Carotenoids modulate fermentation of inulin ex vivo in IBS and overweight adult gut microbiota.

BACKGROUND

Carotenoids have direct antioxidant and anti-inflammatory health benefits. Owing to their low bioavailability, they also reach the colon, yet their microbiome interactions remain poorly characterized.

METHODS

We investigated how β-carotene (BC), lutein (LU), lycopene (LY) and zeaxanthin (ZE), at biological relevant doses (between 1 and 60 mg/d), impact composition and metabolite production of irritable bowel syndrome (IBS) and overweight (OW) adult gut microbiota using the ex vivo SIFR® fermentation system (systemic intestinal fermentation research). Fresh fecal samples were collected from 12 donors (n = 6 per cohort) and incubated for 24 h under anaerobic conditions, with carotenoids administered alone or in combination with prebiotic inulin (IN, tested at 2.5 g/day).

RESULTS

We observed phenotype-specific microbiota characteristics for each cohort at baseline. Carotenoids alone had only minor effects but in combination with prebiotic inulin significantly altered community composition (Bray-Curtis dissimilarity, P < 0.05) and enhanced short-chain fatty acid (SCFA) production. Most carotenoids increased butyrate production vs. inulin alone with ZE (at 2 mg/d) in IBS (+ 7.6%) and LU (at 60 mg/d) in OW (+ 8.0%) showing the strongest effects (padjusted<0.10). In contrast, LY (at 45 mg/d) uniquely increased acetate (+ 3.5%) and propionate (+ 8.0%) at the expense of butyrate (-7.5%, padjusted<0.10) when compared vs. inulin only. Changes in SCFA correlated with carotenoid- and cohort-specific shifts in the abundance of Bifidobacterium, Alistipes, Akkermansia, Faecalibacterium and Coprococcus. ZE also enhanced the effect of inulin on the health-related metabolites 3-phenyllactic acid (PLA) and 2-hydroxyisocaproic acid (HICA), particularly IBS subjects (padjusted<0.20).

CONCLUSIONS

Antioxidant carotenoids may support anaerobic gut microbes including dominant butyrate producers and counteract phenotype-specific dysbiosis, potentially offering novel dietary approaches for IBS and obesity-associated dysbiosis. As these effects were observed when carotenoids were combined with inulin, carotenoids may have greater impacts when consumed as part of a fiber-rich diet, reflecting their natural occurrence in plant-based foods.