The claim of primacy of human gut Bacteroides ovatus in dietary cellobiose degradation

ABSTRACT

A demonstration of cellulose degrading bacterium from human gut changed our view that human cannot degrade the cellulose. However, investigation of cellulose degradation by human gut microbiota on molecular level has not been completed so far. We showed here, using cellobiose as a model that promoted the growth of human gut key members, such as Bacteroides ovatus (BO), to clarify the molecular mechanism. Our results showed that a new polysaccharide utilization locus (PUL) from BO was involved in the cellobiose capturing and degradation. Further, two new cellulases BACOVA_02626^GH5 and BACOVA_02630^GH5 on the cell surface performed the degradation of cellobiose into glucose were determined. The predicted structures of BACOVA_02626^GH5 and BACOVA_02630^GH5 were highly homologous with the cellulase from soil bacteria, and the catalytic residues were highly conservative with two glutamate residues. In murine experiment, we observed cellobiose reshaped the composition of gut microbiota and probably modified the metabolic function of bacteria. Taken together, our findings further highlight the evidence of cellulose can be degraded by human gut microbes and provide new insight in the field of investigation on cellulose.

KEYWORDS:

• Human gut microbiota
• cellobiose
• bacteroide ovatus
• cellulase
• structure

Acknowledgments

We take the chance to thank Zhongshan Municipal Bureau of Science and Technology for their funding support.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data statement

The data that support the findings of this study are available in Sequence Read Archive database (accession number PRJNA878605 for Transcriptomics and PRJNA877289 for 16S rRNA gene sequencing).

Author contributions

All authors have reviewed the final version of the manuscript and approved it for publication. This original manuscript has neither been published nor considering for publication in elsewhere. Among them, M.L. took the responsibility for all the experiments, design, data analysis and manuscript writing. Y.W. performed the Western blotting, qPCR, protein purification and antibody preparation. C.G. contributed to the preparation of antibody. S.W., Y.B., and L.Z. performed the protein structure predication and data analysis. K.D. supervised the whole project and revised the manuscript. All authors read and approved the final manuscript.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2227434

Additional information

Funding

The work was supported by National Key R&D Program of China [2022YFA1303802]; National Natural Science Foundation of China [Grants 31870801 and 31800673]; Shanghai Municipal Science and Technology Major Project, and partially supported by High-level new R&D institute [2019B090904008]; High-level Innovative Research Institute from Department of Science and Technology of Guangdong Province [2021B0909050003].