Skip to main content

Advertisement

SpringerLink
Log in

Progression of regeneration in demosponge Cinachyrella cf cavernosa based on wound location

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In this study, the differential regeneration process in sponge Cinachyrella cf cavernosa (Lamarck, 1815) was examined by creating wounds at basal and apical tissues. The differences in wound healing were investigated based on qualitative and quantitative changes in collagen at both wound locations. The different cell types were also documented. The basal tissue was found to heal faster than apical tissue. Collagen was 21.74% more in regenerating basal tissue than the apical tissue, indicating its involvement in accelerated regeneration. To understand the molecular process of gene regulation during regeneration in basal tissues of C.cf cavernosa, transcriptomic analysis was carried out using Illumina NextSeq 500. From the samples used for RNA-seq, on an average, 35 million reads were obtained. Out of 65587 total Coding DNA Sequences (CDS), 37145 were annotated. The differential gene expression analysis showed upregulation in collagen-related gene Col and actin-related genes during progressive stages of regeneration. Contrary to other metabolism-related genes, lipid metabolism-related genes were expressed in more numbers with consecutive stages of regeneration highlighting their role in stress management of the sponge. This study serves to advance our understanding of the regeneration process, factors affecting the rate of this process and transcriptomic changes in regenerating sponge.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alexander, B. E., M. Achlatis, R. Osinga, H. G. van der Geest, J. P. M. Cleutjens, B. Schutte & J. M. de Goeij, 2015. Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage? PeerJ 3: e820.

    PubMed  PubMed Central  Google Scholar 

  • Andres, S. & W. Huber, 2010. Differential expression analysis for sequence count data. Genome Biology 11: R106, http://genomebiology.com/2010/11/10/R106

  • Ayling, A. L., 1983. Growth and regeneration rates in thinly encrusting demospongiae from temperate waters. The Biological Bulletin 165: 343–352.

    PubMed  Google Scholar 

  • Bennett, H., J. J. Bell, S. K. Davy, N. S. Webster & D. S. Francis, 2018. Elucidating the sponge stress response: lipids and fatty acids can facilitate survival under future climate scenarios. Global Change Biology 2(7): 3130–3144. .

    Google Scholar 

  • Bolger, A.M., M. Lohse & B. Usadel, 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics btu170.

  • Borisenko, I. E., M. Adamska, D.B. Tokina, & A.V. Ereskovsky, 2015. Transdifferentiation is a driving force of regeneration in Halisarca dujardini (Demospongiae, Porifera). PeerJ 3: e1211. 

  • Buchfink, B., C. Xie & D. H. Huson, 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods 12(1): 59–60.

    CAS  PubMed  Google Scholar 

  • Conaco, C., P. Neveu, H. Zhou, M. L. Arcila, S. M. Degnan, B. M. Degnan & K. S. Kosik, 2012. Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions. BMC Genomics 13: 209–228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coutinho, C.C., I. de Andrade Rosa, J.D. de Oliveira Teixeira, L.R. Andrade, M.L. Costa & C. Mermelstein, 2017. Cellular migration, transition and interaction during regeneration of the sponge Hymeniacidon heliophila. PLoS ONE12(5): e0178350.

  • Diehl-Seifert, B., B. Kurelec, R. K. Zahn, A. Dorn, B. Jericevic, G. Uhlenbruck & W. E. G. Muller, 1985. Attachment of sponge cells to collagen substrata: effect of a collagen assembly factor. Journal of Cell Science 79: 271–285.

    CAS  PubMed  Google Scholar 

  • Edgar, R., M. Domrachev & A. E. Lash, 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research 30(1): 207–210.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrlich, H., M. Wysokowski, S. Zółtowska-Aksamitowska, L. Petrenko & T. Jesionowski, 2018. Collagens of Poriferan Origin. Marine Drugs 16: 79.

    PubMed Central  Google Scholar 

  • Ereskovksy, A.V., I. Boriensko, A. Lavrov, F. Bolshakov, D. Tokina, M. Adamsky & M. Adamska, 2017a. Body plan formation during regeneration in sponges. presented in 4th International Congress on Invertebrate Morphology (ICIM4) 18 – 23 August 2017 Moscow, Russia.

  • Ereskovsky, A.V., D. J. Richter, D.V. Lavrov, K.J. Schippers & S.A. Nichols, 2017c. Transcriptome sequencing and delimitation of sympatric Oscarella species (O.carmela and O. pearsei sp. nov) from California, USA. PLoS ONE 12(9): e0183002.

