On some features of embryonic development and metamorphosis of Aurelia aurita (Cnidaria, Scyphozoa)

Aurelia aurita is a cosmopolite species of scyphomedusae. Its anatomy and life cycle are well investigated. This work provides a detailed study on development and structure of A. aurita planula before and during its metamorphosis. Intravital observations and histology study during the settlement and metamorphosis of the planulae demonstrated that the inner manubrium lining of primary polyp (gastroderm) develops from the ectoderm of the planula posterior end. The spatial and temporal dynamics of serotonergic cells from the early embryonic stages until the formation of the primary polyp were studied for the first time. In addition, the distribution of tyrosinated tubulin and neuropeptide RF-amide at different stages of A. aurita development was traced.     

Ultrastructure of the neuromuscular system of the polyp of Aurelia aurita L., 1758 (Cnidaria,scyphozoa)

Fine structural study indicates that the neuromuscular system of stage I polyps of Aurelia aurita is exclusively ectodermal. The three major muscle fields are the radial muscles of the oral disc, the longitudinal muscles of the tentacles, and the muscle cords of the septae and the column; the muscle fields are in physical continuity at the peristomial pits and share a common innervation and type of myofibril. The myofibril is striated in the tentacle base, in the outer oral disc, and in the upper part of the muscle cord; it grades into a smooth muscle toward the tentacle tip, the mouth, and the lower part of the cord. There is a fourth field of longitudinal smooth muscle in the pharynx. The nervous system consists of an epithelial sensory cell in the tentacle and a single type of neuron found in the subepithelial layer of the tentacle, oral disc, and muscle cord. The lack of gap junctions suggests that there is no nonnervous conduction system. The subepithelial layer also contains three types of fibers and a type of soma which cannot be characterized as neuronal. The soma is identified as the “neurosecretory cell” described in Chrysaora. The absence of neuromuscular elements in the column and stolon distinguishes the Aurelia aurita collected from Washington, USA, from English polyps previously described.     

Induction of segmentation in polyps of Aurelia aurita (Scyphozoa, Cnidaria) into medusae and formation of mirror-image medusa anlagen

Polyps of Aurelia aurita can transform into several medusae (jellyfish) in a process of sequential subdivision. During this transformation, two processes take place which are well known to play a key role in the formation of various higher metazoa: segmentation and metamorphosis. In order to compare these processes in bilaterians and cnidarians we studied the control and the kinetics of these processes in Aurelia aurita. Segmentation and metamorphosis visibly start at the polyp's head and proceed down the body column but do not reach the basal disc. The small piece of polyp which remains will develop into a new polyp. The commitment to the medusa stage moves down the body column and precedes the visible onset of segmentation by about one day. Segmentation and metamorphosis can start at the cut surface of transversely cut body columns, leading to a mirror-image pattern of sequentially developing medusae.     

Morphodynamics of the contract plate in the course of oocyte maturation in the scyphozoan Aurelia aurita (Cnidaria: Semaeostomae)

The structure forming in the area of contact between the oocyte and the germinal epithelium in the course of oocyte maturation of the scyphozoan Aurelia aurita is termed the contact plate. This study traces the successive stages of contact plate formation in the course of oocyte maturation at the light microscopic and ultrastructural levels. At early stages ofoocyte development, the appearance of granules is observed in the peripheral cytoplasm of the oocyte; these granules accumulate at the pole, which retains its connection with the germinal epithelium of the gonads. Two types of these granules are recognized: (1) granules with homogeneous content and (2) granules containing loose shapeless material in the form of thick cords. The transformation of type two granules into larger structures, as well as the consolidation of type one and type two granules at later stages of oocyte development, are probably the processes that lead to the formation of the characteristic structure and contact plate, visible in paraffin and semithin sections. It remains unclear where exactly the contact plate is localized at the moment of fertilization: inside or outside the oocyte. The content of granules and components of the plate specifically bind the antibodies (RA47) against mesoglein, the ZP domain-containing protein of the mesoglea of A. aurita. The contact plate, covering only the anomalous pole of the oocyte but detected by the presence of ZP domain-containing proteins, may prove to be the simplest egg membrane of the zona pellucida type.     

