Feeding of cuticles from Tenebrio molitor larvae modulates the gut microbiota and attenuates hepatic steatosis in obese Zucker rats

Abstract

Insect biomass obtained from large-scale mass-rearing of insect larvae has gained considerable attention in recent years as an alternative and sustainable source of food and feed. A byproduct from mass-rearing of insect larvae is the shed cuticles – the most external components of insects which are a relevant source of the polysaccharide chitin. While it has been shown that chitin modulates the gut microbiota and ameliorates lipid metabolic disorders in obese rodent models, feeding studies dealing with isolated insects’ cuticles are completely lacking. Thus, the present study tested the hypothesis that dietary insects’ cuticles modulate the gut microbiome and improve hepatic lipid metabolism in obese Zucker rats. To test this hypothesis, three groups of obese Zucker rats were fed a nutrient-adequate, semisynthetic basal diet which was supplemented with either 0% (group O), 1.5% (group O1.5) or 3.0% (group O3.0) Tenebrio molitor cuticles at the expense of cellulose. Oil red O-stained liver sections showed a marked lipid accumulation, but lipid accumulation was clearly less in group O3.0 than in groups O and O1.5. In line with this, hepatic lipid concentrations were 30% lower in group O3.0 than in group O (p < 0.05). No differences were observed across the obese groups regarding liver concentrations of methionine, S-adenosylmethionine and homocysteine. Analysis of cecal microbial community at the family level revealed that the relative abundances of Bifidobacteriaceae, Coriobacteriaceae Erysipelotrichaceae, Lactobacillaceae, Prevotellaceae, Sutterellaceae, unknown Deltaproteobacteria and unknown Firmicutes were higher and those of Anaeroplasmataceae, Desulfovibrionaceae, Eubacteriaceae, Ruminococcaceae, Saccharibacteria and unknown Clostridiales were lower in group O3.0 compared to group O (p < 0.05). Cecal digesta concentrations of total short-chain fatty acids, acetate and butyrate were higher in group O3.0 than in group O (p < 0.05). Targeted plasma metabolomics revealed 53 metabolites differing between groups, amongst which two indole metabolites, indole-3-propionic acid and 3-indoxylsulfate, were markedly elevated in group O3.0 compared to groups O1.5 and O. Regarding that increased abundances of bacteria of the Actinobacteria phylum and Lactobacillaceae family in the gut have been reported to be associated with antisteatotic, hepatoprotective and antiinflammatory effects, the pronounced increases of Bifidobacteriaceae and Coriobacteriaceae (both Actinobacteria), and of Lactobacillaceae in group O3.0 might have contributed to the amelioration of fatty liver.