Adhesion of freshwater sponge cells mediated by carbohydrate-carbohydrate interactions requires low environmental calcium

Eduardo Vilanova, Priscilla J. Ciodaro, Francisco F. Bezerra, Gustavo R.C. Santos, Juan J. Valle-Delgado, Dario Anselmetti, Xavier Fernàndez-Busquets*, Paulo A.S. Mourão*

*Corresponding author for this work

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Marine ancestors of freshwater sponges had to undergo a series of physiological adaptations to colonize harsh and heterogeneous limnic environments. Besides reduced salinity, river-lake systems also have calcium concentrations far lower than seawater. Cell adhesion in sponges is mediated by calcium-dependent multivalent self-interactions of sulfated polysaccharide components of membrane-bound proteoglycans named aggregation factors. Cells of marine sponges require seawater average calcium concentration (10 mM) to sustain adhesion promoted by aggregation factors. We demonstrate here that the freshwater sponge Spongilla alba can thrive in a calcium-poor aquatic environment and that their cells are able to aggregate and form primmorphs with calcium concentrations 40-fold lower than that required by marine sponges cells. We also find that their gemmules need calcium and other micronutrients to hatch and generate new sponges. The sulfated polysaccharide purified from S. alba has sulfate content and molecular size notably lower than those from marine sponges. Nuclear magnetic resonance analyses indicated that it is composed of a central backbone of non- and 2-sulfated α- and β-glucose units decorated with branches of α-glucose. Assessments with atomic force microscopy/single-molecule force spectroscopy show that S. alba glucan requires 10-fold less calcium than sulfated polysaccharides from marine sponges to self-interact efficiently. Such an ability to retain multicellular morphology with low environmental calcium must have been a crucial evolutionary step for freshwater sponges to successfully colonize inland waters.

Original languageEnglish
Pages (from-to)710-721
Number of pages12
JournalGLYCOBIOLOGY
Volume30
Issue number9
DOIs
Publication statusPublished - 20 Aug 2020
MoE publication typeA1 Journal article-refereed

Keywords

  • carbohydrate interactions
  • evolutionary adaptation
  • Porifera
  • proteoglycans
  • sulfated polysaccharides

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    Vilanova, E., Ciodaro, P. J., Bezerra, F. F., Santos, G. R. C., Valle-Delgado, J. J., Anselmetti, D., Fernàndez-Busquets, X., & Mourão, P. A. S. (2020). Adhesion of freshwater sponge cells mediated by carbohydrate-carbohydrate interactions requires low environmental calcium. GLYCOBIOLOGY, 30(9), 710-721. https://doi.org/10.1093/glycob/cwaa014