Low plasma glucose limits glucose metabolism by RBCs and heart in some species of teleosts

Abstract

Within teleosts there is a species range in plasma glucose levels from undetectable to 20 mM. At low plasma glucose levels the gradient from the extracellular to the intracellular space is decreased. The impact of this on glucose metabolism by RBCs and heart from species with different steady state levels of plasma glucose (Atlantic cod ~ 5 mM; Atlantic salmon ~ 5 mM, cunner ~ 1 mM, lumpfish < 1 mM; short-horned sculpin < 1 mM) is the subject of this review. Under normoxia, at physiological levels of extracellular glucose, RBCs and heart produce lactate although the contribution of anaerobic metabolism to ATP production is small. Sustained lactate production from extracellular glucose appears to be the primary fate of extracellular glucose. In many cases, glycogen is not mobilized and the rate of glucose metabolism = two times the rate of lactate production. As such, alternative metabolic sources are required to fuel oxidative metabolism. Under hypoxia, hearts from Atlantic cod and rainbow trout increase rates of both glucose metabolism and lactate production, partially supported by glycogen reserves. But in lumpfish and short-horned sculpin hearts there is no change in rates of glucose metabolism. The most likely explanation is that glucose uptake is compromised in lumpfish and short-horned sculpin hearts due to a low diffusion gradient. Under these conditions rates of lactate production are well below that of Atlantic cod or rainbow trout. Energy demand must be reduced under hypoxia in lumpfish and short-horned sculpin hearts in order to maintain ATP balance.

Introduction

Glucose is considered to be a universal aerobic fuel and an essential anaerobic fuel. Chavin and Young (1970) presented a comprehensive table of blood glucose levels in teleosts in which a wide species specific range from undetectable to 21 mM was noted with most species being in the 3 to 8 mM window. Numerous species, such as Atlantic wolfish (Anarhichas lupus), ocean pout (Macrozoarces americanus), anglerfish (Lophius americanus) and others had at least some individuals with glucose concentrations below 1 mM. Polakof and colleagues updated this information in reviews that address the regulation of glucose levels and glucose sensing mechanisms (Polakof et al., 2011, Polakof et al., 2012). These papers also provide an extensive summary of the literature that establishes that blood glucose levels are generally lower in ectothermic than endothermic vertebrates (average blood glucose for numerous species of fish, amphibians, and reptiles is approximately 4 mM; mammals approximately 8 mM; birds approximately 15 mM). There is a wide range in species variability that is beyond the scope of this review. The comprehensive documentation in Polakof et al. (2011) and Polakof et al. (2012) confirms the extremely low levels (< 1 mM) of blood glucose in some fish. Low levels of plasma glucose will result in a low diffusion gradient from the extra- to the intracellular space. Experiments that address the impact of low plasma glucose on the capacity to utilize glucose are only now being conducted in a systematic fashion. Here recent findings with fish red blood cells (RBCs) and heart are summarized.