Mutual Cross-Feeding Interactions between Bifidobacterium longum subsp. longum NCC2705 and Eubacterium rectale ATCC 33656 Explain the Bifidogenic and Butyrogenic Effects of Arabinoxylan Oligosaccharides

Abstract

Arabinoxylan oligosaccharides (AXOS) are a promising class of prebiotics that have the potential to stimulate the growth of bifidobacteria and the production of butyrate in the human colon, known as the bifidogenic and butyrogenic effects, respectively. Although these dual effects of AXOS are considered beneficial for human health, their underlying mechanisms are still far from being understood. Therefore, this study investigated the metabolic interactions between Bifidobacterium longum subsp. longum NCC2705 (B. longum NCC2705), an acetate producer and arabinose substituent degrader of AXOS, and Eubacterium rectale ATCC 33656, an acetate-converting butyrate producer. Both strains belong to prevalent species of the human colon microbiota. The strains were grown on AXOS during mono-and coculture fermentations, and their growth, AXOS consumption, metabolite production, and expression of key genes were monitored. The results showed that the growth of both strains and gene expression in both strains were affected by cocultivation and that these effects could be linked to changes in carbohydrate consumption and concomitant metabolite production. The consumption of the arabinose substituents of AXOS by B. longum NCC2705 with the concomitant production of acetate allowed E. rectale ATCC 33656 to produce butyrate (by means of a butyryl coenzyme A [CoA]:acetate CoA-transferase), explaining the butyrogenic effect of AXOS. Eubacterium rectale ATCC 33656 released xylose from the AXOS substrate, which favored the B. longum NCC2705 production of acetate, explaining the bifidogenic effect of AXOS. Hence, those interactions represent mutual cross-feeding mechanisms that favor the coexistence of bifidobacterial strains and butyrate producers in the same ecological niche. In conclusion, this study provides new insights into the bifidogenic and butyrogenic effects of AXOS. F ermentation in the human colon is carried out by trillions of bacteria that contribute not only to health and well-being but also to disease (1-4). For instance, a decrease in the relative abundance of bifidobacteria in the human colon has been associated with antibiotic-associated diarrhea, irritable bowel syndrome, inflammatory bowel disease, allergies, and regressive autism (5, 6). Although it is currently not yet clear whether changes in microbial composition are a cause or a consequence of these disorders, there are indications that metabolites, in particular, the short-chain fatty acids (SCFAs), such as acetate, butyrate, and propionate, that are produced during fermentation in the colon play an important role in intestinal homeostasis (3, 7). Among the SCFAs produced in the human colon, butyrate has drawn the most attention, as it is an essential energy source for the colon epithelial cells and has a protective effect against inflammatory bowel disease and colon cancer (3,8,9). Most butyrate producers belong to the Firmicutes phylum and use a butyryl coenzyme A (CoA):acetate CoA-transferase in the final step of butyrate biosynthesis, which involves the n...

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“…Intriguingly, complex inter-species cross-feeding mechanisms have been described that link the metabolic activity of lactic acid bacteria (e.g., lactobacilli and bifidobacteria, key species generally considered to be probiotic, i.e. to promote host health) with butyrate-producing pathways (Belenguer et al, 2006;De Vuyst and Leroy, 2011;Flint et al, 2007;Rios-Covian et al, 2015;Rivière et al, 2015). In this context it is interesting to note that in extreme cases such as the short-bowel syndrome in humans, fermentation-derived overdoses of lactate (2-3mM in serum) can induce severe neurological symptoms (Ewaschuk et al, 2005), which might be treated by enhancing conversion of lactate to butyrate in the colonic lumen.…”

Genomics of the Genus Bifidobacterium Reveals Species-Specific Adaptation to the Glycan-Rich Gut Environment

“…Recently, several studies have revealed that bifidobacteria play an ecological role in shaping the gut murine microbiome toward a saccharolytic microbiota by means of crossfeeding activities (43,(74)(75)(76)(77)(78)(79). Cross-feeding activities target polysaccharides that reach the gut intact, where they may undergo extracellular hydrolysis by enteric bacteria like bifidobacteria, thus generating simple glycans (i.e., monosaccharides and oligosaccharides) that may become available to other microbial gut inhabitants (80).…”

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