Heat shock proteins in Aurelia (Cnidaria, Scyphozoa)

Heat shock proteins (hsp) in Aurelia identified by one-dimensional SDS-PAGE are of sizes 93,83,70,68,45, and 39 kD, the most rapidly labeled being hsp 70 in all developmental stages. Labeled hsp in the polyp are found mostly in the epidermis; gastrodermal nuclei are also labeled. The minimum temperature for induction of the proteins is about the same (27 degrees to 28 degrees C), regardless of whether polyps have been cultured at 15 degrees or 24 degrees C. Adults and planulae taken from natural water at 28 degrees C do not show accumulation of hsp 70. Induction of strobilation by raising polyps from 15 degrees to 25 degrees C is not associated with appreciable labeling of hsp. Polyps transferred to higher or lower salinity have decreased protein synthesis but do not synthesize stress proteins.     

Systematics and biogeography of the jellyfish Aurelia labiata (Cnidaria: Scyphozoa)

The hypothesis that the common eastern North Pacific Aurelia is A. aurita is falsified with morphological analysis. The name Aurelia labiata is resurrected, and the species is redescribed, to refer to medusae differing from A. aurita by a suite of characters related to a broad and elongated manubrium. Specifically, the oral arms are short, separated by and arising from the base of the fleshy manubrium, and the planulae are brooded upon the manubrium itself, rather than on the oral arms. Aurelia aurita possesses no corresponding enlarged structure. Furthermore, the number of radial canals is typically much greater in A. labiata, and thus the canals often appear more anastomosed than in A. aurita. Finally, most A. labiata medusae possess a 16-scalloped bell margin, whereas the margin is 8-scalloped in most A. aurita. Separation of the two forms has previously been noted on the basis of allozyme and isozyme analyses and on the histology of the neuromuscular system. Partial 18S rDNA sequencing corroborates these findings. Three distinct morphotypes of A. labiata, corresponding to separate marine bioprovinces, have been identified among 17 populations from San Diego, California, to Prince William Sound, Alaska. The long-undisputed species A. limbata may be simply a color morph of A. labiata, or a species within a yet-unelaborated A. labiata species complex. The first known introduction of Aurelia cf. aurita into southern California waters is documented. Although traditional jellyfish taxonomy tends to recognize many species as cosmopolitan or nearly so, these results indicate that coastal species, such as A. labiata, may experience rapid divergence among isolated populations, and that the taxonomy of such species should therefore be scrutinized with special care.     

Life Cycle Reversal in Aurelia sp.1 (Cnidaria,Scyphozoa)

The genus Aurelia is one of the major contributors to jellyfish blooms in coastal waters, possibly due in part to hydroclimatic and anthropogenic causes, as well as their highly adaptive reproductive traits. Despite the wide plasticity of cnidarian life cycles, especially those recognized in certain Hydroza species, the known modifications of Aurelia life history were mostly restricted to its polyp stage. In this study, we document the formation of polyps directly from the ectoderm of degenerating juvenile medusae, cell masses from medusa tissue fragments, and subumbrella of living medusae. This is the first evidence for back-transformation of sexually mature medusae into polyps in Aurelia sp.1. The resulting reconstruction of the schematic life cycle of Aurelia reveals the underestimated potential of life cycle reversal in scyphozoan medusae, with possible implications for biological and ecological studies.     

