Substrate Use Prioritization by a Coculture of Five Species of Gut Bacteria Fed Mixtures of Arabinoxylan, Xyloglucan, β-Glucan, and Pectin

Abstract

Dietary fiber provides growth substrates for bacterial species that belong to the colonic microbiota of humans. The microbiota degrades and ferments substrates, producing characteristic short-chain fatty acid profiles. Dietary fiber contains plant cell wall-associated polysaccharides (hemicelluloses and pectins) that are chemically diverse in composition and structure. Thus, depending on plant sources, dietary fiber daily presents the microbiota with mixtures of plant polysaccharides of various types and complexity. We studied the extent and preferential order in which mixtures of plant polysaccharides (arabinoxylan, xyloglucan, β-glucan, and pectin) were utilized by a coculture of five bacterial species (Bacteroides ovatus, Bifidobacterium longum subspecies longum, Megasphaera elsdenii, Ruminococcus gnavus, and Veillonella parvula). These species are members of the human gut microbiota and have the biochemical capacity, collectively, to degrade and ferment the polysaccharides and produce short-chain fatty acids (SCFAs). B. ovatus utilized glycans in the order β-glucan, pectin, xyloglucan, and arabinoxylan, whereas B. longum subsp. longum utilization was in the order arabinoxylan, arabinan, pectin, and β-glucan. Propionate, as a proportion of total SCFAs, was augmented when polysaccharide mixtures contained galactan, resulting in greater succinate production by B. ovatus and conversion of succinate to propionate by V. parvula. Overall, we derived a synthetic ecological community that carries out SCFA production by the common pathways used by bacterial species for this purpose. Systems like this might be used to predict changes to the emergent properties of the gut ecosystem when diet is altered, with the aim of beneficially affecting human physiology. IMPORTANCE This study addresses the question as to how bacterial species, characteristic of the human gut microbiota, collectively utilize mixtures of plant polysaccharides such as are found in dietary fiber. Five bacterial species with the capacity to degrade polymers and/or produce acidic fermentation products detectable in human feces were used in the experiments. The bacteria showed preferential use of certain polysaccharides over others for growth, and this influenced their fermentation output qualitatively. These kinds of studies are essential in developing concepts of how the gut microbial community shares habitat resources, directly and indirectly, when presented with mixtures of polysaccharides that are found in human diets. The concepts are required in planning dietary interventions that might correct imbalances in the functioning of the human microbiota so as to support measures to reduce metabolic conditions such as obesity.

Activation of ectopic olfactory receptor 544 induces GLP-1 secretion and regulates gut inflammation

“… 45 Similar results have been reported showing dietary fibers, such as arabinoxylan, increased succinate production in a culture of mixed gut microorganisms. 46 However, the fecal levels of succinate are positively associated with body weight. 47 Thus, whether succinate represents a microbial-derived obesity-preventing metabolism or is a metabolite marker of obesity remains to be determined.…”

Sharing a β-Glucan Meal: Transcriptomic Eavesdropping on a Bacteroides ovatus-Subdoligranulum variabile-Hungatella hathewayi Consortium

“…The establishment of an in vitro consortium of anaerobic bacterial species common in the gut microbiota is consistent with limiting experimental systems to a manageable number of constituent species, making it easier in turn to measure interactions within the coculture (11,56,57). For example, augmented propionate production as a proportion of total short-chain fatty acids resulting from the fermentation of a mixture of plant glycans by a synthetic community (Bacteroides ovatus, Bifidobacterium longum subspecies longum, Megasphaera elsdenii, Ruminococcus gnavus, and Veillonella parvula) was recently reported (56). Increased propionate production was due to greater succinate production by B. ovatus from galactan fermentation and conversion of succinate to propionate by V. parvula.…”

Complementary Food Ingredients Alter Infant Gut Microbiome Composition and Metabolism In Vitro

“…Carrots and fruits such as kiwifruit, apple, blackcurrant, and other berries are known to contain pectin-rich cell-wall polysaccharides [67,68]. Pectins enable the growth of a more diverse microbial consortium, led by the early blooms of bifidobacteria, lactobacilli, and streptococci [21,39,40,69]. The resultant lactate and/or acetate may have facilitated the growth of a second line of bacteria, e.g., Lachnospiraceae.…”