Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification

Abstract

The human gut can be viewed as a flow-through system with a short residence time, a high turnover rate and a spatial gradient of physiological conditions. As a consequence, the gut microbiota is exposed to highly fluctuating environmental determinants presented by the host and diet. Here, we assessed the fermentation and colonisation of insoluble wheat bran by faecal microbiota of three individuals at an unprecedented sampling intensity. Time-resolved 16S rRNA gene amplicon sequencing, revealed a dynamic microbial community, characterised by abrupt shifts in composition, delimiting states with a more constant community, giving rise to a succession of bacterial taxa alternately dominating the community over a 72 h timespan. Early stages were dominated by Enterobacteriaceae and Fusobacterium species, growing on the carbohydratelow, protein rich medium to which wheat bran was supplemented. The onset of wheat bran fermentation, marked by a spike in short chain fatty acid production with an increasing butyrate proportion and an increased endo-1,4-β-xylanase activity, corresponded to donor-dependent proportional increases of Bacteroides ovatus/stercoris, Prevotella copri and Firmicutes species, which were strongly enriched in the bran-attached community. Literature and database searches provided novel insights into the metabolic and growth characteristics underlying the observed succession and colonisation, illustrating the potency of a time-resolved analysis to increase our understanding of gut microbiota dynamics upon dietary modulations.

Premilling pearling for producing wheat fractions with distinct digestibility and fermentability

“…De Paepe et al. (2020) reported acetate (20–30 mM), propionate (8–12 mM), and butyrate (5–10 mM) concentrations after 48 hr fermentation of wheat bran similar to those displayed in Figure 4.…”

Microbial enterotypes beyond genus level: Bacteroides species as a predictive biomarker for weight change upon controlled intervention with arabinoxylan oligosaccharides in overweight subjects

“…with overlapping glycan degrading capacity. 38 In fact, intake of xylan-rich foods may be the main determinant of P. copri positive effect on human metabolism, 8 , 19 while a diet rich in fat seems to have the opposite effect. 39 However, on AXOS, we found no weight-loss effect of high baseline abundance of P. copri , which could be due to too few subjects studied or the recently discovered disparate genomic and metabolic capacity of P. copri clades.…”

“…39 Given that the bodyweight changes may be partly due to fermentation end-products of AXOS released distally in the gastrointestinal tract, future studies should investigate potential links between B. cellulosilyticus and fecal SCFA. Acetate is the most highly produced SCFA in response to arabinoxylan fermentation 38 and exclusively produced by B. cellulosilyticus upon arabinogalactan fermentation. 40 While P. copri is a well-known acetate producer, 41 we hypothesize that B. cellulosilyticus may not crossfeed SCFAs in a similar fashion, and thereby not contribute to create a healthy microbial community.…”

Comparative Effect of 22 Dietary Sources of Fiber on Gut Microbiota of Healthy Humans in vitro

“…In addition to the relevant effect of fiber sources on mucosal health, complex fiber structures such as wheat bran can serve as a microenvironment to be colonized by specific degraders (53). The presence of multiple subecological niches within the gut would allow for niche specialization and diversification, while it is recognized that higher fiber promotes greater microbiome diversity (54).…”