Self-recognition and Ca2+-dependent carbohydrate–carbohydrate cell adhesion provide clues to the Cambrian explosion

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2009-07-17Author
Fernandez-Busquets, Xavier
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Kornig, Andre
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Bucior, Iwona
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Burger, Max M.
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Anselmetti, Dario
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https://hdl.handle.net/1912/3889As published
https://doi.org/10.1093/molbev/msp170Abstract
The Cambrian explosion of life was a relatively short period ca. 540 million years ago that
marked a generalized acceleration in the evolution of most animal phyla, but the trigger of this
key biological event remains elusive. Sponges are the oldest extant Precambrian metazoan
phylum and thus a valid model to study factors that could have unleashed the rise of multicellular
animals. One such factor is the advent of self/non-self recognition systems, which would be
evolutionarily beneficial to organisms to prevent germ cell parasitism or the introduction of
deleterious mutations resulting from fusion with genetically different individuals. However, the
molecules responsible for allorecognition probably evolved gradually before the Cambrian
period, and some other (external) factor remains to be identified as the missing triggering event.
Sponge cells associate through calcium-dependent, multivalent carbohydrate-carbohydrate
interactions of the g200 glycan found on extracellular proteoglycans. Single molecule force
spectroscopy analysis of g200-g200 binding indicates that calcium affects the lifetime (+Ca/-Ca:
680 s/3 s) and bond reaction length (+Ca/-Ca: 3.47 Å/2.27 Å). Calculation of mean g200
dissociation times in low and high calcium within the theoretical framework of a cooperative
binding model indicates the non-linear and divergent characteristics leading to either
disaggregated cells or stable multicellular assemblies, respectively. This fundamental
phenomenon can explain a switch from weak to strong adhesion between primitive metazoan
cells caused by the well documented rise in ocean calcium levels at the end of Precambrian time.
We propose that stronger cell adhesion allowed the integrity of genetically uniform animals
composed only of “self” cells, facilitating genetic constitutions to remain within the metazoan
individual and be passed down inheritance lines. The Cambrian explosion might have been
triggered by the coincidence in time of primitive animals endowed with self/non-self recognition,
and of a surge in sea water calcium that increased the binding forces between their calcium-dependent cell adhesion molecules.
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Author Posting. © The Authors, 2009. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Molecular Biology and Evolution 26 (2009): 2551-2561, doi:10.1093/molbev/msp170.
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Preprint: Fernandez-Busquets, Xavier, Kornig, Andre, Bucior, Iwona, Burger, Max M., Anselmetti, Dario, "Self-recognition and Ca2+-dependent carbohydrate–carbohydrate cell adhesion provide clues to the Cambrian explosion", 2009-07-17, https://doi.org/10.1093/molbev/msp170, https://hdl.handle.net/1912/3889Related items
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