Hydrodynamic stimulation of gastrulation in Nematostella early embryos: mechanotransduction mechanisms

The evolutionary emergence of the primitive gut in Metazoa is one of the decisive events that conditioned the major evolutionary transition having led to the origin of animal development. It is thought to have been induced by the specification of the endomesoderm into the multicellular tissue and its invagination (i.e. gastrulation). However, the biochemical signals underlying the evolutionary emergence of endomesoderm specification and gastrulation remain unknown.

We found that hydrodynamic mechanical strains, reminiscent of soft marine flow, trigger active tissue invagination/gastrulation or curvature reversal via a Myo-II-dependent mechanotransductive process in both the metazoan Nematostella vectensis (Cnidaria) and the multi-cellular choanoflagellate Choanoeca flexa. In the latter, our data suggest that the curvature reversal is associated to a sensory-behavioral feeding response.

Choanoflagellates are considered the closest living relative to metazoans, and the common ancestor of choanoflagellates and metazoans dates back at least 700 million years. Therefore, the present findings using these evolutionarily distant species suggest that the primitive emergence of the gut in Metazoa may have been initiated in response to marine mechanical stress already in multicellular pre-Metazoa.

The project is to characterize the molecular mechanism that underlies Myo-II mechanical activation, begeining with Nematostella.

1. Pouille, P. A., Ahmadi, P., Brunet, A. C. & Farge, E. Mechanical Signals Trigger Myosin II Redistribution and Mesoderm Invagination in Drosophila Embryos. Science signaling 2, ra16 (2009). https://doi.org:scisignal.2000098 [pii] 10.1126/scisignal.2000098
2. Mitrossilis, D. et al. Mechanotransductive cascade of Myo-II-dependent mesoderm and endoderm invaginations in embryo gastrulation. Nature communications 8, 13883 (2017). https://doi.org:10.1038/ncomms13883
3. Nguyen, N. M. et al. Mechano-biochemical marine stimulation of inversion, gastrulation, and endomesoderm specification in multicellular Eukaryota. Front Cell Dev Biol 10, 992371 (2022). https://doi.org:10.3389/fcell.2022.992371