Resistant starches from dietary pulses modulate the gut metabolome in association with microbiome in a humanized murine model of ageing

Authors: KADYAN, SAURABH - Florida State University; PARK, GWONCHEOL - Florida State University; WANG, BO - Florida Institute Of Technology; SIGNH, PRASHANT - Florida State University; ARJMANDI, BAHRAM - Florida State University; NAGPAL, RAVINDER - Florida State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/29/2023
Publication Date: 6/29/2023
Citation: Kadyan, S., Park, G., Wang, B., Signh, P., Arjmandi, B., Nagpal, R. 2023. Resistant starches from dietary pulses modulate the gut metabolome in association with microbiome in a humanized murine model of ageing. Scientific Reports. 13. Article 10566. https://doi.org/10.1038/s41598-023-37036-w.
DOI: https://doi.org/10.1038/s41598-023-37036-w

Interpretive Summary: Evidence suggests that plant-based fiber-rich diets improve ageing-associated health by fostering a healthier gut microbiome and a healthier mix of microbial metabolites derived from that microbiome (otherwise known as the metabolome). However, the effects and mechanisms of resistant starches from dietary pulses on the composition of the metabolome remain unclear. In this study, we examined the prebiotic effects of dietary pulse-derived resistant starch on the gut metabolome in older mice carrying a human microbiome. We focused on resistant starches from pinto beans, black-eyed peas, lentils, or chickpeas, compared to the soluble fiber, inulin. We identified specific modulations in the gut metabolome and in microbiome-metabolome interactions within the ageing gut, based on which dietary pulses were consumed. Reductions in gut bile acids and cholesterol, and positive alterations in amino acid metabolism, were observed in animals fed pulse-derived resistant starches. These findings demonstrate the functional effects of pulse products on gut microbial metabolism and their benefit to physiological responses in an aged individual.

Technical Abstract: Emerging evidence suggests that plant-based fiber-rich diets improve ageing-associated health by fostering a healthier gut microbiome and microbial metabolites. However, such effects and mechanisms of resistant starches from dietary pulses remain underexplored. Herein, we examine the prebiotic effects of dietary pulses-derived resistant starch (RS) on gut metabolome in older (60-week old) mice carrying a human microbiome. Gut metabolome and its association with microbiome are examined after 20-weeks feeding of a western-style diet (control; CTL) fortified (5% w/w) with RS from pinto beans (PTB), black-eyed-peas (BEP), lentils (LEN), chickpeas (CKP), or inulin (INU; reference control). NMR spectroscopy-based untargeted metabolomic analysis yield differential abundance linking phenotypic differences in specific metabolites among different RS groups. LEN and CKP increase butyrate, while INU promotes propionate. Conversely, bile acids and cholesterol are reduced in prebiotic groups along with suppressed choline-to-trimethylamine conversion by LEN and CKP, whereas amino acid metabolism is positively altered. Multi-omics microbiome-metabolome interactions reveal an association of beneficial metabolites with the Lactobacilli group, Bacteroides, Dubosiella, Parasutterella, and Parabacteroides, while harmful metabolites correlate with Butyricimonas, Faecalibaculum, Colidextribacter, Enterococcus, Akkermansia, Odoribacter, and Bilophila. These findings demonstrate the functional effects of pulses-derived RS on gut microbial metabolism and their beneficial physiologic responses in an aged host.