A Human Gut Commensal Ferments Cranberry Carbohydrates To Produce Formate

Abstract

Commensal bifidobacteria colonize the human gastrointestinal tract and catabolize glycans that are impervious to host digestion. Accordingly, Bifidobacterium longum typically secretes acetate and lactate as fermentative end products. This study tested the hypothesis that B. longum utilizes cranberry-derived xyloglucans in a strain-dependent manner. Interestingly, the B. longum strain that efficiently utilizes cranberry xyloglucans secretes 2.0 to 2.5 mol of acetate-lactate. The 1.5 acetate:lactate ratio theoretical yield obtained in hexose fermentations shifts during xyloglucan metabolism. Accordingly, this metabolic shift is characterized by increased acetate and formate production at the expense of lactate. α-l-Arabinofuranosidase, an arabinan endo-1,5-α-l-arabinosidase, and a β-xylosidase with a carbohydrate substrate-binding protein and carbohydrate ABC transporter membrane proteins are upregulated (>2-fold change), which suggests carbon flux through this catabolic pathway. Finally, syntrophic interactions occurred with strains that utilize carbohydrate products derived from initial degradation from heterologous bacteria. IMPORTANCE This was a study of bacterial metabolism of complex cranberry carbohydrates termed xyloglucans that are likely not digested prior to reaching the colon. This is significant, as bifidobacteria interact with this dietary compound to potentially impact human host health through energy and metabolite production by utilizing these substrates. Specific bacterial strains utilize cranberry xyloglucans as a nutritive source, indicating unknown mechanisms that are not universal in bifidobacteria. In addition, xyloglucan metabolism proceeds by using an alternative pathway that could lead to further research to investigate mechanisms underlying this interaction. Finally, we observed cross-feeding between bacteria in which one strain degrades the cranberry xyloglucan to make it available to a second strain. Similar nutritive strategies are known to occur within the gut. In aggregate, this study may lead to novel foods or supplements used to impact human health through rational manipulation of the human microbiome.

Enzymatic Adaptation of Bifidobacterium bifidum to Host Glycans, Viewed from Glycoside Hydrolyases and Carbohydrate-Binding Modules

“…Additionally, a correlation with the higher abundance of Bifidobacterium in the total microbiota was observed not only for B. bifidum in breast-fed infants, but also for B. longum, B. adolescentis, and B. catenulatum group in human subjects with a wide age range [44]. Interestingly, some B. longum and B. adolescentis strains were shown to have the capability to serve as cross-feeders of plant-derived polysaccharide degradants [92][93][94]. These observations suggested that intragenus cross-feeding might continue in the bifidobacterial community after weaning.…”

Deciphering the metabolic capabilities of Bifidobacteria using genome-scale metabolic models

“…Similar observations were shared by B. longum subsp. longum UCD401, which secrete high concentrations of formate with xyloglucans as substrate 39 . Furthermore, bifidobacterial secretion of formate while utilising glucose has also been previously observed 40 .…”

Oligosaccharides and Complex Carbohydrates: A New Paradigm for Cranberry Bioactivity

“…The use of multiple fraction names to describe essentially the same material has already led to some confusion regarding which cranberry materials and subfractions can be appropriately compared for even the relatively few studies investigating cranberry oligosaccharides to date [25][26][27][28][29]72,[112][113][114][115][131][132][133]. Insufficient material descriptions are also a problem as a minimal standardized method for characterizing and describing oligosaccharide fractions has yet to be established (see Table. Original, author-assigned fraction names have been used when possible but some (italics) have been elaborated upon or added to by the current authors to facilitate discussion.…”

“…Prior knowledge regarding the general nature and presence of oligosaccharides in cranberry materials [24,72,131] has enabled multiple research groups to pursue separations and analyses using methods specifically targeted to the enrichment or detection of oligosaccharides and other complex carbohydrates. The use of MALDI-TOF/TOF MS/MS techniques and extensive fragmentation pattern analyses has led to the proposal of possible structures for a number of major components within the cranberry xyloglucan series by multiple authors, but additional purified xyloglucans have yet to be obtained in sufficient quantity for full structural analysis and individual bioactivity studies.…”