Immortality and the base of multicellular life: Lessons from cnidarian stem cells

Cnidarians are phylogenetically basal members of the animal kingdom (>600 million years old). Together with plants they share some remarkable features that cannot be found in higher animals. Cnidarians and plants exhibit an almost unlimited regeneration capacity and immortality. Immortality can be ascribed to the asexual mode of reproduction that requires cells with an unlimited self-renewal capacity. We propose that the basic properties of animal stem cells are tightly linked to this archaic mode of reproduction. The cnidarian stem cells can give rise to a number of differentiated cell types including neuronal and germ cells. The genomes of Hydra and Nematostella, representatives of two major cnidarian classes indicate a surprising complexity of both genomes, which is in the range of vertebrates. Recent work indicates that highly conserved signalling pathways control Hydra stem cell differentiation. Furthermore, the availability of genomic resources and novel technologies provide approaches to analyse these cells in vivo. Studies of stem cells in cnidarians will therefore open important insights into the basic mechanisms of stem cell biology. Their critical phylogenetic position at the base of the metazoan branch in the tree of life makes them an important link in unravelling the common mechanisms of stem cell biology between animals and plants.     

Incorporation of a horizontally transferred gene into an operon during cnidarian evolution

Genome sequencing has revealed examples of horizontally transferred genes, but we still know little about how such genes are incorporated into their host genomes. We have previously reported the identification of a gene (flp) that appears to have entered the Hydra genome through horizontal transfer. Here we provide additional evidence in support of our original hypothesis that the transfer was from a unicellular organism, and we show that the transfer occurred in an ancestor of two medusozoan cnidarian species. In addition we show that the gene is part of a bicistronic operon in the Hydra genome. These findings identify a new animal phylum in which trans-spliced leader addition has led to the formation of operons, and define the requirements for evolution of an operon in Hydra. The identification of operons in Hydra also provides a tool that can be exploited in the construction of transgenic Hydra strains.     

Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians

Cnidarians are among the simplest extant animals; however EST analyses reveal that they have a remarkably high level of genetic complexity. In this article, we show that the full diversity of metazoan signaling pathways is represented in this phylum, as are antagonists previously known only in chordates. Many of the cnidarian ESTs match genes previously known only in non-animal kingdoms. At least some of these represent ancient genes lost by all bilaterians examined so far, rather than genes gained by recent lateral gene transfer.     

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

Cnidarians lack well developed organs, but they have evolved the molecular and cellular components needed to assemble a nervous system. The apparent 'simplicity' of the cnidarian nervous net does not occur at the cellular level, but rather in the organisation of conducting systems. Cnidarian neurons are in fact electrically excitable, show the typical extended morphology and are connected by chemical synapses or gap junctions. They have been regarded as peptidergic, given the wealth of neuropeptides generally distributed along neurites and in cell bodies, supporting the hypothesis of a modulatory role in neurotransmission. However, the presence of clear-cored, as well as dense-cored synaptic vesicles in cnidarian neurons suggests both fast and slow synaptic transmission mechanisms. In fact, biochemical and functional evidence indicates that classical neurotransmitters and their metabolic partners are present in cnidarian tissues, where they are involved in coordinating motility and behavior. We have identified and characterized in Hydra tissues receptors to the inhibitory and excitatory amino acid neurotransmitters, GABA, glycine and NMDA, that are similar to mammalian ionotropic receptors in terms of their biochemical and pharmacological properties. These receptors appear to regulate pacemaker activities and their physiological correlates; in the live animal, they also affect feeding behavior, namely the duration and termination of the response elicited by reduced glutathione, with opposite actions of GABA and glycine or NMDA, respectively. These results suggest that modulation of cellular signaling through ligand-gated-ion channels is an ancient characteristic in the animal kingdom, and that the pharmacological properties of these receptors have been highly conserved during evolution.     

Cnidarian neurobiology: what does the future hold?

