Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans

Abstract

Bees are thought to be strict users of carbohydrates as metabolic fuel for flight. Many insects, however, have the ability to oxidize the amino acid proline at a high rate, which is a unique feature of this group of animals. The presence of proline in the haemolymph of bees and in the nectar of plants led to the hypothesis that plants may produce proline as a metabolic reward for pollinators. We investigated flight muscle metabolism of hymenopteran species using high-resolution respirometry performed on permeabilized muscle fibres. The muscle fibres of the honeybee, Apis mellifera, do not have a detectable capacity to oxidize proline, as those from the migratory locust, Locusta migratoria, used here as an outgroup representative. The closely related bumblebee, Bombus impatiens, can oxidize proline alone and more than doubles its respiratory capacity when proline is combined with carbohydrate-derived substrates. A distant wasp species, Vespula vulgaris, exhibits the same metabolic phenotype as the bumblebee, suggesting that proline oxidation is common in hymenopterans. Using a combination of mitochondrial substrates and inhibitors, we further show that in B. impatiens, proline oxidation provides reducing equivalents and electrons directly to the electron transport system. Together, these findings demonstrate that some bee and wasp species can greatly enhance the oxidation of carbohydrates using proline as fuel for flight.

Autumn shifts in cold tolerance metabolites in overwintering adult mountain pine beetles

“…It is possible that new mountain pine beetle adults use proline to decrease their supercooling point, though further study would be needed to confirm this possibility. Proline is also metabolized along with carbohydrates during flight [34,35]. Proline generation may serve a dual purpose where beetles use the amino acid as a cryoprotectant in the winter and then metabolize remaining proline as a flight fuel for dispersal.…”

Effect of proline-enriched abalone feed on selected metabolite levels of slow-growing adultHaliotis midae

“…The activation of fatty acid catabolism in this study is also supported by the working of proline, which stimulates mitochondrial activity. Although no literature supporting this in abalone could be found, evidence for this has previously been reported in other species like bumblebees (Teulier et al, ). Research done on plants show that during stress, proline and lipid metabolism share dual roles (Shinde, Villamor, Lin, Sharma, & Verslues, ), suggesting that proline has the ability to regulate β‐oxidation, subsequently resulting in decreased acetylcarnitine and an increase in alanine, as seen in this experiment (Figure ).…”

“…The activation of fatty acid catabolism in this study is also supported by the working of proline, which stimulates mitochondrial activity. Although no literature supporting this in abalone could be found, evidence for this has previously been reported in other species like bumblebees (Teulier et al, 2016). Research done on plants show that during stress, proline and lipid metabolism share dual roles (Shinde, Villamor, Lin, Sharma, & Verslues, 2016), suggesting that proline has the ability to regulate β-oxidation, subsequently resulting in decreased acetylcarnitine and an increase in alanine, as seen in this F I G U R E 5 Metabolic muscle profile of slow-growing Haliotis midae with comparative concentrations of those metabolites significantly different in the carbohydrate (blue), amino acid (green) and fatty acid (brown) metabolic pathways, are indicated by an increase (↑) or decrease (↓) in comparison to that fast-growing abalone group [Colour figure can be viewed at wileyonlinelibrary.com] experiment ( Figure 5).…”

Autumn shifts in cold tolerance metabolites in overwintering adult mountain pine beetles

“…It is possible that new mountain pine beetle adults use proline to decrease their supercooling point, though further study would be needed to confirm this possibility. Proline is also metabolized along with carbohydrates during flight (Gäde and Auerswald 2002; Teulier et al 2016). Proline generation may serve a dual purpose where beetles use the amino acid as a cryoprotectant in the winter and then metabolize remaining proline as a flight fuel for dispersal.…”