Muscles contract when one protein molecule in a muscle fibre, myosin, pulls on another protein, actin, similar to a team of people pulling a chain (actin)hand over hand. But, the myosin arms can only bend at the elbow joint to achieve movement. To relax the muscle, the arms unbend and let go of the chain. Extraordinarily, some insects can contract and relax their flight muscles at a rate of 200 times per second, around 10 times faster than muscles in a similar sized non-flying insect. Because the muscles from most animals are incapable of such an Olympian performance, biologists are interested to know how insect flight muscles operate so quickly and what prevents them from operating at even higher speeds.

Douglas Swank, Vivek Vishnudas and David Maughan from the Rensselaer Polytechnic Institute, New York and the University of Vermont explore this question in a recent article using Drosophila melanogaster flight muscles. Muscles consume energy for contraction by breaking down adenosine triphosphate (ATP), which is bound to myosin in the presence of calcium, to adenosine diphosphate (ADP) and inorganic phosphate (Pi). This allows the myosin arms in a muscle fibre to bend and pull the actin chain,causing contraction. The concentration of ATP, ADP and Pi affect the speed of this chemical reaction, and hence contraction speed. Furthermore,Pi can bind to myosin, which prevents ATP binding and indirectly inhibits contraction.

The team already knew that flies with a mutation in their myosin, causing it to behave like a myosin found in slow twitch muscles, had flight muscles that couldn't contract or relax as fast. But, the length of pull for each myosin arm on the actin chain remained constant, suggesting that biochemical,not mechanical, factors were limiting contraction speed.

To investigate what these biochemical factors were, they manipulated the ATP and Pi concentrations in muscle fibres containing the slow myosin and fast flight muscle myosin and made two striking observations. First, fast flight muscle fibres needed a very high concentration of ATP to work and a 7-fold higher ATP concentration to contract by the same amount as slow fibres.

Second, Pi caused the two fibre types to respond differently to ATP. For example, the contraction frequency at which slow muscles achieved maximum force output increased as Pi concentration increased. In fast muscles, the maximum force output decreased as Piconcentration increased, and the contraction frequency producing this maximum force remained constant. This suggested that Pi wasn't competing with ATP for myosin binding sites in slow muscles. Fast muscle bound less ATP as Pi concentration increased, due to competition between the molecules for binding sites on the myosin. These results suggested that ATP affinity in flight muscle fibres is much lower than in slow muscle fibres and also that different biochemical factors were limiting contraction rates in the two fibre types. Using a model for biochemical reaction kinetics, the team confirmed that Pi release was indeed the rate-limiting factor of the high-frequency contractions of insect flight muscles.

Swank and colleagues reasoned that Drosophila could compensate for low ATP affinity by increasing intracellular ATP concentration in the fast muscles to promote ATP binding over Pi binding. They suggested that controlling ATP concentration could be a unique mechanism whereby Drosophila achieve an optimum balance between muscle contraction frequency and power production, since contraction frequency is dependent on ATP concentration. This enables insects to achieve superior muscle performance and ultimately overcome the energetic demands of aerial flight.

Swank, D. M., Vishnudas, V. K. and Maughan, D. W.(
). An exceptionally fast actomyosin reaction powers insect flight muscle.
Proc. Natl. Acad. Sci. USA