Proline as a Sparker Metabolite of Oxidative Metabolism during the Flight of the Bumblebee, Bombus impatiens.

Ammar Saleem,Charles-A. Darveau,Nadia Stec

doi:10.3390/metabo11080511

Abstract

Several insect species use the amino acid proline as a major energy substrate. Although initially thought to be limited to blood-feeding dipterans, studies have revealed this capability is more widespread. Recent work with isolated flight muscle showed that the bumblebee Bombus impatiens can oxidize proline at a high rate. However, its role as a metabolic fuel to power flight is unclear. To elucidate the extent to which proline is oxidized to power flight and how its contribution changes during flight, we profiled 14 metabolites central to energy and proline metabolism at key time points in flight muscle and abdominal tissues. Ultra-high performance liquid chromatography-electrospray ionization-quadrupole time of flight mass spectrometry (UPLC-ESI-QTOF MS) analysis revealed that proline is likely used as a sparker metabolite of the tricarboxylic acid cycle at the onset of flight, whereby it supplements the intermediates of the cycle. Carbohydrates are the major energy substrates, which is evidenced by marked decreases in abdominal glycogen stores and a lack of alanine accumulation to replenish flight muscle proline. The time course of fuel stores and metabolites changes during flight highlights homeostatic regulation of energy substrates and patterns of changes in metabolic intermediates within pathways. This study clarifies the role of proline and carbohydrate metabolism during flight in hymenopterans, such as B. impatiens.

Highlights

Animals power their locomotion using various energy substrates, mostly carbohydrates and lipids, but sometimes favoring amino acids
Proline oxidation can be used to augment tricarboxylic acid (TCA) cycle intermediates required for acetyl-CoA oxidation [2,6], thereby serving as a so-called sparker of mitochondrial metabolism
The capacity to oxidize the amino acid proline may be linked to the ability to use it as a fuel for flight

Summary

Introduction

Animals power their locomotion using various energy substrates, mostly carbohydrates and lipids, but sometimes favoring amino acids. Locusts initially use carbohydrates as their main fuel, but eventually switch to the high energy content of lipids for long flights [1]. Other insects use amino acids as a source of energy, such as the blood-feeding tsetse fly, Glossina morsitans, that fuels its flight using proline almost exclusively [2,3]. Proline oxidation can be used to augment tricarboxylic acid (TCA) cycle intermediates required for acetyl-CoA oxidation [2,6], thereby serving as a so-called sparker of mitochondrial metabolism. Used to various extents and over different timelines among species that use it as main fuel or as a sparker of the TCA cycle, proline oxidation appears to be a common metabolic feature of diverse insect groups

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Conclusion