Cnidarians have long been recognized as occupying a unique position in nervous system evolution and, consequently, have attracted considerable attention from neurobiologists over the years. During the latter half of the 20th century, the application of a variety of electrophysiological and other methods provided us with a great deal of information about the scope and composition of the cnidarian nervous system. Here, I will briefly review what is known about cnidarian nervous systems, what remains to be found and, most importantly, discuss the status and future of the field.     

GFP expression in Hydra: lessons from the particle gun

The cnidarian Hydra is an important model organism to study pattern formation and tem cell differentiation. In the past, however, it has been difficult to study gene function in Hydra because the animals have hot been accessible to gene transfection studies, we have now developed a method to transiently express GFP-tagged proteins in Hydra using a green fluorescent protein (GFP) expression plasmid under the control of the Hydra actin promoter and a particle gun to introduce it into Hydra cell nuclei. We achieve strong transient GFP expression in a small but reproducible number of epithelial and interstitial cells. Implications for the use of this method to carry out single cell assays with GFP-tagged Hydra proteins are discussed.     

Exceptionally preserved jellyfishes from the Middle Cambrian

Cnidarians represent an early diverging animal group and thus insight into their origin and diversification is key to understanding metazoan evolution. Further, cnidarian jellyfish comprise an important component of modern marine planktonic ecosystems. Here we report on exceptionally preserved cnidarian jellyfish fossils from the Middle Cambrian (approximately 505 million years old) Marjum Formation of Utah. These are the first described Cambrian jellyfish fossils to display exquisite preservation of soft part anatomy including detailed features of structures interpreted as trailing tentacles and subumbrellar and exumbrellar surfaces. If the interpretation of these preserved characters is correct, their presence is diagnostic of modern jellyfish taxa. These new discoveries may provide insight into the scope of cnidarian diversity shortly after the Cambrian radiation, and would reinforce the notion that important taxonomic components of the modern planktonic realm were in place by the Cambrian period.     

Variations on a theme? Polyp and medusa development in Podocoryna carnea

Hydrobiologia - The life cycles of many cnidarian species are notable for including two stages with very different morphologies – sessile polyp and swimming medusa. Cnidarians thus provide an...     

A peptide-gated ion channel from the freshwater polyp Hydra

Chemical transmitters are either low molecular weight molecules or neuropeptides. As a general rule, neuropeptides activate only slow metabotropic receptors. To date, only one exception to this rule is known, the FMRFamide-activated Na(+) channel (FaNaC) from snails. Until now FaNaC has been regarded as a curiosity, and it was not known whether peptide-gated ionotropic receptors are also present in other animal groups. Nervous systems first evolved in cnidarians, which extensively use neuropeptides. Here we report cloning from the freshwater cnidarian Hydra of a novel ion channel (Hydra sodium channel, HyNaC) that is directly gated by the neuropeptides Hydra-RFamides I and II and is related to FaNaC. The cells expressing HyNaC localize to the base of the tentacles, adjacent to the neurons producing the Hydra-RFamides, suggesting that the peptides are the natural ligands for this channel. Our results suggest that neuropeptides were already used for fast transmission in ancient nervous systems.     

DNA-binding characteristics of cnidarian Pax-C and Pax-B proteins in vivo and in vitro: no simple relationship with the Pax-6 and Pax-2/5/8 classes

Cnidarians are the simplest animals in which distinct eyes are present. We have previously suggested that cnidarian Pax-Cam might represent a precursor of the Pax-6 class. Here we show that when expressed in Drosophila imaginal discs, Pax-Cam chimeric proteins containing the C-terminal region of EY were capable of eye induction and driving expression of a reporter gene under the control of a known EY target (the sine oculis gene). Whilst these results are consistent with a Pax-6-like function for Pax-Cam, in band shift experiments we were unable to distinguish the DNA-binding behaviour of the Pax-Cam Paired domain from that of a second Acropora Pax protein, Pax-Bam. The ability of a Pax-Bam/EY chimera to also induce eye formation in leg imaginal discs, together with the in vitro data, cast doubt on previously assumed direct relationships between cnidarian Pax genes and the Pax-6 and Pax-2/5/8 classes of bilateral animals.     

