Near freezing temperatures are fatal for most animals. At low temperatures endothermic heart muscle fails when the calcium channels, which release the calcium signal that triggers a contraction, start leaking. But most fish's body temperatures are the same as the water they live in, even if the water is almost freezing. Matti Vornanen explains that some stenothermal fish spend their entire lives at low temperatures. In this issue of J. Exp. Biol, he describes how the stenothermal burbot protects its heart from the cold. Burbot cardiac muscle has a modified calcium delivery system that triggers the muscles contractions, so that the heart continues to function at temperatures when others would have failed (p. 1597).
Muscle fibres are built up from actin and myosin filaments that are linked by a myosin bridge. Each heartbeat is triggered by the release of calcium from a structure in each muscle cell called the sarcoplasmic reticulum (SR). The calcium signal prepares the myosin head to consume ATP, and slide the filaments past each other to drive the muscular contraction. But as temperatures drop, the SR calcium channels begin to leak, draining the SR's calcium store and causing heart failure.
Some cold adapted eurythermal fish survive low temperatures by enlarging their heart muscle, but how have fish that spend their entire life at low temperatures adapted to living in the freezer?
Vornanen decided that the burbot was the ideal species to answer this question. Working with Virpi Tiitu, he set out to characterise the burbot's heartbeat at its cold physiological temperature.
Not surprisingly, the hearts pumped best at 1°C. Vornanen began investigating what kept the heart pumping by looking at the muscle's ATPase that drives the contraction. If the ATPase was the key to keeping the heart muscle contracting, the enzyme's activity would be optimised for very low temperatures. But the burbot myocardial ATPase functioned best at 10°C. So Vornanen began looking to see how the burbot's sarcoplasmic reticulum stood up to the cold.
He tested the muscle's response to ryanodine, a compound that inhibits calcium channels. At low concentrations, ryanodine locks ion channels open while at higher levels, it clamps the channels shut. By inhibiting an increasing number of channels as the ryanodine concentration rises, the muscle begins to lose force as the SR's calcium pulse falls. Vornanen checked how the burbot heart responded to ryanodine at temperatures from 7°C down to 1°C. If the stenotherm's calcium channels behaved like mammalian channels,they would become leaky as the temperature dropped and the heart muscle fail. But if the channels were adapted to continue functioning at near freezing temperatures, the heart would weaken, but continue beating during the ryanodine treatment. The experiments confirmed that instead of becoming leaky,the burbot's channels function perfectly at 1°C.
Having proved that the key to cold survival is held by the SR calcium channels, Vornanen is keen to find out how these stenothermal calcium channels differ from their endothermal counterparts.