  • Ereskovsky, A. V., I. E. Borisenko, P. Lapébie, E. Gazave, D. B. Tokina & C. Borchiellini, 2015. Oscarella lobularis (Homoscleromorpha, Porifera) Regeneration: Epithelial Morphogenesis and Metaplasia. PLoS One 10(8): e0134566.

    PubMed  PubMed Central  Google Scholar 

  • Ereskovsky, A. V., A. I. Lavrov, F. V. Bolshakov & D. B. Tokina, 2017a. Regeneration in White Sea sponge Leucosolenia complicata(Porifera, Calcarea). Invertebrate Zoology 14(2): 108–113.

    Google Scholar 

  • Ereskovsky, A. V., D. B. Tokina, D. M. Saidov, S. Baghduian, E. Le Goff & A. I. Lavrov, 2019. Transdifferentiation and mesenchymal-to-epithelial transition during regeneration in demospongiae (Porifera). Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. https://doi.org/10.1002/jez.b.22919.

    Article  Google Scholar 

  • Fortunato, S. A. V., M. Adamski, O. M. Ramos, S. Leininger, J. Liu, D. E. K. Ferrier & M. Adamska, 2014. Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514: 620–635.

    CAS  PubMed  Google Scholar 

  • Francis, W. R., M. Eitel, S. Vargas, M. Adamski, S. H. D. Haddock, S. Krebs, H. Blum, D. Erpenbeck & G. Woerheide, 2017. The genome of the contractile demosponge Tethya wilhelma and the evolution of metazoan neural signalling pathways. Biorxiv. https://doi.org/10.1101/120998.

    Article  Google Scholar 

  • Goetz, S., J. M. Garcia-Gomez, J. Terol, T. D. Williams, S. H. Nagaraj, M. J. Nueda, M. Robles, M. Talon, J. Dopazo & A. Conesa, 2008. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research 36(10): 3420–3435.

    Google Scholar 

  • Grabherr, M. G., B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, X. Adiconis, L. Fan, R. Raychowdhury, Q. Zeng, Z. Chen, E. Mauceli, N. Hacohen, A. Gnirke, N. Rhind, F. di Palma, B. W. Birren, C. Nusbaum, K. Lindblad-Toh, N. Friedman & A. Regev, 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29(7): 644–652.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grice, L. E. & B. M. Degnan, 2017. Transcriptomic profiling of the allorecognition response to grafting in the Demosponge Amphimedon queenslandica. Marine Drugs 15: 136–149.

    PubMed Central  Google Scholar 

  • Guzman, C. & C. Conaco, 2016. Gene expression dynamics accompanying the sponge thermal stress response. PLoS ONE 11(10): e0165368.

    PubMed  PubMed Central  Google Scholar 

  • Henry, L. & M. Hart, 2005. Regeneration from injury and resource allocation in sponges and corals – a review. International Review of Hydrobiology 90(2): 125–158.

    Google Scholar 

  • Hoppe, W. H., 1998. Growth, regeneration and predation in three species of large coral reef sponges. Marine Ecology Progress Series 50: 117–125.

    Google Scholar 

  • Howe, E. A., R. Sinha, D. Schlauch & J. Quackenbush, 2011. RNA-Seq analysis in MeV. Bioinformatics 27(22): 3209–3210.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kenny, N. J., J. M. de Goeij, D. M. de Bakker, C. G. Whalen, E. Berezikov & A. Riesgo, 2018. Towards the identification of ancestrally shared regenerative mechanisms across the Metazoa: A Transcriptomic case study in the Demosponge Halisarca caerulea. Marine Genomics 37: 135–147.

    PubMed  Google Scholar 

  • Larroux, C., B. Fahey, D. Liubicich, V. F. Hinman, M. Gauthier, M. Gongora, K. Green, G. Wörheide, S. P. Leys & B. Degnan, 2006. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evolution & Development 8(2): 150–173.

    CAS  Google Scholar 

  • Lavrov, A.I., F. V. Bolshakov, D.B. Tokina & A.V. Ereskovsky, 2018. Sewing wounds up: the epithelial morphogenesis as a central mechanism of calcaronean sponge regeneration. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 330: 351–371.

  • Lavrov, A. I. & I. A. Kosevich, 2014. Sponge cell reaggregation: Mechanisms and dynamics of the process. Russian Journal of Developmental Biology 45(4): 205–223.