Evolutionary crossroads in developmental biology: Cnidaria

There is growing interest in the use of cnidarians (corals, sea anemones, jellyfish and hydroids) to investigate the evolution of key aspects of animal development, such as the formation of the third germ layer (mesoderm), the nervous system and the generation of bilaterality. The recent sequencing of the Nematostella and Hydra genomes, and the establishment of methods for manipulating gene expression, have inspired new research efforts using cnidarians. Here, we present the main features of cnidarian models and their advantages for research, and summarize key recent findings using these models that have informed our understanding of the evolution of the developmental processes underlying metazoan body plan formation.     

First identification and localization of a visual pigment in Hydra (Cnidaria, Hydrozoa)

The cnidarian Hydra does not possess identified photoreceptive structures or specialized cells for light detection; nevertheless, it shows a marked photosensitivity. So far no evidence has been previously reported about the localization of the proteins involved in the photoresponse. We used polyclonal antibodies and immunofluorescence microscopy on whole-mount Hydra to identify a putative rhodopsin-like protein. Our results show an immunoreactivity in the ectodermal layer of Hydra, which corresponds in position to the nervous epidermal sensory cells. These data provide the first identification of a rhodopsin-like protein in a phylogenetically old invertebrate and give a new insight into the Hydra photoreceptive response.     

Seven GC-rich microbial genomes adopt similar codon usage patterns regardless of their phylogenetic lineages

Seven GC-rich (group I) and three AT-rich (group II) microbial genomes are analyzed in this paper. The seven microbes in group I belong to different phylogenetic lineages, even different domains of life. The common feature is that they are highly GC-rich organisms, with more than 60% genomic GC content. Group II includes three bacteria, which belong to the same subdivision as Pseudomonas aeruginosa in group I. The genomic GC content of the three bacteria is in the range of 26-50%. It is shown that although the phylogenetic lineages of the organisms in group I are remote, the common feature of highly genomic GC content forces them to adopt similar codon usage patterns, which constitutes the basis of an algorithm using a set of universal parameters to recognize known genes in the seven genomes. The common codon usage pattern of function known genes in the seven genomes is GGS type, where G, G, and S are the bases of G, non-G, and G/C, respectively. On the contrary, although the phylogenetic lineages of the three bacteria in group II are quite close, the codon usage patterns of function known genes in these genomes are obviously distinct. There are no universal parameters to identify known genes in the three genomes in group II. It can be deduced that the genomic GC content is more important than phylogenetic lineage in gene recognition programs. We hope that the work might be useful for understanding the common characteristics in the organization of microbial genomes.     

Hydra, a fruitful model system for 270 years

The discovery of Hydra regeneration by Abraham Trembley in 1744 promoted much scientific curiosity thanks to his clever design of experimental strategies away from the natural environment. Since then, this little freshwater cnidarian polyp flourished as a potent and fruitful model system. Here, we review some general biological questions that benefitted from Hydra research, such as the nature of embryogenesis, neurogenesis, induction by organizers, sex reversal, symbiosis, aging, feeding behavior, light regulation, multipotency of somatic stem cells, temperature-induced cell death, neuronal transdifferentiation, to cite only a few. To understand how phenotypes arise, theoricists also chose Hydra to model patterning and morphogenetic events, providing helpful concepts such as reaction-diffusion, positional information, and autocatalysis combined with lateral inhibition. Indeed, throughout these past 270 years, scientists used transplantation and grafting experiments, together with tissue, cell and molecular labelings, as well as biochemical procedures, in order to establish the solid foundations of cell and developmental biology. Nowadays, thanks to transgenic, genomic and proteomic tools, Hydra remains a promising model for these fields, but also for addressing novel questions such as evolutionary mechanisms, maintenance of dynamic homeostasis, regulation of stemness, functions of autophagy, cell death, stress response, innate immunity, bioactive compounds in ecosystems, ecotoxicant sensing and science communication.     

