Superfast contractions without superfast energetics: ATP usage by SR‐Ca2+ pumps and crossbridges in toadfish swimbladder muscle

Abstract

1. The rate at which an isometrically contracting muscle uses energy is thought to be proportional to its twitch speed. In both slow and fast muscles, however, a constant proportion (25-40 %) of the total energy has been found to be used by SR-Ca2+ pumps and the remainder by crossbridges. We examined whether SR-Ca2+ pumps account for a larger proportion of the energy in the fastest vertebrate muscle known (the toadfish swimbladder), and whether the swimbladder muscle utilizes energy at the superfast rate one would predict from its mechanics. 2. The ATP utilization rates of the SR-Ca2+ pumps and crossbridges were measured using a coupled assay system on fibres skinned with saponin. Surprisingly, despite its superfast twitch speed, the ATP utilization rate of swimbladder was no higher than that of much slower fast-twitch amphibian muscles. 3. The swimbladder achieves tremendous twitch speeds with a modest steady-state ATP utilization rate by employing two mechanisms: having a small number of attached crossbridges and probably utilizing intracellular Ca2+ buffers (parvalbumin) to spread out the time over which Ca2+ pumping can occur. 4. Finally, although the total ATP utilization rate was not as rapid as expected, the relative proportions used by SR-Ca2+ pumps and the crossbridges were similar to other muscles.