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A tissue-engineered jellyfish with biomimetic propulsion

Abstract

Reverse engineering of biological form and function requires hierarchical design over several orders of space and time. Recent advances in the mechanistic understanding of biosynthetic compound materials1,2,3, computer-aided design approaches in molecular synthetic biology4,5 and traditional soft robotics6,7, and increasing aptitude in generating structural and chemical microenvironments that promote cellular self-organization8,9,10 have enhanced the ability to recapitulate such hierarchical architecture in engineered biological systems. Here we combined these capabilities in a systematic design strategy to reverse engineer a muscular pump. We report the construction of a freely swimming jellyfish from chemically dissociated rat tissue and silicone polymer as a proof of concept. The constructs, termed 'medusoids', were designed with computer simulations and experiments to match key determinants of jellyfish propulsion and feeding performance by quantitatively mimicking structural design, stroke kinematics and animal-fluid interactions. The combination of the engineering design algorithm with quantitative benchmarks of physiological performance suggests that our strategy is broadly applicable to reverse engineering of muscular organs or simple life forms that pump to survive.

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Acknowledgements

We acknowledge financial support from the Wyss Institute for Biologically Inspired Engineering at Harvard, the Harvard Materials Research Science and Engineering Center under National Science Foundation award number DMR-0213805, US National Institutes of Health grant 1 R01 HL079126 (K.K.P.), and from the office of Naval Research and National Science Foundation Program in Fluid Dynamics (J.O.D.). We acknowledge the Harvard Center for Nanoscale Science for use of facilities and the New England Aquarium for supplying jellyfish. We thank J. Goss, P.W. Alford, K.R. Sutherland, K. Balachandran, C. Regan, P. Campbell, S. Spina and A. Agarwal for comments and technical support.

Author information

Authors and Affiliations

Authors

Contributions

K.K.P., J.O.D. and J.C.N. conceived the project, designed the experiments and prepared the manuscript. J.O.D. and J.C.N. developed the fluid model. J.C.N. did the experiments and analyzed the data. H.L., A.W.F., C.M.R., M.L.M. and A.G. supervised experiments, analyzed data and gave conceptual advice. M.L.M. isolated rat cardiomyocytes for experiments.

Corresponding authors

Correspondence to John O Dabiri or Kevin Kit Parker.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Methods and Supplementary Figs. 1-8 (PDF 6118 kb)

Supplementary Movie 1

This movie shows the stroke cycle in a free-swimming juvenile Moon jellyfish (Aurelia aurita)consisting of muscle-powered contraction (power stroke) and elastic recoil (recovery stroke) (MOV 4232 kb)

Supplementary Movie 2

This movie shows the failure of a biomimetic Medusoid design to propel itself. The Medusoidconstruct was paced at 1 Hz through an externally applied monophasic square pulse (2.5V/cm,10ms duration). Due to mismatch of muscle stresses and substrate compliance, musclecontraction does not result in sufficient bell deformation, and no thrust is generated (MOV 1473 kb)

Supplementary Movie 3

This movie demonstrates jellyfish-like body contraction and free-swimming of optimallydesigned Medusoid constructs. Medusoids were paced at 1 Hz through an externally appliedmonophasic square pulse (2.5V/cm, 10ms duration). The first scene shows a mature constructstill attached at its center to its casting mold, just prior to release. (Note that the striatedappearance of the casting mold is caused by its fabrication process; in particular, this striationdoes not reflect the alignment of the muscle tissue on top of the silicone membrane covering themold). Subsequent scenes show exemplary propulsion of free-swimming Medusoids (MOV 5675 kb)

Supplementary Movie 4

This movie demonstrates comparative propulsion efficacy (distance per stroke) in jellyfish andoptimal Medusoids, whereas suboptimal Medusoids (“sieve design”) exhibit inferiorperformance. While Medusoids were paced at 1 Hz through an externally applied electric field of6 V, here the jellyfish contracts at a frequency of ca. 2 Hz. In order to facilitate comparison, theframe rate of the jellyfish recording was halved to synchronize stroke phases (MOV 2731 kb)

Supplementary Movie 5

This movie shows a sequence of raw DPIV data for jellyfish, Medusoid and suboptimally (=sieve-) designed Medusoids. Here, fluid flow around the jellyfish/Medusoid bell is visualized by the displacement of neutrally buoyant particles suspended within the fluid and illuminatedwithin a single plane using laser light. The relative motion of the particles allows quantifying 2Dfluid flow within the plane (MOV 2997 kb)

Supplementary Movie 6

This movie shows the fluid flow field and the vorticity field of a juvenile jellyfish during thestroke cycle. The movie was generated from DPIV data. The power stroke is characterized bymaximal fluid velocities and formation of a starting vortex, generating thrust. The recoverystroke is characterized by reduced fluid velocities and the formation of a stopping vortex,generating feeding currents towards the subumbrellar side (MOV 5745 kb)

Supplementary Movie 7

This movie shows the fluid flow field and the vorticity field of an optimally designed Medusoidduring the stroke cycle. The movie was generated from DPIV data. As in the jellyfish, the powerstroke generates maximal fluid velocities and a starting vortex ring, resulting in thrust. Therecovery stroke generates a stopping vortex ring that draws feeding currents towards the subumbrella (MOV 4993 kb)

Supplementary Movie 8

This movie shows the fluid flow field and the vorticity field of a suboptimal Medusoid design.The movie was generated from DPIV data. In contrast to jellyfish and optimal Medusoids,suboptimal Medusoids with “sieve design” fail to sufficiently accelerate fluid during the powerstroke, resulting in poor thrust generation. Vorticity patterns are more diffuse compared to thoseobserved in jellyfish and optimal designs, and further flow analysis revealed that generation offeeding currents was inferior as well (Fig. 4) (MOV 6131 kb)

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Nawroth, J., Lee, H., Feinberg, A. et al. A tissue-engineered jellyfish with biomimetic propulsion. Nat Biotechnol 30, 792–797 (2012). https://doi.org/10.1038/nbt.2269

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