Abstract
ABSTRACTβ-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food. Currently, the collective understanding of β-mannan saccharification in the human colon is limited to a few keystone species, which presumably liberate low-molecular-weight mannooligosaccharide fragments that become directly available to the surrounding microbial community. Here, we show that a dominant butyrate producer in the human gut, Faecalibacterium prausnitzii, is able to acquire and degrade various β-mannooligosaccharides (β-MOS), which are derived by the primary mannanolytic activity of neighboring gut microbiota. Detailed biochemical analyses of selected protein components from their two β-MOS utilization loci (F. prausnitzii β-MOS utilization loci [FpMULs]) supported a concerted model whereby the imported β-MOS are stepwise disassembled intracellularly by highly adapted enzymes. Coculturing experiments of F. prausnitzii with the primary degraders Bacteroides ovatus and Roseburia intestinalis on polymeric β-mannan resulted in syntrophic growth, thus confirming the high efficiency of the FpMULs’ uptake system. Genomic comparison with human F. prausnitzii strains and analyses of 2,441 public human metagenomes revealed that FpMULs are highly conserved and distributed worldwide. Together, our results provide a significant advance in the knowledge of β-mannan metabolism and the degree to which its degradation is mediated by cross-feeding interactions between prominent beneficial microbes in the human gut.
Highlights
ABSTRACT b-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food
Endo-b-1,4-mannanase activity was originally reported for two GH113 enzymes, we demonstrated that a GH113 within the mannan utilization locus of R. intestinalis is a reducing end mannose-releasing exo-oligomannosidase
Biochemical work presented demonstrates that two MULs support the ability of F. prausnitzii to utilize b-MOS. b-MOS from diet are highly variable with respect to
Summary
ABSTRACT b-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food. Genomic, and detailed biochemical analyses, this work reveals the mechanism enabling F. prausnitzii, as a model Ruminococcaceae within Firmicutes, to cross-feed and access b-mannan-derived oligosaccharides released in the gut ecosystem by the action of primary degraders. Species within the Firmicutes phylum have been shown to organize cohorts of genes encoding glycan utilization systems into loci and being primary degraders of common dietary carbohydrates [7,8,9]. F. prausnitzii contributes to colonic epithelial homeostasis by stimulating the production of mucin O-glycans and by maintaining appropriate proportions of different cell types of the secretory lineage [16] These aforementioned properties make F. prausnitzii a potential novel health-promoting probiotic [17], and interventions aimed at increasing the representation of these butyrate-producing bacteria may be used to confer protection against several intestinal disorders
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