Embryonic development of the moon jellyfishAurelia aurita(Cnidaria, Scyphozoa): another variant on the theme of invagination

Abstract

Background Aurelia aurita (Scyphozoa, Cnidaria) is an emblematic species of the jellyfish. Currently, it is an emerging model of Evo-Devo for studying evolution and molecular regulation of metazoans’ complex life cycle, early development, and cell differentiation. For Aurelia, the genome was sequenced, the molecular cascades involved in the life cycle transitions were characterized, and embryogenesis was studied on the level of gross morphology. As a reliable representative of the class Scyphozoa, Aurelia can be used for comparative analysis of embryonic development within Cnidaria and between Cnidaria and Bilateria. One of the intriguing questions that can be posed is whether the invagination occurring during gastrulation of different cnidarians relies on the same cellular mechanisms. To answer this question, a detailed study of the cellular mechanisms underlying the early development of Aurelia is required. Methods We studied the embryogenesis of A. aurita using the modern methods of light microscopy, immunocytochemistry, confocal laser microscopy, scanning and transmission electron microscopy. Results In this article, we report a comprehensive study of the early development of A. aurita from the White Sea population. We described in detail the embryonic development of A. aurita from early cleavage up to the planula larva. We focused mainly on the cell morphogenetic movements underlying gastrulation. The dynamics of cell shape changes and cell behavior during invagination of the archenteron (future endoderm) were characterized. That allowed comparing the gastrulation by invagination in two cnidarian species—scyphozoan A. aurita and anthozoan Nematostella vectensis. We described the successive stages of blastopore closure and found that segregation of the germ layers in A. aurita is linked to the ’healing’ of the blastopore lip. We followed the developmental origin of the planula body parts and characterized the planula cells’ ultrastructure. We also found that the planula endoderm consists of three morphologically distinct compartments along the oral-aboral axis. Conclusions Epithelial invagination is a fundamental morphogenetic movement that is believed as highly conserved across metazoans. Our data on the cell shaping and behaviours driving invagination in A. aurita contribute to understanding of morphologically similar morphogenesis in different animals. By comparative analysis, we clearly show that invagination may differ at the cellular level between cnidarian species belonging to different classes (Anthozoa and Scyphozoa). The number of cells involved in invagination, the dynamics of the shape of the archenteron cells, the stage of epithelial-mesenchymal transition that these cells can reach, and the fate of blastopore lip cells may vary greatly between species. These results help to gain insight into the evolution of morphogenesis within the Cnidaria and within Metazoa in general.

Postembryonic development and lifestyle shift in the commensal ribbon worm

“…4 D–I). The morphogenesis of the posterior sucker in M. japonica appeared similar to so-called “tissue invagination”, which is one of the fundamental mechanisms in the early development of metazoan body plans [ 31 , 32 ] and is commonly observed during gastrulation in invertebrates [ 31 – 33 ], including nemerteans [ 21 , 34 ]. Although the existence of a sucker primordium has been shown in Hammarstein’s illustrations ([ 18 ], Figs.…”

Neuromuscular development in the emerging scyphozoan model system, Cassiopea xamachana: implications for the evolution of cnidarian nervous systems

“…Some cnidarian planulae, however, do show functional muscles, e.g., the benthic larva of the hydroid Clava multicornis (Forsskål, 1775), which moves by lateral bending ( Piraino et al, 2011 ). The ectoderm of C. xamachana and other cnidarian planulae consists mostly of epithelio-muscular (supportive) cells ( Martin and Chia, 1982 ; Kraus et al, 2022 ). Body deformations in the larva-to-polyp transition are found to be driven by muscular hydraulics in the sea anemone Nematostella vectensis Stephenson, 1935 ( Stokkermans et al, 2022 ).…”

Cnidaria XIAP activates caspase-mediated cell death

“…The moon jellyfish Aurelia is an emblematic medusa in Cnidaria, with a complex life cycle like most medusozoans (Gold et al, 2019). Over twenty species of Aurelia have been recognized (Kraus, Osadchenko, & Kosevich, 2022;Lawley et al, 2021). Among them, A. coerulea and Aurelia aurita are invasive species widely distributed around the Northwest Pacific and Atlantic coast of Europe (Kraus et al, 2022).…”