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Research Article
Differential tissue stiffness of body column facilitates locomotion of Hydra on solid substrates
Suyash Naik, Manu Unni, Devanshu Sinha, Shatruhan Singh Rajput, Puli Chandramouli Reddy, Elena Kartvelishvily, Inna Solomonov, Irit Sagi, Apratim Chatterji, Shivprasad Patil, Sanjeev Galande
Journal of Experimental Biology 2020 223: jeb232702 doi: 10.1242/jeb.232702 Published 29 October 2020
Suyash Naik
1Department of Biology, Indian Institute of Science Education and Research, Pune 411008, India
2Department of Physics, Indian Institute of Science Education and Research, Pune 411008, India
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  • ORCID record for Suyash Naik
Manu Unni
1Department of Biology, Indian Institute of Science Education and Research, Pune 411008, India
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Devanshu Sinha
2Department of Physics, Indian Institute of Science Education and Research, Pune 411008, India
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Shatruhan Singh Rajput
2Department of Physics, Indian Institute of Science Education and Research, Pune 411008, India
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Puli Chandramouli Reddy
1Department of Biology, Indian Institute of Science Education and Research, Pune 411008, India
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Elena Kartvelishvily
3Electron Microscopy Unit, Weizmann Institute of Science, Rehovot 7610001, Israel
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Inna Solomonov
4Department of Biological Regulation, Weizmann Institute of Science, Rehovot 7610001, Israel
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Irit Sagi
4Department of Biological Regulation, Weizmann Institute of Science, Rehovot 7610001, Israel
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Apratim Chatterji
2Department of Physics, Indian Institute of Science Education and Research, Pune 411008, India
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Shivprasad Patil
2Department of Physics, Indian Institute of Science Education and Research, Pune 411008, India
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  • For correspondence: sanjeev@iiserpune.ac.in s.patil@iiserpune.ac.in
Sanjeev Galande
1Department of Biology, Indian Institute of Science Education and Research, Pune 411008, India
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  • For correspondence: sanjeev@iiserpune.ac.in s.patil@iiserpune.ac.in
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ABSTRACT

The bell-shaped members of the Cnidaria typically move around by swimming, whereas the Hydra polyp can perform locomotion on solid substrates in an aquatic environment. To address the biomechanics of locomotion on rigid substrates, we studied the ‘somersaulting’ locomotion in Hydra. We applied atomic force microscopy to measure the local mechanical properties of Hydra's body column and identified the existence of differential Young's modulus between the shoulder region versus rest of the body column at 3:1 ratio. We show that somersaulting primarily depends on differential tissue stiffness of the body column and is explained by computational models that accurately recapitulate the mechanics involved in this process. We demonstrate that perturbation of the observed stiffness variation in the body column by modulating the extracellular matrix polymerization impairs the ‘somersault’ movement. These results provide a mechanistic basis for the evolutionary significance of differential extracellular matrix properties and tissue stiffness.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: S.A.N., M.K.U., P.R., I. Solomonov, A.C., S.P., S.G.; Methodology: S.A.N., M.K.U., D.S., S.S.R., E.K., S.P., S.G.; Software: D.S., A.C.; Validation: S.A.N., M.K.U., S.P., S.G.; Formal analysis: S.A.N., M.K.U., D.S.; Investigation: S.A.N., M.K.U.; Resources: E.K., I. Sagi, A.C., S.P., S.G.; Data curation: S.A.N., M.K.U., I. Solomonov, S.P., S.G.; Writing - original draft: S.A.N., M.K.U., A.C., S.P., S.G.; Writing - review & editing: S.A.N., M.K.U., P.R., A.C., S.P., S.G.; Visualization: S.A.N., M.K.U., D.S., E.K.; Supervision: I. Sagi, A.C., S.P., S.G.; Project administration: I. Sagi, S.P., S.G.; Funding acquisition: I. Sagi, S.G.

  • Funding

    This work was supported by the Centre of Excellence in Epigenetics program (BT/01/COE/09/07) of the Department of Biotechnology, Government of India and the JC Bose National Fellowship from the Science and Engineering Research Board (JCB/2019/000013) (S.G.). We used the computer cluster obtained using a grant from the Department of Biotechnology (BT/PR16542/BID/7/654/2016) to A.C. A.C. acknowledges funding by DST Nanomission, India, the Thematic Unit Program (SR/NM/TP-13/2016) and the Department of Science and Technology, India (MTR/2019/000078). The authors acknowledge funding from IISER Pune - intramural (D.S., S.S.R., S.G., S.P. and A.C.); Department of Biotechnology postdoctoral fellowship (PCR); the Wellcome Trust-Department of Biotechnology India Alliance for Intermediate Fellowship (500172/Z/09/Z) (S.P.) and Early Career Fellowship (IA/E/16/1/503057) (P.C.R.); Department of Science and Technology, India (SERB grant no. EMR/2015/000018; A.C.); fellowships from the University Grants Commission (UGC) (M.U.); EMBO Short-term fellowship and Infosys Foundation for international travel support (M.U.); and Kishore Vaigyanik Protsahan Yojana (KVPY) (S.N.).

  • Data availability

    Source data files are available from the Dryad Digital Repository (Naik et al., 2020): https://doi.org/10.5061/dryad.qbzkh18fx

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.232702.supplemental

  • Received July 6, 2020.
  • Accepted September 3, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Biomechanics
  • Extracellular matrix
  • Tissue rheology
  • Atomic force microscopy

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Research Article
Differential tissue stiffness of body column facilitates locomotion of Hydra on solid substrates
Suyash Naik, Manu Unni, Devanshu Sinha, Shatruhan Singh Rajput, Puli Chandramouli Reddy, Elena Kartvelishvily, Inna Solomonov, Irit Sagi, Apratim Chatterji, Shivprasad Patil, Sanjeev Galande
Journal of Experimental Biology 2020 223: jeb232702 doi: 10.1242/jeb.232702 Published 29 October 2020
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Research Article
Differential tissue stiffness of body column facilitates locomotion of Hydra on solid substrates
Suyash Naik, Manu Unni, Devanshu Sinha, Shatruhan Singh Rajput, Puli Chandramouli Reddy, Elena Kartvelishvily, Inna Solomonov, Irit Sagi, Apratim Chatterji, Shivprasad Patil, Sanjeev Galande
Journal of Experimental Biology 2020 223: jeb232702 doi: 10.1242/jeb.232702 Published 29 October 2020

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