Open AccessHuman Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides
Author(s) -
Lars Jordhøy Lindstad,
Galiana Lo,
Shaun Leivers,
Zijia Lu,
Leszek Michalak,
Gabriel Vasconcelos Pereira,
Åsmund K. Røhr,
Eric C. Martens,
Lauren S. McKee,
Petra Louis,
Sylvia H. Duncan,
Bjørge Westereng,
Phillip B. Pope,
Sabina Leanti La Rosa
Publication year - 2021
Publication title -
mbio
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.562
H-Index - 121
eISSN - 2161-2129
pISSN - 2150-7511
DOI - 10.1128/mbio.03628-20
Subject(s) - faecalibacterium prausnitzii , mannan , bacteroides thetaiotaomicron , roseburia , biology , microbiology and biotechnology , gut flora , bacteroides , butyrate , human microbiome , firmicutes , bacteria , biochemistry , microbiome , polysaccharide , genetics , fermentation , 16s ribosomal rna
β-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 [ Fp MULs]) 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 Fp MULs’ uptake system. Genomic comparison with human F. prausnitzii strains and analyses of 2,441 public human metagenomes revealed that Fp MULs 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.