On natural metamorphosis inducers of the cnidarians Hydractinia echinata (Hydrozoa) and Aurelia aurita (Scyphozoa)

 Hydractinia echinata and Aurelia aurita produce motile larvae which undergo metamorphosis to sessile polyps when induced by external cues. The polyps are found at restricted sites, A. aurita predominantly on rocks close to the shore, H. echinata on shells inhabited by hermit crabs. It has been argued that the differential distribution of the polyps in their natural environment largely reflects the distribution of the natural metamorphosis-inducing cues. In the case of H. echinata, bacteria of the genus Alteromonas were argued to meet these conditions. We found that almost all substrates collected in the littoral to induce metamorphosis in H. echinata, and several bacterial strains isolated from the sea, including the common E. coli, induce metamorphosis efficiently. In A. aurita metamorphosis may be induced by the water–air interface, whereby metamorphosis precedes (final) settlement. Received: 7 December 1998 / Accepted: 8 July 1999     

Bacterially induced stolon settlement in the scyphopolyp ofAurelia aurita (Cnidaria,Scyphozoa)

Unsettled stoloniferous scyphopolyps ofAurelia aurita Lamarck were offered different substrates for settlement under defined conditions. On addition of different biogenic and abiotic substrates, a pure strain of bacteria, a species of Micrococcaceae, was observed to trigger the settlement of the stolon. The settlement reaction only takes place following direct contact with the bacteria; sterile filtrated culture medium of the same bacterial strain was not able to induce settlement. The bacteria were found to be effective on stolon settlement during the logarithmic growth phase, but not during the stationary phase.     

Development time of planula larvae on the oral arms of the scyphomedusa Aurelia aurita

The development time from zygote to late stage of planula larvaeon the oral arms of Aurelia aurita was found to be 270 and 170h at 12 and 22°C, respectively. The mean ratio of the diameterof the long axis to the short axis in newly released planulaewas 2.27.     

Metabolism of 131I in relation to strobilation of Aurelia aurita L. (Scyphozoa)

The ¹³¹I isotope of iodine has been used to follow the uptake and metabolism of iodine during the process of strobilation in pre-conditioned polyps of Aurelia aurita L. Strobilating polyps accumulated free iodide from the media against a concentration gradient, the segmented portion of the polyps accumulating about three times as much as the basal portion. Almost all of the accumulated iodide appeared in the soluble portion of an acid-ethanol extract of polyp tissue as inorganic iodide. The time course of accumulation of iodine was not affected by previous exposure to either higher temperature or iodide. Inorganic iodide rather than organically bound iodine is thought to be the effective factor in the initiation of strobilation.     

Protein composition of mesoglea and mesogloeal cells of medusa Aurelia aurita

Protein composition of mesoglea of the scyphomedusa Aurelia aurita was revealed in SDS-PAGE. Some major bands are visible in mesoglea of a mature medusa: 30, 45-47, 85 kDa, three bands between 100-200 kDa, and several bands with molecular weights > 300 kDa. Polyclonal antisera RA45/47 against protein 45 kDa were raised. RA45/47 react with 45-47 kDa protein in mesogleal sample and protein 120 kDa in mesogleal cells on immunoblot. Immunohistochemical analysis of A. aurita histological sections of young and mature medusae showed antigen localization in mesogleal cell granules and in the apical part of ectodermal cells. In mature medusae, the antigen was localized also in elastic fibers. We can conclude that in A. aurita mesogleal cells, along with ectodermal cells, take part in the formation of extracellular matrix of mesoglea.     

Structure and Function of Glycosylated Tandem Repeats from Candida albicans Als Adhesins

