Hydra Nervous System Research Articles

A new look at the architecture and dynamics of the Hydra nerve net

The Hydra nervous system is the paradigm of a ‘simple nerve net’. Nerve cells in Hydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of the Hydra nerve net by immunostaining fixed polyps with a novel antibody that stains all nerve cells in Hydra. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution TEM (transmission electron microscopy) and serial block face SEM (scanning electron microscopy) show that the nerve nets consist of bundles of parallel overlapping neurites. Results from transgenic lines show that neurite bundles include different neural circuits and hence that neurites in bundles require circuit-specific recognition. Nerve cell-specific innexins indicate that gap junctions can provide this specificity. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.

A new look at the architecture and dynamics of the Hydra nerve net.

The Hydra nervous system is the paradigm of a 'simple nerve net'. Nerve cells in Hydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of the Hydra nerve net by immunostaining fixed polyps with a novel antibody that stains all nerve cells in Hydra. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution TEM (transmission electron microscopy) and serial block face SEM (scanning electron microscopy) show that the nerve nets consist of bundles of parallel overlapping neurites. Results from transgenic lines show that neurite bundles include different neural circuits and hence that neurites in bundles require circuit-specific recognition. Nerve cell-specific innexins indicate that gap junctions can provide this specificity. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.

Multiple neuronal populations control the eating behavior in Hydra and are responsive to microbial signals

Although recent studies indicate the impact of microbes on the central nervous systems and behavior, it remains unclear how the relationship between the functionality of the nervous system, behavior, and the microbiota evolved. In this work, we analyzed the eating behavior of Hydra, a host that has a simple nervous system and a low-complexity microbiota. To identify the neuronal subpopulations involved, we used a subpopulation-specific cell ablation system and calcium imaging. The role of the microbiota was uncovered by manipulating the diversity of the natural microbiota. We show that different neuronal subpopulations are functioning together to control eating behavior. Animals with a drastically reduced microbiome had severe difficulties in mouth opening due to a significantly increased level of glutamate. This could be reversed by adding a full complement of the microbiota. In summary, we provide a mechanistic explanation of how Hydra's nervous system controls eating behavior and what role microbes play in this.

Ensemble synchronization in the reassembly of Hydra’s nervous system

Although much is known about how the structure of the nervous system develops, it is still unclear how its functional modularity arises. A dream experiment would be to observe the entire development of a nervous system, correlating the emergence of functional units with their associated behaviors. This is possible in the cnidarian Hydra vulgaris, which, after its complete dissociation into individual cells, can reassemble itself back together into a normal animal. We used calcium imaging to monitor the complete neuronal activity of dissociated Hydra as they reaggregated over several days. Initially uncoordinated neuronal activity became synchronized into coactive neuronal ensembles. These local modules then synchronized with others, building larger functional ensembles that eventually extended throughout the entire reaggregate, generating neuronal rhythms similar to those of intact animals. Global synchronization was not due to neurite outgrowth but to strengthening of functional connections between ensembles. We conclude that Hydra's nervous system achieves its functional reassembly through the hierarchical modularity of neuronal ensembles. VIDEO ABSTRACT.

Efficient expression of a cnidarian peptide-gated ion channel in mammalian cells

ABSTRACT Hydra Na+ channels (HyNaCs) are peptide-gated ion channels of the DEG/ENaC gene family that are directly activated by neuropeptides of the Hydra nervous system. They have previously been successfully characterized in Xenopus oocytes. To establish their expression in mammalian cells, we transiently expressed heteromeric HyNaC2/3/5 in human HEK 293 and monkey COS-7 cells. We found that the expression of HyNaC2/3/5 using native cDNAs was inefficient and that codon optimization strongly increased protein expression and current amplitude in patch-clamp experiments. We used the improved expression of codon-optimized channel subunits to perform Ca2+ imaging and to demonstrate their glycosylation pattern. In summary, we established efficient expression of a cnidarian ion channel in mammalian cell lines.

Linking neurons to immunity: Lessons from Hydra.

According to the Greek mythology (1), Heracles’ second labor was the destruction of the Lernaean Hydra, a fearsome fire-breathing monster with a dog-like body and nine snake heads. Many had tried to slay the Lernaean Hydra but in vain: Any head that was cut off regrew and multiplied. It is remarkable how consistent the narrative of this myth is with our recent understanding of tissue and organ regeneration. Heracles was successful not only because of his divine origin (he was the son of Zeus after all) and the help of Athena, but particularly because of the assistance he received from his nephew Iolaus, who was assigned the job of cauterizing the exposed stumps of the Hydra’s severed heads. Of course, we now understand why Iolaus’ contribution was so critical: His flame consumed the local stem cells and stopped them from generating a new head! In PNAS, Klimovich et al. (2) go one step further and provide a reasonable explanation as to why the Lernaean Hydra could remain healthy despite inhabiting the dirty waters of an unfathomable Peloponnesian swamp. Using Hydra as the experimental model organism, the authors define the molecular identity of a unique group of neurons that are responsible for the rhythmic contractions of the body and provide insight into the immune mechanisms they (and other neurons) employ to regulate the animal’s microbial environment. These findings reveal remarkable similarities between the pacemaker activities of the Hydra nervous system and the nervous system of the gut in vertebrates (including humans), advancing our understanding of the interaction between microbiota and host organ systems. Hydra , a freshwater metazoan of the phylum Cnidaria , was first introduced in the laboratory in 1740s (3), when the Swiss naturalist Abraham Trembley discovered that cutting the body of this animal in half resulted in the … [↵][1]1Email: vassilis.pachnis{at}crick.ac.uk. [1]: #xref-corresp-1-1

Stem cell differentiation trajectories in Hydra resolved at single-cell resolution.