    CAS  Google Scholar 

  • Lavrov, A. I. & I. A. Kosevich, 2016. Sponge cell reaggregation: Cellular structure and morphogenetic potencies of multicellular aggregates. Journal of Experimental Zoology: Part A Ecological Genetics & Physiology 325A: 158–177.

    Google Scholar 

  • Li, B. & C. N. Dewey, 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, W. & A. Godzik, 2006. CD-HIT: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659.

    CAS  PubMed  Google Scholar 

  • Moriya, Y., M. Itoh, S. Okuda, A. C. Yoshizawa & M. Kanehisa, 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35: W182–W185. .

    PubMed  PubMed Central  Google Scholar 

  • Nichols, S.A., B.W. Roberts, D.J. Richter, S.R. Fairclough & N. King, 2012. Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex. Proceedings of the National Academy of Sciences 109(32): 13046–13051.

  • Pawlik, J. R., T.-L. Loh & S. E. McMurray, 2017. A review of bottom-up vs top-down control of sponges on Caribbean fore-reefs: what’s old, what’s new, and future directions. PeerJ 6: e4343.

    Google Scholar 

  • Perez-Porro, A. R., D. Navarro-Gomez, M. J. Uriz & G. Giribet, 2013. A NGS approach to the encrusting Mediterranean sponge Crella elegans (Porifera, Demospongiae, Poecilosclerida): transcriptome sequencing, characterization and overview of the gene expression along three life cycle stages. Molecular Ecology Resources 13: 494–509.

    CAS  PubMed  Google Scholar 

  • Pozzolini, M., L. Gallus, S. Ghignone, S. Ferrando, S. Candiani, M. Bozzo, M. Bortolino, G. Costa, G. Bravestello & S. Scarfi (2019) Insights into the metazoan regenerative mechanisms: roles of TGF superfamily members in tissue regeneration of the marine sponge Chondrosia reniformis. Journal of Experimental Biology 222: jeb207894.

  • Puchtler, H., F. S. Waldrop & L. S. Valentine, 1973. Polarization microscopic studies of connective tissue stained with Picro-Sirius Red FBA. Beitrage zur Pathologie 150: 174–187.

    CAS  PubMed  Google Scholar 

  • Qiu, F., S. Ding, H. Ou, D. Wang, J. Chen & M. M. Miyamoto, 2015. Transcriptome changes during the life cycle of the Red sea sponge, Mycale phyllophila (Porifera, Demospongiae, Poecilosclerida). Genes 6: 1023–1052.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raine-Fenning, N. J., M. P. Brincat & Y. Muscat-Baron, 2003. Skin ageing and menopause: implications for treatment. American Journal of Clinical Dermatology 4(6): 371–378.

    PubMed  Google Scholar 

  • Reiswig, H. M., 1973. Population dynamics of three Jamaican Demospongiae. Bulletin of Marine Science 23(2): 191–226.

    Google Scholar 

  • Renard, E., S. P. Leys, G. Wörheide & C. Borchiellini, 2018. Understanding animal evolution: the added value of sponge transcriptomics and genomics. BioEssays 40(9): e1700237.

    PubMed  Google Scholar 

  • Responte, D. J., R. M. Natoli & K. A. Athanasiou, 2007. Collagens of articular cartilage: structure, function, and importance in tissue engineering. Biomedical Engineering 35(5): 363–411.

    Google Scholar 

  • Riesgo, A., S. C. S. Andrade, P. P. Sharma, M. Novo, A. R. Perez-Porro, V. Vahtera, V. L. Gonzalez, G. Y. Kawauchi & G. Giribet, 2012. Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Frontiers in Zoology 9: 33–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riesgo, A., N. Farrar, P. J. Windsor, G. Giribet & S. P. Leys, 2014a. The analysis of eight transcriptomes from all Poriferan classes reveals surprising genetic complexity in sponges. Molecular Biology and Evolution 31(5): 1102–1120.

    CAS  PubMed  Google Scholar 

  • Riesgo, A., K. Peterson, C. Richardson, T. Heist, B. Strehlow, M. McCauley, M. Hill & A. Hill, 2014b. Transcriptomic analysis of differential host gene expression upon uptake of symbionts: a case study with Symbiodinium and the major bioeroding sponge Cliona varians. BMC Genomics 15: 376–398.

    PubMed  PubMed Central  Google Scholar 

  • Schmahl, G. P., 1999. Recovery and growth of the giant barrel sponge (Xestospongia muta) following physical injury from a vessel grounding in the Florida Keys. Memoires of Queensland Museum 44: 532–532.