Tandem repeat (TR) regions are common in yeast adhesins, but their structures are unknown, and their activities are poorly understood. TR regions in Candida albicans Als proteins are conserved glycosylated 36-residue sequences with cell-cell aggregation activity (J. M. Rauceo, R. De Armond, H. Otoo, P. C. Kahn, S. A. Klotz, N. K. Gaur, and P. N. Lipke, Eukaryot. Cell 5:1664–1673, 2006). Ab initio modeling with either Rosetta or LINUS generated consistent structures of three-stranded antiparallel β-sheet domains, whereas randomly shuffled sequences with the same composition generated various structures with consistently higher energies. O- and N-glycosylation patterns showed that each TR domain had exposed hydrophobic surfaces surrounded by glycosylation sites. These structures are consistent with domain dimensions and stability measurements by atomic force microscopy (D. Alsteen, V. Dupres, S. A. Klotz, N. K. Gaur, P. N. Lipke, and Y. F. Dufrene, ACS Nano 3:1677–1682, 2009) and with circular dichroism determination of secondary structure and thermal stability. Functional assays showed that the hydrophobic surfaces of TR domains supported binding to polystyrene surfaces and other TR domains, leading to nonsaturable homophilic binding. The domain structures are like “classic” subunit interaction surfaces and can explain previously observed patterns of promiscuous interactions between TR domains in any Als proteins or between TR domains and surfaces of other proteins. Together, the modeling techniques and the supporting data lead to an approach that relates structure and function in many kinds of repeat domains in fungal adhesins.Yeast adhesins are a diverse set of cell adhesion proteins that mediate adhesion to host cells, environmental substrates, other fungi, and coinfecting bacteria (6, 8, 20, 21, 23, 29). The adhesins share common features, including compact N-terminal domains similar to Ig or lectin domains, Thr-rich midpieces, often in tandem repeats, and long highly glycosylated Ser/Thr-rich C-terminal regions that extend the functional domains out from the cell surface. No structures for the Thr-rich midpieces are known, but they can mediate aggregation of fungal cells (33, 35, 47). The prevalence and conservation of such repeats argue that they are functionally important, despite limited data on their structure and function.In Candida albicans, the Als adhesins are homologous proteins, products of 8 loci that encode numerous alleles of cell surface adhesins (16). In each mature Als protein, there are, from the N terminus, three tandem Ig-like domains, a β-sheet-rich conserved 127-residue amyloid-forming T region, a variable number of 36-residue tandem repeats (TRs), and a highly glycosylated stalk region that extends the N-terminal domains away from the cell surface (Fig. 1) (16, 33, 41). The C termini of these and other wall-associated adhesins are covalently cross-linked into the cell wall through transglycosylation of a modified glycosylphosphatidylinositol (GPI) anchor (18, 25). This modular design, including tandem repeats, is typical of fungal adhesins (8).Open in a separate windowFig. 1.Schematic diagram of the sequence of Als5p. The regions are named above, and the number of amino acid residues in each region is shown below. The modeled sequences are in the TR region.The Als protein Ig-like region, T region, and TR region all have protein-protein interaction activities (26, 33, 35). The Ig-like regions can interact with diverse mammalian proteins, presumably in a way analogous to antibody-antigen binding, as has been shown in the homologous protein α-agglutinin from Saccharomyces cerevisiae (8, 24, 26, 35). The T regions interact through formation of amyloid-like structures both in vivo and in vitro (33, 34a, 36). An insight into the function of the tandem repeats followed from observations that Als proteins initiate and maintain cell-to-cell aggregations, either spontaneously (“autoaggregation”) or following adhesion to a bead-bound defined ligand (10, 11, 36). Aggregation is more extensive for Als proteins with more tandem repeats (26, 35). This result suggested that the tandem repeats are uniquely structured to facilitate or mediate the aggregative function. Circular dichroism spectroscopy of the TR region of Als5p shows a β-sheet-rich structure in the soluble protein (35).In support of their direct involvement in aggregation, the repeat region of the C. albicans adhesin Als5p mediates cell-cell aggregation in the absence of the Ig-like and T domains (35). Moreover, the repeats can also potentiate binding of Als5p to fibronectin (35). Thus, the TR domains mediate cellular aggregation and increased binding to fibronectin. In addition, TR domains and their amino acid sequences are highly conserved across several Candida species (3). These properties need to be explained by their three-dimensional structure.Because there are no homologous structures known, we modeled by two independent ab initio methods. Rosetta assembles structures by combining short peptide structures extracted from the protein structural database PDB (38), then combines structures in a Monte Carlo approach, and assesses energetics of assembled structures. Rosetta has recently been shown to generate accurate models for protein-sized domains (40). We also predicted structures with LINUS, which generates randomized structures and rapidly estimates energetics to choose low-energy models (45). The models were supported by structural analyses with atomic force microscopy and circular dichroism spectroscopy. Functional assays showed that the TR domains can mediate binding activities predicted from the calculated structures.     

