Dietary fiber modulates gut microbiome and metabolome in a host sex-specific manner in a murine model of aging

Saurabh Kadyan; Gwoncheol Park; Bo Wang; Ravinder Nagpal

doi:10.3389/fmolb.2023.1182643

Dietary fiber modulates gut microbiome and metabolome in a host sex-specific manner in a murine model of aging

Front Mol Biosci. 2023 Jun 15:10:1182643. doi: 10.3389/fmolb.2023.1182643. eCollection 2023.

Authors

Saurabh Kadyan¹, Gwoncheol Park¹, Bo Wang², Ravinder Nagpal¹

Affiliations

¹ Department of Nutrition and Integrative Physiology, College of Health and Human Sciences, Florida State University, Tallahassee, FL, United States.
² Department of Biomedical and Chemical Engineering and Sciences, Florida Institute of Technology, Melbourne, FL, United States.

Abstract

Emerging evidence reveals the fundamental role of the gut microbiome in human health. Among various factors regulating our gut microbiome, diet is one of the most indispensable and prominent one. Inulin is one of the most widely-studied dietary fiber for its beneficial prebiotic effects by positively modulating the gut microbiome and microbial metabolites. Recent research underscores sexual dimorphism and sex-specific disparities in microbiome and also diet-microbiome interactions. However, whether and how the prebiotic effects of dietary fiber differ among sexes remain underexplored. To this end, we herein examine sex-specific differences in the prebiotic effects of inulin on gut microbiome and metabolome in a humanized murine model of aging i.e., aged mice carrying human fecal microbiota. The findings demonstrate that inulin exerts prebiotic effects, but in a sex-dependent manner. Overall, inulin increases the proportion of Bacteroides, Blautia, and glycine, while decreasing Eggerthella, Lactococcus, Streptococcus, trimethylamine, 3-hydroxyisobutyrate, leucine and methionine in both sexes. However, we note sex-specific effects of inulin including suppression of f_Enteroccaceae:_, Odoribacter, bile acids, malonate, thymine, valine, acetoin, and ethanol while promotion of Dubosiella, pyruvate, and glycine in males. Whereas, suppression of Faecalibaculum, Lachnoclostridium, Schaedlerella, phenylalanine and enhancement of Parasutterella, Phocaeicola, f_Lachnospiraceae;_, Barnesiella, Butyricimonas, glycine, propionate, acetate and glutamate are observed in females. Altogether, the study reveals that prebiotic mechanisms of dietary fiber vary in a sex-dependent manner, underscoring the importance of including both sexes in preclinical/clinical studies to comprehend the mechanisms and functional aspects of dietary interventions for effective extrapolation and translation in precision nutrition milieus.

Keywords: fiber; gut dysbiosis; inulin; metabolites; metabolomics; microbiota; prebiotics; sexual dimorphism.

Grants and funding

This work was supported by funding from the Pulse Crop Health Initiative program of the United States Department of Agriculture (USDA-ARS, Accession No. 440658) to RN. The findings and conclusions in this publication have not been formally disseminated by the USDA and should not be construed to represent any agency determination or policy. The Florida State University startup funds and FSU Council on Research and Creativity (CRC) First-Year Assistant Professor grant award (to RN) are also duly acknowledged. BW would like to thank the National Science Foundation (NSF; Grant No. 2245530) for support in metabolomics studies.