Processing Has Differential Effects on Microbiota-Accessible Carbohydrates in Whole Grains during In Vitro Fermentation

Whole grains are generally low in nondigestible carbohydrates that are available for fermentation by the gut microbiota, or microbiota-accessible carbohydrates (MAC). However, there is potential to increase MAC in whole grains through food processing. Five processing methods: boiling, extrusion, sourdough bread, unleavened bread, and yeast bread, were applied to whole wheat flour and then subjected to in vitro digestion followed by fermentation using fecal microbiomes from 10 subjects. The microbiomes separated into 2 groups: those that showed high carbohydrate utilization ( CU) and those that exhibited low CU. The former exhibited not only enhanced CU but also increased butyrate production (MAC, 31.1 +/- 1.1% versus 19.3 +/- 1.2%, P < 0.001; butyrate, 5.26 +/- 0.26 mM versus 3.17 +/- 0.27 mM, P < 0.001). Only the microbiomes in the high-CU group showed significant differences among processing methods: extrusion and sourdough bread led to dichotomous results for MAC and short-chain fatty acid production, where extrusion resulted in high MAC but low butyrate production while sourdough bread resulted in low MAC but high butyrate production. Extrusion led to a noticeable decrease in alpha-diversity and some members of the families Ruminococcaceae and Lachnospiraceae, with increases in Acinetobacter, Enterococcus, and Staphylococcaceae. This study demonstrated that only microbiomes that exhibited high CU responded to the effects of processing by showing significant differences among processing methods. In these microbiomes, extrusion was able to increase accessibility of the cell wall polysaccharides but did not increase butyrate production. In contrast, sourdough bread led to high butyrate production by supporting important butyrate- producers in the families Lachnospiraceae and Ruminococcaceae. IMPORTANCE Dietary nondigestible carbohydrates, or dietary fiber, have long been recognized for their beneficial health effects. However, recent studies have revealed that fermentation of nondigestible carbohydrates by gut bacteria is critical in mediating many of the health-promoting properties of dietary fibers. Whole grains are excellent candidates to supply the microbiome with a plentiful source of nondigestible carbohydrates, although unfortunately a majority of these carbohydrates in whole grains are not available to gut bacteria for fermentation. Processing is known to alter the structural characteristics of nondigestible carbohydrates in whole grains, yet the relationship between these effects and gut microbial fermentation is unknown. This research aimed to address this important research gap by identifying interactions between whole-grain processing and gut bacteria, with the ultimate goal of increasing the availability of nondigestible carbohydrates for fermentation to enhance host health.