埃迪卡拉纪至寒武纪苗岭世刺细胞动物化石研究现状与展望

刺细胞动物是一类具有刺细胞的水生无脊椎动物,分布在世界各地的海洋和淡水中.作为后生动物最早分化出的一支,刺细胞动物对研究后生动物的起源和早期演化具有极其重要的意义,也为研究后生动物系统发育、地层对比和古地理恢复等方面提供了重要的科研线索.本文简要介绍了刺细胞动物早期(埃迪卡拉纪至寒武纪苗岭世)的化石记录和研究现状,将刺...     

The Hydra genome: insights, puzzles and opportunities for developmental biologists

The sequencing of a Hydra genome marked the beginning of a new era in the use of Hydra as a developmental model. Analysis of the genome sequence has led to a number of interesting findings, has required revisiting of previous work, and most importantly presents new opportunities for understanding the developmental biology of Hydra. This review will de-scribe the history of the Hydra genome project, a selection of results from it that are relevant to developmental biologists, and some future research opportunities provided by Hydra genomics.     

The Synaptonemal Complex of Basal Metazoan Hydra:More Similarities to Vertebrate than Invertebrate Meiosis Model Organisms

The synaptonemal complex （SC） is an evolutionarily well-conserved structure that mediates chromosome synapsis during prophase of the first meiotic division. Although its structure is conserved, the characterized protein components in the current metazoan meiosis model systems （Drosophila melanogaster, Caenorhabditis elegans, and Mus musculus） show no sequence homology, challenging the question of a single evolutionary origin of the SC. However, our recent studies revealed the monophyletic origin of the mammalian SC protein components. Many of them being ancient in Metazoa and already present in the cnidarian Hydra. Remarkably, a comparison between different model systems disclosed a great similarity between the SC components of Hydra and mammals while the proteins of the ecdysozoan systems （D. rnelanogaster and C. elegans） differ significantly. In this review, we introduce the basal-branching metazoan species Hydra as a potential novel invertebrate model system for meiosis research and particularly for the investigation of SC evolution, function and assembly. Also, available methods for SC research in Hydra are summarized.     

The attachment of nematocytes from the primitive invertebrate Hydra to fibronectin is specific and RGD-dependent.

The transient attachment of cells to components of the extracellular matrix is an important step in the complex molecular mechanisms involved in amoeboid cell locomotion. We have analyzed the attachment of nematocytes from the freshwater cnidarian Hydra to fibronectin which is a constituent of the mesoglea, the extracellular matrix, of the polyps. The percentage of attaching cells increased gradually in a concentration-dependent manner and reached a plateau value at a fibronectin concentration of 50 micrograms/ml. Attachment was inhibited by exposure of the fibronectin-coated surfaces to antibodies against the cell binding domain of fibronectin or by incubating the cells with peptides containing the recognition sequence Arg-Gly-Asp (RGD) known from vertebrate cells. This, together with data obtained by affinity chromatography, indicates that RGD-dependent binding to fibronectin, mediated by a receptor which possibly belongs to the integrin family, already occurs in Hydra, a member of an evolutionary low invertebrate phylum.     

Genome sizes and chromosomes in the basal metazoan Hydra

Hydras belong to one of the earliest eumetazoan animal groups, but to date very little is known about their genome sizes, gene numbers, and chromosomes. Here we provide genome size estimates and corresponding karyotypes for five Hydra species. Nuclear DNA contents were assessed by slide-based Feulgen microphotometry. Hydra oligactis possesses the largest genome of 1450 Mbp, followed by similar 1 C capacities in H. carnea (1350 Mbp), H. vulgaris (1250 Mpb) and H. circumcincta (1150 Mbp). The smallest genome of 380 Mbp was determined in H. viridissima. While the number of chromosomes is identical in all five Hydra species (2n = 30), the size of the chromosomes is strictly correlated to the size of the genome, with H. viridissima having conspicuously small chromosomes. The taxonomic and evolutionary significance of the C-value and chromosomal size variation in this ancient group of metazoans as well as its impact on genomic organization and forthcoming genome projects are discussed.