Recent insight into oligosaccharide uptake and metabolism in probiotic bacteria

Abstract

In recent years, a plethora of studies have demonstrated the paramount physiological importance of the gut microbiota on various aspects of human health and development. Particular focus has been set on probiotic members of this community, the best studied of which are assigned into the Lactobacillus and Bifidobacterium genera. Effects such as pathogen exclusion, alleviation of inflammation and allergies, colon cancer, and other bowel disorders are attributed to the activity of probiotic bacteria, which selectively ferment prebiotics comprising mainly non-digestible oligosaccharides. Thus, glycan metabolism is an important attribute of probiotic action and a factor influencing the composition of the gut microbiota.

In the quest to understand the molecular mechanism of this selectivity for certain glycans, we have explored the routes of uptake and utilization of a variety of oligosaccharides differing in size, composition, and glycosidic linkages. A combination of “omics” technologies bioinformatics, enzymology and protein characterization proved fruitful in elucidating the protein transport and catabolic machinery conferring the utilization of glucosides, galactosides, and xylosides in the two clinically validated probiotic strains Lactobacillus acidophilus NCFM and Bifidobacterium animalis subsp. lactis Bl-04. Importantly, we have been able to identify and in some cases validate the specificity of several transport systems, which are otherwise poorly annotated. Further, we have demonstrated for the first time that non-naturally occurring tri- and tetra-saccharides are internalized and efficiently utilized by probiotic bacteria in some cases better than well-established natural prebiotics.

Selected highlights of these data are presented, emphasising the importance and the diversity of oligosaccharide transport in probiotic bacteria.

Keywords::

• Prebiotic
• oligosaccharide uptake
• ATP-binding cassette transport system
• phosphotransferase system
• transcriptional analysis

Acknowledgments

Karina Jansen, Mette Pries, and Anne Blicher (Technical University of Denmark); Dorthe Boelskifte and Jens-Christian Navarro Poulsen (University of Copenhagen) are thanked for technical assistance. Alexander Viborg Holm is thanked for providing help with bioinformatics of GH4.

Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.

This work was supported by a grant from the Danish Strategic Research Council's Programme Committee on Health, Food, and Welfare to the project “Gene discovery and molecular interactions in prebiotics/probiotics systems. Focus on carbohydrate prebiotics” as well as the Danish Natural Science Research Council, the Centre for Advanced Food Studies and the Carlsberg Foundation. The Technical University of Denmark is acknowledged for a H. C. Ørsted postdoctoral fellowship to AM and for PhD scholarships to JMA, MSM and ME. DuPont is also acknowledged for financial support for PhD student JMA.