Volker Schmid

Evolution and Functional Diversity of Jellyfish Opsins

Cnidaria are the most basal animal phylum possessing complex eyes [1]. Their eyes predominantly use ciliary photoreceptor cells (c-PRCs) like vertebrates, whereas insect eyes use rhabdomeric photoreceptor cells (r-PRCs) [1-4]. These two cell types show not only different cytoarchitectures but distinct phototransduction cascades, which are triggered by the respective types of opsins (e.g., [5]), ciliary opsins (c-opsins) and rhabdomeric opsins (r-opsins) [6]. Recent reports suggested that the c- and r-PRCs and their respective opsins diverged at least before the deuterostome-protostome split [7-9]. To study the earlier evolution of animal PRCs and opsins, we investigated two hydrozoan jellyfishes. We report here the first-characterized cnidarian opsins. Molecular phylogeny revealed that the cloned 20 jellyfish opsins, together with all the opsins from a hydra and some from a sea anemone, are more closely related to the c-opsins than to any other major opsin subfamily, indicating that the divergence of c- and r-opsins antedates the Cnidaria-Bilateria split. Possible scenarios of animal PRC evolution are discussed. Furthermore, Cladonema opsins show several distinct tissue- and stage-specific expression patterns. The expression of specific opsins in the eyes suggests a role in vision, whereas that in the gonads suggests a role in light-controlled release of gametes.

Reversing the Life Cycle: Medusae Transforming into Polyps and Cell Transdifferentiation in Turritopsis nutricula (Cnidaria, Hydrozoa)

Organisms develop through a series of stages leading to sexually mature adults. In a few cases ontogeny reversal is possible, but it does not occur typically after the onset of sexual reproduction. All stages of the medusa Turritopsis nutricula, from newly liberated to fully mature individuals, can transform back into colonial hydroids, either directly or through a resting period, thus escaping death and achieving potential immortality. This is the first metazoan known to revert to a colonial, juvenile morph after having achieved sexual maturity in a solitary stage. Selective excision experiments show that the transformation of medusae into polyps occurs only if differentiated cells of the exumbrellar epidermis and part of the gastrovascular system are present, revealing a transformation potential unparalleled in the animal kingdom.

Isolated, mononucleated, striated muscle can undergo pluripotent transdifferentiation and form a complex regenerate

Isolated, mononucleated, cross-striated muscle of a medusa can be activated by collagenase treatment to transdifferentiate completely to various new cell types and to regenerate autonomously the sexual (without gametes) and feeding organ of the animal. Under these circumstances all isolated muscle fragments produce smooth muscle cells and a glandular cell type (y-cells). When culture conditions are appropriate, endoderm is also formed, followed by regeneration of a complex organ of seven or eight new non-muscle cell types, including nematocytes, digestive, secretory, gland, interstitial, and presumably nerve cells.

Evolutionary aspects of developmentally regulated helix-loop-helix transcription factors in striated muscle of jellyfish

The function of basic helix-loop-helix (bHLH) proteins in cell differentiation was shown to be conserved from Drosophila to vertebrates, exemplified by the function of MyoD in striated muscle differentiation. In phylogeny striated muscle tissue appears first in jellyfish and the question of its evolutionary position is controversially discussed. For this reason we have studied the developmental role of myogenic bHLH genes in medusa development. Based on their dimerization ability, four genes of the bHLH family of transcription factors were isolated from the hydrozoan jellyfish Podocoryne carnea. While the proteins Id and Ash group with cognate family members from bilaterians, Net-like and JellyD1 could not be unequivocally classified. Id is expressed during the medusa budding process and in the adult medusa, Ash and Net-like are expressed in all life cycle stages from egg to adult medusa and JellyD1 is expressed in the blastula and gastrula stages, the planula larva, and in late medusa bud stages. The dimerization specificity, the expression pattern, and the conservation of two residues specific for a MyoD bHLH domain suggest that JellyD1 is related to an ancestral MyoD gene. Id, Net-like, and JellyD1 are either expressed in the entocodon or its derived tissues, the striated and smooth muscle of the bell. These findings strengthen the hypothesis that the entocodon is a mesoderm-like structure and that the common ancestor of Cnidaria and Bilateria was more complex in cell-type architecture and body organization than commonly thought.

The cnidarian premises of metazoan evolution: From triploblasty, to coelom formation, to metamery

Abstract The hydromedusan subumbrellar muscle tissues originate from a mass of endo‐ and ectoderm derived cells proliferating inwardly. This mass of cells, called entocodon, is separated by the ecto‐and endoderm through a layer of extracellular matrix, thus forming a locally triploblastic arrangement of tissues. By cavitation and differentiation, the entocodon gives rise to the striated and smooth muscle layers of the subumbrella. The structure of the striated muscle is histologically identical to that described for triploblasts, where striated muscle is mainly mesodermic. Together with the mode of development, this suggests that not all Cnidaria are diploblastic and that the subumbrellar cavity is a coelom‐like structure. The subumbreHar cavity is formed late in ontogeny, whereas the coelom in higher animals is normally formed during embryonic development. Instead of remaining closed, the subumbrella becomes open, with the muscular mesothelium in contact with the environment. This view of cnidarian struc...

