Structurally complex carbohydrates maintain diversity in gut-derived microbial consortia under high dilution pressure

Abstract

Dietary fibers are major substrates for maintaining and shaping gut microbiota, but the structural specificity of these fibers for the diversity, structure, and function of gut microbiota are poorly understood. Here, we employed an in vitro sequential batch fecal culture approach to address two ecological questions: 1) whether the chemical complexity of a carbohydrate influences its ability to maintain microbial diversity against high dilution pressure 2) whether substrate structuring or obligate microbe-microbe metabolic interactions (e.g. exchange of amino acids or vitamins) exert more influence on maintained diversity. Sorghum arabinoxylan (SAX, a complex polysaccharide), inulin (a low-complexity oligosaccharide) and their corresponding monosaccharide controls were selected as model carbohydrates. Our results demonstrate that complex carbohydrates stably sustain diverse microbial consortia. Furthermore, other metabolic interactions were less influential in structuring microbial consortia consuming SAX than inulin. Finally, very similar final consortia were enriched on SAX from the same individual's fecal microbiota one month later, suggesting that polysaccharide structure is more influential than stochastic alterations in microbiome composition in governing the outcomes of sequential batch cultivation experiments. These data suggest that carbohydrate structural complexity affords independent niches that structure fermenting microbial consortia, whereas other metabolic interactions govern the composition of communities fermenting simpler carbohydrates.

Fine Carbohydrate Structure of Dietary Resistant Glucans Governs the Structure and Function of Human Gut Microbiota

“…For each donor’s microbiota, collected samples were immediately placed into ice post-collection and rapidly transferred to an anaerobic chamber (Coy Laboratory Products, Grass Lake, MI, USA), where they were processed as previously described [ 15 ]. The basal media (phosphate buffer) contained NaCl, KCl, urea as the sole nitrogen source, Na 2 SO 4 , resazurin, Na 2 HPO 4, and were autoclaved together; heat sensitive compounds such as CaCl 2 , MgCl 2 , 1000X P1 metal solution and cysteine hydrochloride were added post-cooling.…”

“…Because the enzymes required for degradation of complex carbohydrates are highly specific to their cognate glycosidic linkages, and possibly to higher-order structures [ 12 , 13 ], there exists the potential for organisms to specialize in hydrolyzing specific bonds and/or consuming specific parts of the molecule [ 14 ]. If true, this niche partitioning may allow cooperative consumption of polysaccharides, in which organisms avoid competition through division of metabolic labor [ 15 ] and, thereby, increase the microbial diversity that can be sustained.…”

Genomic reconstruction of short-chain fatty acid production by the human gut microbiota

“…We also analyzed the Hadza 16S metagenomics dataset representing 222 HGM samples collected from a rural community of the Hadza hunter-gatherers from Tanzania (Schnorr et al, 2014). To analyze Spearman correlation between measured SCFA concentrations and predicted production capabilities, we also analyzed 16S datasets from published in vivo and in vitro fermentation studies of HGM microbiota (Chen M. et al, 2020;Deehan et al, 2020;Elmén et al, 2020). The 16S amplicon sequencing data from all of these datasets were analyzed using the dada2 plugin in QIIME2 (Caporaso et al, 2010).…”

“…In particular, in vivo dietary intervention studies allow to identify variable effects of dietary fibers on stimulation of production of SCFAs, especially butyrate, and link these effects to HGM composition ( Venkataraman et al, 2016 ; Baxter et al, 2019 ; Deehan et al, 2020 ). On another hand, experiments on in vitro bacterial fermentation of HGM inoculum allow to study the effect of individual dietary compounds on metabolic SCFA profiles and taxonomic composition under simultaneous control of a few key parameters of anaerobic fermentation experiments such as medium composition, temperature, fiber particle size and glycosidic bond configuration, speed of fermentation ( Reichardt et al, 2014 ; Harris et al, 2017 ; Fehlbaum et al, 2018 ; Chen M. et al, 2020 ; Miclotte et al, 2020 ; Thakkar et al, 2020 ; Yao et al, 2020 ; Teichmann and Cockburn, 2021 ). Extensive literature searches to identify in vitro batch fermentation studies of impact of fermentable carbohydrates on SCFA production, as recently reviewed by Harris et al (2020) , allowed the authors to classify non-digestible carbohydrate substrates according to their effect on promoting production of individual SCFA.…”

Dysregulated inflammation may predispose patients with serious mental illnesses to severe COVID‑19 (Review)

“…By contrast, beans and legumes are known for their low glycemic index, and contain the essential amino acids and micronutrients required for an appropriate and precisely targeted immune response ( 79 , 80 ). Furthemore, dietary fiber, abundantly present in a legume-rich diet, creates a suitable milieu for the survival and growth of gut microbiota and provides metabolic precursors for secondary bacterial metabolites that affect immunity and neurotransmission ( 81 , 82 ).…”