A newly discovered oxidant defence system and its involvement in the development of Aurelia aurita (Scyphozoa, Cnidaria): reactive oxygen species and elemental iodine control medusa formation

In Aurelia aurita, applied iodine induces medusa formation (strobilation). This process also occurs when the temperature is lowered. This was found to increase oxidative stress resulting in an increased production of iodine from iodide. One polyp produces several medusae (initially termed ephyrae) starting at the polyp's oral end. The spreading of strobilation down the body column is controlled by a feedback loop: ephyra anlagen decrease the tyrosine content in adjacent polyp tissue by producing melanin from tyrosine. Endogenous tyrosine is able to remove iodine by forming iodiferous tyrosine compounds. The reduced level of tyrosine causes the ephyra-polyp-border to move towards the basal end of the former polyp. We argue that an oxidant defence system may exist which makes use of iodide and tyrosine. Like other marine invertebrates, polyps of Aurelia contain iodide ions. Inevitably produced peroxides oxidise iodide into iodine. The danger to be harmed by iodine is strongly decreased by endogenous tyrosine which reacts with iodine to form iodiferous tyrosine compounds including thyroxin. Both substances together, iodide and tyrosine, form an efficient oxidant defence system which shields the tissue against damage by reactive oxygen species. In the course of evolution (from a species at the basis of the animal kingdom like Aurelia to a highly evolved species like man) the waste product thyroxin (indicating a high metabolic rate) has developed into a hormone which controls the metabolic rate.     

Growth, Degrowth, and Irreversible Cell Differentiation in Aurelia aurita

Growth patterns of the Scyphomedusa Aurelia aurita from TomalesBay. California, were examined in the field and in the laboratory.Manipulation of growth patterns demonstrated that degrowth andregrowth are not constrained by initial ievelopmental stage.Although initial degrowth of certain tissues is allometric (e.g.,gonads regress in 5 to 8 days; bell diameter decreases morerapidly at first than do the oral arms), thereafter regressionappears identical to, but reversed from normal growth. Regrowthpatterns are normal. Sexual maturation in the sea does not alwaysalter subsequent capacity for degrowth or regrowth to sexualmaturity in the laboratory, because reproductive and somatictissues do not always degenerate after spawning. Gonadal tissuecan be renewed and maintained in a ripe condition in the laboratoryapparently indefinitely. Sexual maturation is a size-dependentphenomenon, not an agespecific developmental event. Spermatogenesis, once initiated, proceeds irrespective of outsideevents. Labeled spermatogonial cells can continue to differentiateto form sperm even though the gonad containing those cells,and the animal itself, show rapid degrowth. The importance ofthis decoupling of developmental events is discussed. The experimentalimportance of animals with flexible life cycles is emphasized.     

Effect of mono- and divalent cations on polyp morphogenesis in isolated tentacles of Aurelia aurita(Scyphozoa)

Tentacles excised from syphistoma polyps of Aurelia aurita undergo rapid regeneration to form whole polyps following exposure to an excess or absence of specific ions. It has been shown that a 12–18 h exposure of isolated tentacles to 58 mM excess of Cs⁺ results in a rapid firing of nematocysts, followed by an accelerated, synchronous polyp morphogenesis. Absence of Mgt²⁺ from the culture solution for 4–24 h also led to an accelerated, synchronous polyp regeneration. In either experimental set-up, incubation in 5–10 mM hydroxyurea effectively halted regeneration. Exposure to an excess of Li⁺ (50–200 mm) or K⁺ (10–50 mM) caused no firing of nematocysts and a percentage of polyp regeneration only slightly higher than control tentacles. Use of the K⁺ channel blocker tetraethylammonium (TEA; 100–300 mM) lead to similar levels of regeneration. A Ca²⁺ or K⁺-reduced artificial culture solution did not enhance regeneration. Ouabain (1 mM) dampened the Cs⁺ induced acceleration of polyp morphogenesis, and when given without Cs⁺, elicited a control level response.