Characterization of Bifidobacterium kashiwanohense that utilizes both milk- and plant-derived oligosaccharides

ABSTRACT

Bifidobacteria are prominent members of the human gut microbiota throughout life. The ability to utilize milk- and plant-derived carbohydrates is important for bifidobacterial colonization of the infant and adult gut. The Bifidobacterium catenulatum subspecies kashiwanohense (B. kashiwanohense) was originally isolated from infant feces. However, only a few strains have been described, and the characteristics of this subspecies have been poorly investigated. Here, we characterized genotypes and phenotypes of 23 B. kashiwanohense-associated strains, including 12 newly sequenced isolates. Genome-based analysis clarified the phylogenetic relationship between these strains, revealing that only 13 strains are genuine B. kashiwanohense. We defined specific marker sequences and investigated the worldwide prevalence of B. kashiwanohense based on metagenome data. This revealed that not only infants but also adults and weaning children harbor this subspecies in the gut. Most B. kashiwanohense strains utilize long-chain xylans and possess genes for extracellular xylanase (GH10), arabinofuranosidase and xylosidase (GH43), and ABC transporters that contribute to the utilization of xylan-derived oligosaccharides. We also confirmed that B. kashiwanohense strains utilize short- and long-chain human milk oligosaccharides and possess genes for fucosidase (GH95 and GH29) and specific ABC transporter substrate-binding proteins that contribute to the utilization of a wide range of human milk oligosaccharides. Collectively, we found that B. kashiwanohense strains utilize both plant- and milk-derived carbohydrates and identified key genetic factors that allow them to assimilate various carbohydrates.

KEYWORDS:

• Bifidobacterium kashiwanohense
• xylan
• human milk oligosaccharide
• plant-derived carbohydrate
• extracellular xylanase
• ABC transporter SBP

Acknowledgments

We thank Akira Shigehisa, Takuya Takahashi, and Hirokazu Tsuji for execution of the study and critical reviews. This research was financially supported by Yakult Central Institute.

Disclosure statement

All authors are employees of Yakult Honsha Co., Ltd.

Author contributions

T. Matsuki and K. Orihara conceived and designed the experiments. K. Orihara, K. Oki, T. Hara, and N. Tsukuda performed DNA sequencing and genome analysis. K. Orihara and Y. Watanabe performed metagenome analysis. K. Yahagi, T. Hara, and K. Orihara purified HMOs and investigated HMOs utilization. K. Orihara, Y. Saito, and T. Sasai contributed the SBP-HMO interaction and 3D structure prediction. J. Fujimoto contributed to the design and execution of the study. K. Orihara and T. Matsuki wrote the manuscript. All authors reviewed and approved the manuscript.

Data availability statement

The bifidobacterial genome sequences have been deposited in the NCBI Sequence Read Archive under BioProject Accession Code PRJNA883016 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA883016)

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2207455.

Additional information

Funding

This work was supported by Yakult Honsha Co., Ltd.