Deepak Krishnamurthy

The principles of cascading power limits in small, fast biological and engineered systems

Hop, skip, jump, or massive leap In biological and engineered systems, an inherent trade-off exists between the force and velocity that can be delivered by a muscle, spring, or combination of the two. However, one can amplify the maximum throwing power of an arm by storing the energy in a bow or sling shot with a latch mechanism for sudden release. Ilton et al. used modeling to explore the performance of motor-driven versus spring-latch systems in engineering and biology across size scales. They found a range of general principles that are common to animals, plants, fungi, and machines that use elastic structures to maximize kinetic energy. Science, this issue p. eaao1082 Combining motors, springs, and latches offers many routes to optimization of mechanical power in biological and engineered systems. INTRODUCTION Mechanical power, whether for launched missiles or running humans, is limited by the universal, physical trade-off between force and velocity. However, many biological systems use power-amplifying mechanisms that enable unmatched accelerations in challenging environments and across a wide range of size scales. How these mechanisms actually enhance power output remains unclear. Power-amplified biological systems are of particular interest because they achieve a trio of combined capabilities that exceed current engineering performance: (i) high accelerations that (ii) can be continuously fueled through metabolic processes and (iii) are used repeatedly with minimal performance degradation throughout the life of the organism. Although engineers have struggled to design lightweight and long-lasting devices that can deliver high power output, biological systems have been performing such feats for millions of years and using these systems for a myriad of functions. RATIONALE Through a mathematical analysis that is equally applicable to biological and synthetic systems, we investigate how power enhancement emerges through the dynamic coupling of motors, springs, latches, and projectiles and relate the findings to data on existing biological and engineered systems. The model incorporates nonideal behavior of spring and latch systems in a scalable framework using both dimensional and dimensionless approaches. RESULTS Motors, springs, and latches all experience force-velocity trade-offs, and their integration exemplifies the cascading effects of power limits. Springs circumvent motor power limits when projectile mass is small and the motor’s force-velocity dynamics limit performance. However, springs also exhibit force-velocity trade-offs when their mass, mechanical properties, and time dependence are incorporated. Latches dynamically modulate spring power through variation in latch shape and velocity. Motor-driven and spring-driven movements are distinct in their transitions across performance (power, maximum velocity, and duration), which are largely dictated by projectile mass. When analyzed as a single, integrated system, the necessity for tuning and inherent tunability are evident. Simply increasing the force output of a motor does not enhance performance; the spring and latch capacities must also shift. Simply decreasing the size of the system also does not enhance performance; spring energy storage falls off at smaller scales due to the effects of materials, stiffness, and geometry. With this mathematical foundation of scaling and integration, we apply a new lens to patterns of biological scaling limits and propose new design principles for integrated and tuned systems. CONCLUSION Our model reveals a foundational framework for the scaling, synthetic design, and evolutionary diversification of power-amplified systems. The model enables a straightforward approach to analyzing biological systems, encourages a rich design space and functionality for synthetic systems, and highlights a compelling need for the integrative analysis of spring and latch dynamics in both synthetic and biological systems. Power-amplified biological and synthetic systems use spring elements to drive motion over a range of size scales. Mathematical modeling reveals a cascade of power limits and mass-dependent transitions in power delivery that arise from the integration of motors, springs, and latches to actuate movement. Variation of these components creates synergistic effects relevant to the analysis and synthesis of diverse power-amplified systems. Mechanical power limitations emerge from the physical trade-off between force and velocity. Many biological systems incorporate power-enhancing mechanisms enabling extraordinary accelerations at small sizes. We establish how power enhancement emerges through the dynamic coupling of motors, springs, and latches and reveal how each displays its own force-velocity behavior. We mathematically demonstrate a tunable performance space for spring-actuated movement that is applicable to biological and synthetic systems. Incorporating nonideal spring behavior and parameterizing latch dynamics allows the identification of critical transitions in mass and trade-offs in spring scaling, both of which offer explanations for long-observed scaling patterns in biological systems. This analysis defines the cascading challenges of power enhancement, explores their emergent effects in biological and engineered systems, and charts a pathway for higher-level analysis and synthesis of power-amplified systems.

Coupled active systems encode emergent behavioral dynamics of the unicellular predator Lacrymaria olor

Multiple active systems in a cell work together to produce sophisticated cellular behaviors such as motility and search. However, it is often unclear how this coupling specifies the complex emergent dynamics that define such behaviors. As a model system, we analyzed the hunting strategy of Lacrymaria olor, a unicellular predatory ciliate that uses extreme morphological changes to extend, contract and whip an apparent “cell neck” over many body lengths to capture prey. Tracking millions of unique subcellular morphologies over time revealed that these fast dynamics encode a comprehensive local search behavior apparent only at longer timescales. This hunting behavior emerges as a tug-of-war between active sub-cellular structures that use surface cilia and cortex contractility to deform the structure of the neck. The resulting search space can be described mathematically using a small number of normal shape modes that change amplitude rapidly during hunts. The distribution of these shape modes in space and time reveals a transition point between tense and compressed neck morphologies at the mean neck length, such that new shapes are readily sampled by repeatedly extending and retracting across this critical length. Molecular perturbations to the cell-signaling controller show that coupling between ciliary and contractile programs is needed to maintain this length/shape relationship; neither system alone provides the dynamic repertoire of shapes necessary for comprehensive search. Our results highlight the utility of coupling antagonistic active systems as a strategy for encoding or engineering complex behaviors in molecular machines. One Sentence Summary: Analysis of millions of unique cellular morphologies of the highly dynamic single-celled predator Lacrymaria olor reveals that it programs a comprehensive search space and emergent hunting behavior through coupling surface based active cilia and cortex based contractile molecular systems together.