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Self-repairing symmetry in jellyfish through mechanically driven reorganization

Abrams, Michael J. and Basinger, Ty and Yuan, William and Guo, Chin-Lin and Goentoro, Lea (2015) Self-repairing symmetry in jellyfish through mechanically driven reorganization. Proceedings of the National Academy of Sciences of the United States of America, 112 (26). E3365-E3373. ISSN 0027-8424. PMCID PMC4491739. https://resolver.caltech.edu/CaltechAUTHORS:20150615-145357610

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[img] Video (MPEG) (Movie S1. An Aurelia ephyra swimming in seawater. A 1-d-old ephyra. The movie is in real time) - Supplemental Material
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[img] Video (MPEG) (Movie S2. Symmetrization facilitates maturation into adult medusae. The medusae were filmed 4 wk after amputation. The movies are in real time. Part 1: Medusa growing from symmetrized pentamer. Part 2: An abnormal medusa from ephyrae that dontt symmetrize) - Supplemental Material
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[img] Video (MPEG) (Movie S3. Simulation of a tetramer symmetrizing using our mathematical model. Every cycle of contraction and elastic recoil generates a net push into the cut site. With every cycle, the ephyra relaxes into a new stable configuration where the arms go...) - Supplemental Material
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[img] Video (MPEG) (Movie S4. Frequency of muscle contraction dictates the speed of symmetrization. The movies are in real time. Part 1: Tetramer swimming in seawater. Part 2: Tetramer swimming in seawater with reduced MgCl2 (50% of the concentration in normal seawater)...) - Supplemental Material
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Abstract

What happens when an animal is injured and loses important structures? Some animals simply heal the wound, whereas others are able to regenerate lost parts. In this study, we report a previously unidentified strategy of self-repair, where moon jellyfish respond to injuries by reorganizing existing parts, and rebuilding essential body symmetry, without regenerating what is lost. Specifically, in response to arm amputation, the young jellyfish of Aurelia aurita rearrange their remaining arms, recenter their manubria, and rebuild their muscular networks, all completed within 12 hours to 4 days. We call this process symmetrization. We find that symmetrization is not driven by external cues, cell proliferation, cell death, and proceeded even when foreign arms were grafted on. Instead, we find that forces generated by the muscular network are essential. Inhibiting pulsation using muscle relaxants completely, and reversibly, blocked symmetrization. Furthermore, we observed that decreasing pulse frequency using muscle relaxants slowed symmetrization, whereas increasing pulse frequency by lowering the magnesium concentration in seawater accelerated symmetrization. A mathematical model that describes the compressive forces from the muscle contraction, within the context of the elastic response from the mesoglea and the ephyra geometry, can recapitulate the recovery of global symmetry. Thus, self-repair in Aurelia proceeds through the reorganization of existing parts, and is driven by forces generated by its own propulsion machinery. We find evidence for symmetrization across species of jellyfish (Chrysaora pacifica, Mastigias sp., and Cotylorhiza tuberculata).


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1502497112DOIArticle
http://www.pnas.org/content/112/26/E3365PublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1502497112/-/DCSupplementalPublisherSupporting Information
http://www.npr.org/2015/06/15/414050924/instead-of-replacing-missing-body-parts-moon-jellies-recycleFeatured InNPR: Science
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4491739/PubMed CentralArticle
ORCID:
AuthorORCID
Goentoro, Lea0000-0002-3904-0195
Additional Information:© 2015 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved May 7, 2015 (received for review February 6, 2015). Published online before print June 15, 2015, doi: 10.1073/pnas.1502497112. We thank the Cabrillo Marine Aquarium and Monterey Bay Aquarium for supplying jellyfish polyps, and especially K. Darrow and W. Patry for their advice on jellyfish nursery. We thank N. Andrew for critical comments that led us to conceiving the pulsation modulation experiment, J. Dabiri for discussions throughout the study, J. Nawroth for pointing us to cactus spines, and E. Meyerowitz for pointing out the importance of viscous ratchet. We thank M. Elowitz, B. Hay, J. H. Cho, C. Frick, H. Nunns, N. Olsman, J. T. Abrams, and B. G. Abrams for suggestions and comments on the manuscript. This work was supported by the National Science Foundation Graduate Research Fellowship Program (to M.J.A.). Author contributions: M.J.A., T.B., and L.G. designed research; M.J.A. and T.B. performed experiments; W.Y. performed the grafting experiments; M.J.A., C.-L.G., and L.G. designed the mathematical model; C.L.G. performed the mathematical modeling; M.J.A., T.B., and L.G. analyzed data; and M.J.A., T.B., and L.G. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1502497112/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipUNSPECIFIED
Subject Keywords:self-repair; reorganization; jellyfish; symmetry; propulsion
Issue or Number:26
PubMed Central ID:PMC4491739
Record Number:CaltechAUTHORS:20150615-145357610
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150615-145357610
Official Citation:Michael J. Abrams, Ty Basinger, William Yuan, Chin-Lin Guo, and Lea Goentoro Self-repairing symmetry in jellyfish through mechanically driven reorganization PNAS 2015 112 (26) E3365-E3373; published ahead of print June 15, 2015, doi:10.1073/pnas.1502497112
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:58262
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:15 Jun 2015 22:13
Last Modified:03 Oct 2019 08:34

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