Response of Tribolium castaneum to dietary mannitol, with remarks on its possible nutritive effects

Abstract

Mannitol, one of the sugar alcohols, is often used as a low-calorific carbohydrate by animals. In some insects, mannitol acts as a cryoprotectant to endure coldness, but also become a poisonous agent. Adults of the red flour beetle Tribolium castaneum were shown to recognize mannitol as a factor stimulating their feeding behavior, but it remains unclear whether T. castaneum can utilize mannitol as a source of nutrition, because the enzymes needed to metabolize mannitol are unknown in this species. This study shows that T. castaneum utilizes mannitol as a nutrient in a dietary assay based on a sole carbon source added to artificial gypsum diet. The amount of mannitol excreted was less than that ingested, suggesting that it is absorbed in the insect body. The hemolymph of T. castaneum contained no mannitol but contained trehalose, a known blood sugar in insects, even after being fed mannitol. This study also revealed that dietary mannitol was metabolized to triglyceride, the main component of the fat body, forming lipid droplets. It was found that metabolites of a mannitol-supplemented diet extend the lifespan of T. castaneum, compared with those obtained by metabolizing a mannitol-free diet. Given that the insects presented transcriptional changes upon being fed carbohydrates, it might be possible to identify specific genes related to mannitol-specific metabolism by their upregulation upon mannitol intake in T. castaneum. The present study investigated mannitol-responsive gene expression using RNA-Seq. Twenty-eight genes, including those encoding trehalose-6-phosphate synthase and fatty acid synthase, were differentially expressed between beetles that were fed or not fed mannitol. The identification of upregulated genes provides us with important insights into the molecular events following mannitol intake.

Mannitol ingestion causes concentration-dependent, sex-specific mortality in adults of the fruit fly (Drosophila melanogaster)

“…If mannitol cannot be metabolized efficiently it may accumulate in the crop. T. castaneum beetles likely utilizes NADP + -dependent D-arabitol dehydrogenase for mannitol catalysis [9] but this enzyme is not found in D. melanogaster [42]. Sorbitol dehydrogenase (SDH) is another possible pathway for mannitol breakdown [43], as mannitol is an isomer of sorbitol [44] and SDH is found in Drosophila (Gene ID: 40836, 41313) [45].…”

“…Mannitol reduced survival and prevented adult female reproduction in Pimpla turionellae ichneumonid wasps [7]. In contrast, mannitol stimulated feeding behavior at low doses (72.6mM) in red flour beetles ( Tribolium castaneum ) and increased the longevity of females in comparison to males [8-9]. In contrast, adult female Drosophila melanogaster fed 1M mannitol food showed significantly decreased longevity over a seventeen-day trial in comparison to males [10].…”

Larval mannitol diets increase mortality, prolong development, and decrease adult body sizes in fruit flies (Drosophila melanogaster)

“…Because concentrations of all non-mannitol carbohydrates were kept the same in larval foods, D. melanogaster would need to be able to metabolize mannitol in order for it to increase levels of trehalose in the hemolymph like the other, metabolizable sugars (glucose and sucrose) used in previous studies. No studies have examined if D. melanogaster , or its common gut microbes, can metabolize mannitol, but recent work on another insect, Tribolium castaneum , shows that adult females have higher trehalose levels in the hemolymph after feeding on mannitol [26]. Circulating trehalose is responsible for TOR activation in D. melanogaster fat bodies, contributing to cell growth during development; mannitol’s catalysis to trehalose may be responsible for mediating its effects on growth rate and the interval to the cessation of growth via the insulin/TOR signaling pathway similar to other carbohydrates [11,45].…”

“…In the sweet potato whitefly ( Bemisia tabaci ), mannitol was found not to be lethal to nymphs, only adults, at a concentration of 10% [70]. Given mannitol’s vastly different effects on adults of different species (from nutritive to lethal), more work should be done to understand mannitol’s effects on development across taxa [20,26,27,70–74]. This may further our understanding of how species differ mechanistically in their responses to this polyol, particularly important since adverse mannitol developmental effects closely align with the phenotypic effects of high-sugar diets on D. melanogaster larvae, mediated via the insulin-signaling pathway.…”

“…Mannitol is used as a low-calorie sweetener, sweetening foods without increasing blood glucose levels or insulin in humans [24,25]. However, ingestion and breakdown of mannitol by Tribolium castaneum beetles increased hemolymph trehalose levels, indicating mannitol may be a nutritive source of dietary carbohydrates in some insect taxa [26,27]. We hypothesized that mannitol ingestion during D. melanogaster development would generate phenotypes similar to those produced by high sugar diets [10,17,18].…”