Elevated osmolytes in rainbow smelt: the effects of urea, glycerol and trimethylamine oxide on muscle contractile properties

Abstract

Rainbow smelt, Osmerus mordax, experience a wide range of temperatures in their native habitat. In response to cold, smelt express anti-freeze proteins and the osmolytes glycerol, trimethylamine N-oxide (TMAO) and urea to avoid freezing. The physiological influences of these osmolytes are not well understood. Urea destabilizes proteins, while TMAO counteracts the proteindestabilizing forces of urea. The influence of glycerol on muscle function has not been explored. We examined the effects of urea, glycerol and TMAO through muscle mechanics experiments with treatments of the three osmolytes at physiological concentrations. Experiments were carried out at 10°C. The contractile properties of fast-twitch muscle bundles were determined in physiological saline and in the presence of 50 mmol l −1 urea, 50 mmol l −1 TMAO and/or 200 mmol l −1 glycerol in saline. Muscle exposed to urea and glycerol produced less force and displayed slower contractile properties. However, treatment with TMAO led to higher force and faster relaxation by muscle bundles. TMAO increased power production during cyclical activity, while urea and glycerol led to reduced oscillatory power output. When muscle bundles were exposed to a combination of the three osmolytes, they displayed little change in contraction kinetics relative to control, although power output under lower oscillatory conditions was enhanced while maximum power output was reduced. The results suggest that maintenance of muscle function in winter smelt requires a balanced combination of urea, glycerol and TMAO.

Rainbow smelt: the unusual case of cryoprotection by sustained glycerol production in an aquatic animal

“…In addition, fish acclimated to 5 °C had faster muscle contractile properties such as maximum shortening velocity (Woytanowski and Coughlin 2013). Although the data are preliminary, it also appears that maintenance of muscle function in winter rainbow smelt requires a balanced combination of glycerol, urea, and TMAO (Coughlin et al 2014). These findings need to be extended to animals at sub-zero temperatures to assess the possibility that glycerol accumulation relates to swimming capability.…”

Red muscle function and thermal acclimation to cold in rainbow smelt, Osmerus mordax, and rainbow trout, Oncorhynchus mykiss

“…The oscillatory power output of red muscle bundles was determined using work loop experiments at 10°C, where the muscle was oscillated to simulate muscle activity during swimming (Coughlin, Long, et al, ). Work loop activation conditions to maximize power at each oscillation frequency were determined through pilot experiments.…”

“…Because of the freeze resistance measures used by smelt, they are able to take advantage of a nutrient-rich location that many other fish are unable to use (Driedzic & Ewart, 2004). A thermal acclimation response of the muscle to cold water permits an active feeding even in the coldest of winter months (Coughlin, Long, Gezzi, Modi, & Woluko, 2016;Woytanowski & Coughlin, 2012). Trout are relatively stenothermal in comparison with smelt-trout prefer temperatures ranging from 12 to 16°C but are known to survive in water temperature ranging from 5 to 24°C (Candiotto, Bo, & Fenoglio, 2011).…”