    Google Scholar 

  • Shield, C. J. & J. D. Witman, 1993. The impact of Henricia sanguinolenta(O.F. Mu¨ller) (Echinodermata:Asteroidea) predation on the finger sponges, Isodictya spp. Journal of Experimental Marine Biology & Ecology 166: 107–133.

    Google Scholar 

  • Simpson, T. L., 1984. The cell biology of sponges. Springer-Verlag, New York Inc.

    Google Scholar 

  • Singh, A. & N. L. Thakur, 2016. Influence of spatial competitor on the growth and regeneration of the marine sponge Cinachyrella cf. cavernosa (Porifera, Demospongiae). Hydrobiologia 768: 111–123.

    CAS  Google Scholar 

  • Srivastava, M., O. Simakov, J. Chapman, B. Fahey, M. E. A. Gauthier, T. Mitros, G. S. Richards, C. Conaco, M. Dacre, U. Hellsten, C. Larroux, N. H. Putnam, M. Stanke, M. Adamska, A. Darling, S. M. Degnan, T. H. Oakley, D. C. Plachetzki, Y. Zhai, M. Adamski, A. Calcino, S. F. Cummins, D. M. Goodstein, C. Harris, D. J. Jackson, S. P. Leys, S. Shu, B. J. Woodcroft, M. Vervoort, K. S. Kosik, G. Manning, B. M. Degnan & D. S. Rokhsar, 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720–728.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swatschek, D., W. Schatton, J. Kellermann, W. E. G. Mueller & J. Kreuter, 2002. Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. European Journal of Pharmaceutics & Biopharmaceutics 53: 107–113.

    CAS  Google Scholar 

  • Van Soest, R. W. M., N. Boury-Esnault, J. Vacelet, M. Dohrmann, D. Erpenbeck, N. J. De Voogd, N. Santodomingo, B. Vanhoorne, M. Kelly & J. N. A. Hooper, 2012. Global diversity of sponges (Porifera). PLoS ONE 7(4): e35105.

    PubMed  PubMed Central  Google Scholar 

  • Voigt, O., M. Adamaska, M. Adamaski, A. Kittlemann, W. Lukardis & G. Wörheide, 2017. Spicule formation in calcareous sponges: coordinated expression of biomineralization genes and spicule-type specific genes. Scientific Reports 7: 45658–45668.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. ISBN 978-3-319-24277-4.

    Google Scholar 

  • Wilkinson, C.R. & J.E. Thompson, 1997. Experimental sponge transplantation provides information on reproduction by fragmentation. In Proceedings of the 8th International Coral Reef Symposium, Vol. 2. Panama: Smithsonian Tropical Research Institute. pp. 1417–20.

  • Wulff, J. L., 2006. Resistance vs recovery: morphological strategies of coral reef sponges. Functional Ecology 20: 699–708.

    Google Scholar 

  • Wulff, J., 2010. Regeneration of sponges in ecological context: is regeneration an integral part of life history and morphological strategies? Integrative and Comparative Biology 50(4): 494–505.

    PubMed  Google Scholar 

Download references

Acknowledgements

Authors thank the Director, CSIR-NIO for providing infrastructure facilities. We thank Dr Abhishek Saha for providing a polarised light microscope, Mr Azraj Dahihande for invaluable help in sample collection and laboratory experiments, and Mr Shriraj Jakhalekar for identification of cell types. We would also like to thank Dr Nagendra Singh of the National Centre for Biological Sciences and CCAMP for making TEM facility available. A.D. thanks Council of Scientific and Industrial Research for a research fellowship. Both authors acknowledge and appreciate the comments given by anonymous reviewers. This work was partially supported by Council of Scientific and Industrial Research funded project ‘Ocean Finder’ (PSC0105) and is NIO contribution 6530.

Author information

Authors and Affiliations

  1. CSIR-National Institute of Oceanography, Dona Paula, 403004, Goa, India

    Aabha Deshpande & Narsinh L. Thakur

  2. Academy of Scientific and Innovative Research, Chennai, India

    Aabha Deshpande & Narsinh L. Thakur

Authors
  1. Aabha Deshpande
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Narsinh L. Thakur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Narsinh L. Thakur.

Additional information

Handling editor: Diego Fontaneto.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 120 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deshpande, A., Thakur, N.L. Progression of regeneration in demosponge Cinachyrella cf cavernosa based on wound location. Hydrobiologia 847, 2555–2571 (2020). https://doi.org/10.1007/s10750-020-04274-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04274-2

Keywords

Search

Navigation