Role of Bifidobacterium pseudocatenulatum in Degradation and Consumption of Xylan-Derived Carbohydrates

Authors

Elizabeth Drey, University of Nebraska—Lincoln
Car Reen Kok, University of Nebraska—Lincoln
Robert Hutkins, University of Nebraska-LincolnFollow

Document Type

Article

Date of this Version

10-6-2022

Citation

Xylan and Xylooligosaccharide Utilization by Bifidobacteria. Applied and Environmental Microbiology. October 2022, Volume 88 Issue 20. DOI: 10.1128/aem.01299-22

Comments

Used by permission.

Abstract

Xylans, a family of xylose-based polysaccharides, are dietary fibers resistant to digestion. They therefore reach the large intestine intact; there, they are utilized by members of the gut microbiota. They are initially broken down by primary degraders that utilize extracellular xylanases to cleave xylan into smaller oligomers. The resulting xylooligosaccharides (XOS) can either be further metabolized directly by primary degraders or cross-feed secondary consumers, including Bifidobacterium. While several Bifidobacterium species have metabolic systems for XOS, most grow poorly on longer- chain XOS and xylan substrates. In this study, we isolated strains of Bifidobacterium pseudocatenulatum and observed that some, including B. pseudocatenulatum ED02, displayed growth on XOS with a high degree of polymerization (DP) and straight-chain xylan, suggesting a primary degrader phenotype that is rare in Bifidobacterium. In silico analyses revealed that only the genomes of these xylan-fermenting (xylan⁺) strains contained an extracellular GH10 endo-β-1.4 xylanase, a key enzyme for primary degradation of xylan. The presence of an extracellular xylanase was confirmed by the appearance of xylan hydrolysis products in cell-free supernatants. Extracellular xylanolytic activity was only detected in xylan⁺ strains, as indicated by the production of XOS fragments with a DP of 2 to 6, identified by thin-layer chromatography (TLC) and high-performance liquid chromatography (HPLC). Additionally, in vitro fecal fermentations revealed that strains with a xylan⁺ phenotype can persist with xylan supplementation. These results indicate that xylan⁺ B. pseudocatenulatum strains may have a competitive advantage in the complex environment of the gastrointestinal tract, due to their ability to act as primary degraders of xylan through extracellular enzymatic degradation.