculty of Agro-Industry, Kasetsart University, Bangkok 10900, Thailand.

    View full text