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Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability.

ABSTRACT: A surprising feature of animal locomotion is that organisms typically produce substantial forces in directions other than what is necessary to move the animal through its environment, such as perpendicular to, or counter to, the direction of travel. The effect of these forces has been difficult to observe because they are often mutually opposing and therefore cancel out. Indeed, it is likely that these forces do not contribute directly to movement but may serve an equally important role: to simplify and enhance the control of locomotion. To test this hypothesis, we examined a well-suited model system, the glass knifefish Eigenmannia virescens, which produces mutually opposing forces during a hovering behavior that is analogous to a hummingbird feeding from a moving flower. Our results and analyses, which include kinematic data from the fish, a mathematical model of its swimming dynamics, and experiments with a biomimetic robot, demonstrate that the production and differential control of mutually opposing forces is a strategy that generates passive stabilization while simultaneously enhancing maneuverability. Mutually opposing forces during locomotion are widespread across animal taxa, and these results indicate that such forces can eliminate the tradeoff between stability and maneuverability, thereby simplifying neural control.

SUBMITTER: Sefati S

PROVIDER: S-EPMC3839770 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability.

Sefati Shahin S Neveln Izaak D ID Roth Eatai E Mitchell Terence R T TR Snyder James B JB Maciver Malcolm A MA Fortune Eric S ES Cowan Noah J NJ

Proceedings of the National Academy of Sciences of the United States of America 20131104 47

A surprising feature of animal locomotion is that organisms typically produce substantial forces in directions other than what is necessary to move the animal through its environment, such as perpendicular to, or counter to, the direction of travel. The effect of these forces has been difficult to observe because they are often mutually opposing and therefore cancel out. Indeed, it is likely that these forces do not contribute directly to movement but may serve an equally important role: to simp ...[more]

PMID: 24191034

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Project description:Natural proteins often partake in several highly specific protein-protein interactions. They are thus subject to multiple opposing forces during evolutionary selection. To be functional, such multispecific proteins need to be stable in complex with each interaction partner, and, at the same time, to maintain affinity toward all partners. How is this multispecificity acquired through natural evolution? To answer this compelling question, we study a prototypical multispecific protein, calmodulin (CaM), which has evolved to interact with hundreds of target proteins. Starting from high-resolution structures of sixteen CaM-target complexes, we employ state-of-the-art computational methods to predict a hundred CaM sequences best suited for interaction with each individual CaM target. Then, we design CaM sequences most compatible with each possible combination of two, three, and all sixteen targets simultaneously, producing almost 70,000 low energy CaM sequences. By comparing these sequences and their energies, we gain insight into how nature has managed to find the compromise between the need for favorable interaction energies and the need for multispecificity. We observe that designing for more partners simultaneously yields CaM sequences that better match natural sequence profiles, thus emphasizing the importance of such strategies in nature. Furthermore, we show that the CaM binding interface can be nicely partitioned into positions that are critical for the affinity of all CaM-target complexes and those that are molded to provide interaction specificity. We reveal several basic categories of sequence-level tradeoffs that enable the compromise necessary for the promiscuity of this protein. We also thoroughly quantify the tradeoff between interaction energetics and multispecificity and find that facilitating seemingly competing interactions requires only a small deviation from optimal energies. We conclude that multispecific proteins have been subjected to a rigorous optimization process that has fine-tuned their sequences for interactions with a precise set of targets, thus conferring their multiple cellular functions.

Dataset Information

Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability.

Publications

Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability.

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