Interactions between gut commensal bacteria and polysaccharides derived from algae and legumes: identification of metabolites produced and pathways involved.

UNLABELLED: Diet is a key driver of gut microbiome functions, largely via microbial fermentation of dietary fibers. We investigated how 15 human gut commensals from Bacteroidota, Bacillota, and Actinomycetota metabolize structurally distinct poly-/oligosaccharides from algae (Ulva lactuca, Saccharina latissima, Undaria pinnatifida) and chickpeas (Cicer arietinum). In low-nutrient, carbon-defined cultures, we quantified growth (ΔOD), acidification (ΔpH), and short-chain fatty acids (SCFAs). Then, we conducted untargeted liquid chromatography-high-resolution mass spectrometry (LC-HRMS) metabolomics and RNA sequencing on eight representative strains. Chickpea raffinose-family oligosaccharides (RFOs) broadly stimulated growth, fermentation, and SCFA production across phyla, whereas algal polysaccharide use was restricted to specific Bacteroidota species. Metabolomics revealed phylum- and strain-resolved signatures and bioactive molecules beyond SCFAs, including tryptophan derivatives (for example, indolelactic acid), γ-aminobutyric acid (GABA), and micronutrient-related compounds (for example, riboflavin), whose abundance depended on both taxon and substrate. Transcriptomic analysis in the presence of raffinose indicated coordinated activation of carbohydrate-active enzymes (CAZymes), specialized transport systems (SusC/D, TonB, or ATP-binding cassette [ABC] transporters), and transcriptional regulators (for example, LacI), consistent with substrate-responsive carbohydrate gene clusters. Bacteroidota exhibited the largest CAZyme mobilization and transcriptional remodeling, while Bacillota and Actinomycetota showed targeted responses consistent with narrower substrate scopes.

CONCLUSIONS: Fiber structure mechanistically links to selective microbial functions. Pulses-derived RFOs elicit broad, phylum-specific metabolic programs, and algae polysaccharides engage a limited set of Bacteroidota specialists. This integrative framework (growth, SCFAs, metabolomics, transcriptomics) refines how discrete fiber types can be matched to microbial capacities, informing precision-nutrition strategies that leverage sustainable fibers (pulses, algae) to promote health-relevant metabolites and targeted microbiome modulation.