Isolation and Characterization of an Agaro-Oligosaccharide (AO)-Hydrolyzing Bacterium from the Gut Microflora of Chinese Individuals

Abstract

Agarose (AP) from red algae has a long history as food ingredients in East Asia. Agaro-oligosaccharides (AO) derived from AP have shown potential prebiotic effects. However, the human gut microbes responsible for the degradation of AO and AP have not yet been fully investigated. Here, we reported that AO and AP can be degraded and utilized at various rates by fecal microbiota obtained from different individuals. Bacteroides uniformis L8 isolated from human feces showed a pronounced ability to degrade AO and generate D-galactose as its final end product. PCR-DGGE analysis showed B. uniformis to be common in the fecal samples, but only B. uniformis L8 had the ability to degrade AO. A synergistic strain, here classified as Escherichia coli B2, was also identified because it could utilize the D-galactose as the growth substrate. The cross-feeding interaction between B. uniformis L8 and E. coli B2 led to exhaustion of the AO supply. Bifidobacterium infantis and Bifidobacterium adolescentis can utilize one of the intermediates of AO hydrolysis, agarotriose. Growth curves indicated that AO was the substrate that most favorably sustained the growth of B. uniformis L8. In contrast, κ-carrageenan oligosaccharides (KCO), guluronic acid oligosaccharides (GO), and mannuronic acid oligosaccharides (MO) were found to be unusable to B. uniformis L8. Current results indicate that B. uniformis L8 is a special degrader of AO in the gut microbiota. Because B. uniformis can mitigate high-fat-diet-induced metabolic disorders, further study is required to determine the potential applications of AO.

Carrageenan oligosaccharides and their degrading bacteria induce intestinal inflammation in germ-free mouse

“…Similar to a previous report[53], the presence of E. coli improved the KCO degradation ability of B.xylanisolvens, suggesting a cross-feeding phenomenon exists between the KCO degrader and E. coli[53]. We hypothesize that E. coli can utilize the metabolites generated by B. xylanisolvens, particularly galactose, thereby reducing the negative feedback of monosaccharide degradation products (on carrageenase synthesis) in B. xylanisolvens and improving its KCO degradation capacity[53]. Moreover, PCR-DGGE analysis and DGGE band sequencing showed that KCO could promote the growth of B. xylanisolvens in five of eight fecal samples with KCO degradation capacity(Fig.…”

“…By in vitro KCObased batch fermentation and degradation screening, a KCO-degrading species, B. xylanisolvens, and its partner strain, E. coli, were identified. Similar to a previous report[53], the presence of E. coli improved the KCO degradation ability of B.xylanisolvens, suggesting a cross-feeding phenomenon exists between the KCO degrader and E. coli[53]. We hypothesize that E. coli can utilize the metabolites generated by B. xylanisolvens, particularly galactose, thereby reducing the negative feedback of monosaccharide degradation products (on carrageenase synthesis) in B. xylanisolvens and improving its KCO degradation capacity[53].…”

Structural features underlying prebiotic activity of conventional and potential prebiotic oligosaccharides in food and health

“…Agaro‐oligosaccharides (AO) generated by acid hydrolysis have been demonstrated to significantly increase the bifidobacterial populations without influencing other bacterial populations such as Bacteroides , Lactobacilli / Enterococci , Eubacterium rectale / Clostridium coccoides and Clostridium histolyticum (Ramnani et al, ). Contrastingly, Li et al found Bifidobacterium infantis and Bifidobacterium adolescentis to be able to utilize agarotriose, which is an intermediate of AO hydrolysis and not the AO as such (Li et al, ). This indicates that the bifidobacteria are not the primary degraders of AO.…”

“…Agar is a linear polysaccharide consisting of 3,6‐anhydro‐ l ‐galactose and d ‐galactose units alternately linked by α‐(1, 3) and β‐(1, 4) glycosidic bonds and is extracted from marine red seaweeds such as Gelidium and Gracilaria (Li et al, ). Higher molecular weight neoagaro‐oligosaccharides generated from agar by hydrolysis with β‐agarase (β‐1, 4 linkages) have been demonstrated to have bifidogenic activity in vitro and a large positive influence in lactobacilli populations, both in vitro and in mice (Hu et al, ).…”

“…This indicates that the bifidobacteria are not the primary degraders of AO. In the same study, isolated Bacteroides uniformis L8 from human feces was shown to have a pronounced ability to degrade AO and generate d ‐galactose and can therefore be considered the primary organism responsible for AO fermentation (Li et al, ). In contrast, κ‐carrageenan oligosaccharides (KCO), guluronic acid oligosaccharides (GO), and mannuronic acid oligosaccharides (MO) were found to be unusable to B. uniformis L8 (Li et al, ).…”