An exceptionally fast actomyosin reaction powers insect flight muscle.
Insects, as a group, have been remarkably successful in adapting to a great range of physical and biological environments, in large part because of their ability to fly. The evolution of flight in small insects was accompanied by striking adaptations of the thoracic musculature that enabled very high wing beat frequencies. At the cellular and protein filament level, a stretch activation mechanism evolved that allowed high-oscillatory work to be achieved at very high frequencies as contraction and nerve stimulus became asynchronous. At the molecular level, critical adaptations occurred within the motor protein myosin II, because its elementary interactions with actin set the speed of sarcomere contraction. Here, we show that the key myosin enzymatic adaptations required for powering the very fast flight muscles in the fruit fly Drosophila melanogaster include the highest measured detachment rate of myosin from actin (forward rate constant, 3,698 s(-1)), an exceptionally weak affinity of MgATP for myosin (association constant, 0.2 mM(-1)), and a unique rate-limiting step in the cross-bridge cycle at the point of inorganic phosphate release. The latter adaptations are constraints imposed by the overriding requirement for exceptionally fast release of the hydrolytic product MgADP. Otherwise, as in Drosophila embryonic muscle and other slow muscle types, a step associated with MgADP release limits muscle contraction speed by delaying the detachment of myosin from actin.
Swank
Douglas M
DM
Department of Biology and Center for Biotechnology, Rensselaer Polytechnic Institute, 110 Eighth Street, Troy, NY 12180, USA. swankd@rpi.edu
Vishnudas
Vivek K
VK
Maughan
David W
DW
D000205:Actomyosin / Q000378:metabolism*; D000818:Animals; D004331:Drosophila melanogaster / Q000502:physiology*; D005260:Female; D005426:Flight, Animal / Q000502:physiology*; D007700:Kinetics; D018482:Muscle, Skeletal / Q000378:metabolism*; D020033:Protein Isoforms / Q000378:metabolism; D011817:Rabbits; D013997:Time Factors
D020033:Protein Isoforms; D000205:Actomyosin