Transdifferentiation in medusae

Publisher Summary This chapter discusses the in vitro transdifferentiation system that is established using isolated medusa tissues of differentiated cells. Transdifferentiation can be defined as a switch (or reprogramming or rechanneling) of cells that have already expressed specific differentiated traits into another cell type distinguished from the original cells by a set of phenotypic characters. In all known cases of true transdifferentiation the newly acquired state is stable and a switch to the original cell type has never been reported. Medusae (jellyfish) belong to Cnidaria , a group of animals that lack a true mesoderm and are essentially classified as bilayered animals. They have two properties that have been of crucial importance for the establishment of an experimental transdifferentiation system: (1) many species are able to regenerate most of their body parts, and (2) the swimming organ (the umbrella or bell) is composed of three tissue layers, of which two consist of only one well-differentiated cell type. The transdifferentiation processes observed in medusa demonstrate that well-differentiated animal cells can retain the ability to change cellular commitment and to form various new cell types that can be organized into a functional regenerate.

Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea

We characterized a Pax gene from the hydrozoan Podocoryne carnea. It is most similar to cnidarian Pax-B genes and encodes a paired domain, a homeodomain and an octapeptide. Expression analysis demonstrates the presence of Pax-B transcripts in eggs, the ectoderm of the planula larva and in a few scattered cells in the apical polyp ectoderm. In developing and mature medusae, Pax-B is localized in particular endodermal cells, oriented toward the outside. Pax-B is not expressed in muscle cells. However, if isolated striated muscle tissue is activated for transdifferentiation, the gene is expressed within 1 h, before new cell types, such as smooth muscle and nerve cells, have formed. The expression data indicate that Pax-B is involved in nerve cell differentiation.

Ultrastructure of mechanoreceptors of the polyp Coryne pintneri (hydrozoa, athecata)☆

Abstract 1. 1. The ectoderm of the athecate hydroid polyps of Cladonema, Sarsia and Coryne contains long stereocilia, which act as mechanoreceptors. 2. 2. These stereocilia which are abundant on the filiform tentacles originate from an elongated ciliary cell which is situated within an accessory cell. 3. 3. The present paper describes the ultrastructure of this two-cell system, focusing on the architecture of the ciliary apparatus. 4. 4. The close resemblance between the structures of this ciliary apparatus and that of the nematocytes cnidocil is emphasized and discussed.

The HOX-like gene Cnox2-Pc is expressed at the anterior region in all life cycle stages of the jellyfish Podocoryne carnea

Abstract The marine jellyfish Podocoryne carnea (Cnidaria, Hydrozoa) has a metagenic life cycle consisting of a larva, a colonial polyp and a free-swimming jellyfish (medusa). To study the function of HOX genes in primitive diploblastic animals we screened a library of P. carnea cDNA using PCR primers derived from the most conserved regions in helix 1 and helix 3 of the homeobox. A novel gene, Cnox2-Pc, has been isolated and characterized. Cnox2-Pc is a HOX cluster-like gene, and its homeodomain shows similarity to the Deformed subfamily of HOM-C/HOX genes. In situ hybridization revealed that Cnox2-Pc is expressed in the anterior region of the larva, the polyp head, and the most apical ectoderm of the differentiating bud during medusa development. In adult medusa expression is restricted to the gastrovascular entoderm. The results suggest that Cnox2-Pc is involved in establishment of an anterior-posterior axis during development in primitive metazoans.

A TOXIN HOMOLOGY DOMAIN IN AN ASTACIN-LIKE METALLOPROTEINASE OF THE JELLYFISH PODOCORYNE CARNEA WITH A DUAL ROLE IN DIGESTION AND DEVELOPMENT

Abstract Metalloproteinases of the astacin family such as tolloid play major roles in animal morphogenesis. Cnidarians are thought to be evolutionary simple organisms and, therefore, a metalloproteinase from the marine hydrozoan Podocoryne carnea was analysed to evaluate the role of this conserved gene familiy at the base of animal evolution. Surprisingly, the proteinase domain of Podocornyne PMP1 is more similar to human meprin than to HMP1 from another hydrozoan, the freshwater polyp Hydra vulgaris. However, PMP1 and HMP1 both contain a small C-terminal domain with six cysteines that distinguishes them from other astacin-like molecules. Similar domains have been described only recently from sea anemone toxins specific for potassium channels. This toxin homology (Tox1) domain is clearly distinct from epidermal growth factor (EGF)-like domains or other cysteine-rich modules and terminates with the characteristic pattern CXXXCXXC with three out of six cysteines in the last eight residues of the protein. PMP1 is transiently expressed at various sites of morphogenetic activity during medusa bud development. In the adult medusa, however, expression is concentrated to the manubrium, the feeding organ, where the PMP1 gene is highly induced upon feeding. These disparate expression patterns suggest a dual role of PMP1 comparable to tolloid in development and, like astacin in the crayfish, also for food digestion. The Tox1 domain of PMP1 could serve as a toxin to keep the pray paralysed after ingestion, but as a sequence module such Tox1 domains with six cysteines are neither restricted to cnidarians nor to toxins.