Bioenergetic Pathways in the Sperm of an Under-Ice Spawning Fish, Burbot (Lota lota): The Role of Mitochondrial Respiration in a Varying Thermal Environment

Abstract

Simple SummaryThe burbot (Lota lota) is the only endangered or threatened freshwater gadoid that usually spawns in icy waters (<6 °C), and whereas the sperm bioenergetics of many fish species have been studied in the context of adaptation to warmer environments, the sperm of cold-water fish are the least explored. Therefore, this study was undertaken to determine both the roles of the most important energy-supplying pathway(s) in the burbot before and after sperm become motile at the spawning temperature, and the mitochondrial adaptation at the maximum temperature that is tolerable. The results reveal that burbot sperm have a naturally low oxygen consumption rate (respiration) and a limited capacity for enhancement under exposure to an uncoupler. Oxidative phosphorylation is more realized near the critical thermal tolerance limit. However, similar to the sperm of most other freshwater species, this pathway, which occurs during motility, is insufficient to fulfill the large energy demands of the motile sperm. Therefore, be it at the spawning temperature or at a higher temperature, the majority of the energy required for motility is derived from pre-stored ATP reserves produced during a quiescent state.Regarding the sperm of cold-water fish, the contributions of different bioenergetic pathways, including mitochondrial respiration, to energy production at the spawning temperature and its adaptation at the maximum critical temperature (CTmax) are unclear. The roles of glycolysis, fatty acid oxidation, oxidative phosphorylation (OXPHOS) at 4 °C, and OXPHOS at 15 °C for energy production in burbot (Lota lota) spermatozoa were studied by motility and the oxygen consumption rate (OCR) (with and without pathway inhibitors and the OXPHOS uncoupler). At both temperatures, the effects of the inhibitors and the uncoupler on the motility duration, curvilinear velocity, and track linearity were insignificant; in addition, the OCRs in activation and non-activation media differed insignificantly and were not enhanced after uncoupler treatment. After inhibitor treatment in both media, OXPHOS was insignificantly different at the 2, 30, and 60 s time points at 4 °C but was reduced significantly at the 30 and 60 s time points after treatment with sodium azide at 15 °C. In conclusion, for burbot sperm at both the spawning temperature and the CTmax, the energy synthesized via OXPHOS during motility was insufficient. Therefore, the majority of the energy required to sustain motility was derived from pre-accumulated energy produced and stored during the quiescent state of the spermatozoa.