The adult Hydra polyp continually renews all of its cells using three separate stem cell populations, but the genetic pathways enabling this homeostatic tissue maintenance are not well understood. We sequenced 24,985 Hydra single-cell transcriptomes and identified the molecular signatures of a broad spectrum of cell states, from stem cells to terminally differentiated cells. We constructed differentiation trajectories for each cell lineage and identified gene modules and putative regulators expressed along these trajectories, thus creating a comprehensive molecular map of all developmental lineages in the adult animal. In addition, we built a gene expression map of the Hydra nervous system. Our work constitutes a resource for addressing questions regarding the evolution of metazoan developmental processes and nervous system function.

Peptide-gated ion channels and the simple nervous system of Hydra.

Neurons either use electrical or chemical synapses to communicate with each other. Transmitters at chemical synapses are either small molecules or neuropeptides. After binding to their receptors, transmitters elicit postsynaptic potentials, which can either be fast and transient or slow and longer lasting, depending on the type of receptor. Fast transient potentials are mediated by ionotropic receptors and slow long-lasting potentials by metabotropic receptors. Transmitters and receptors are well studied for animals with a complex nervous system such as vertebrates and insects, but much less is known for animals with a simple nervous system like Cnidaria. As cnidarians arose early in animal evolution, nervous systems might have first evolved within this group and the study of neurotransmission in cnidarians might reveal an ancient mechanism of neuronal communication. The simple nervous system of the cnidarian Hydra extensively uses neuropeptides and, recently, we cloned and functionally characterized an ion channel that is directly activated by neuropeptides of the Hydra nervous system. These results demonstrate the existence of peptide-gated ion channels in Hydra, suggesting they mediate fast transmission in its nervous system. As related channels are also present in the genomes of the cnidarian Nematostella, of placozoans and of ctenophores, it should be considered that the early nervous systems of cnidarians and ctenophores have co-opted neuropeptides for fast transmission at chemical synapses.

Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review

Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

Cnidarians represent the first animal phylum with an organized nervous system and a complex active behavior. The hydra nervous system is formed of sensory-motoneurons, ganglia neurons and mechanoreceptor cells named nematocytes, which all differentiate from a common stem cell. The neurons are organized as a nerve net and a subset of neurons participate in a more complex structure, the nerve ring that was identified in most cnidarian species at the base of the tentacles. In order to better understand the genetic control of this neuronal network, we analysed the expression of evolutionarily conserved regulatory genes in the hydra nervous system. The Prd-class homeogene prdl-b and the nuclear orphan receptor hyCOUP-TF are expressed at strong levels in proliferating nematoblasts, a lineage where they were found repressed during patterning and morphogenesis, and at low levels in distinct subsets of neurons. Interestingly, Prd-class homeobox and COUP-TF genes are also expressed during neurogenesis in bilaterians, suggesting that mechanoreceptor and neuronal cells derive from a common ancestral cell. Moreover, the Prd-class homeobox gene prdl-a, the Antp-class homeobox gene msh, and the thrombospondin-related gene TSP1, which are expressed in distinct subset of neurons in the adult polyp, are also expressed during early budding and/or head regeneration. These data strengthen the fact that two distinct regulations, one for neurogenesis and another for patterning, already apply to these regulatory genes, a feature also identified in bilaterian related genes.

Identification of a vasopressin-like immunoreactive substance in hydra

Vasopressin (VP)-like immunoreactivity has long been known in the hydra nervous system, but has not yet been structurally identified. In this study, using HPLC fractionation and an immunological assay, we have purified two peptides, FPQSFLPRGamide and SFLPRGamide, from Hydra magnipapillata. Both the peptides shared the same C-terminal structure, -PRGamide, with Arg-VP. The nonapeptide proved to be Hym-355, a peptide that stimulates neuronal differentiation in hydra. Detailed evaluation by competitive enzyme-linked immunosorbent assay (ELISA) and double immunostaining using anti-VP and anti-Hym-355 antibodies enabled us to conclude that the two peptides account for a major part of the VP-like immunoreactivity in hydra nerve cells.

Immunocytochemically defined populations of neurons progressively increase in size through embryogenesis of Hydra vulgaris.

The hydra nervous system shares many features with nervous systems of more complex organisms but serves as a unique model system due to its simplicity and constant regeneration. Development of neuron populations during and after hydra embryogenesis is not well understood. In this study, neurons were identified at prehatching and posthatching stages with RFamide or JD1 antisera. These populations were further subdivided into ganglion, sensory, or unclassifiable neurons, and all identified populations were statistically analyzed over developmental time. RFamide-positive neurons appeared 20 days after the cuticle formed around the embryo. The JD1-positive neuron population appeared just after hatching, but by adulthood it had surpassed the size of the RFamide-positive population. All neuron populations progressively increased through their adult levels. Density of most of the populations, however, did not. For instance, during the 5-fold increase in size that the hydra experienced between 5 days posthatching and adulthood, the number of RFamide-positive neurons rose approximately 2-fold and the number of JD1-positive neurons 4-fold. However, the density of neurons in each of these populations fell. These data do not support the hypothesis that large-scale culling of neurons during development, frequently found in other animals, occurs in hydra.

FMRFamide-like immunoreactivity in the nervous system of Hydra.

FMRFamide-like immunoreactivity has been localized in different parts of the hydra nervous system. Immunoreactivity occurs in nerve perikarya and processes in the ectoderm of the lower peduncle region near the basal disk, in the ectoderm of the hypostome and in the ectoderm of the tentacles. The immunoreactive nerve perikarya in the lower peduncle region form ganglion-like structures. Radioimmunoassays of extracts of hydra gave displacement curves parallel to standard FMRFamide and values of at least 8 pmol/gram wet weight of FMRFamide-like immunoreactivity. The immunoreactive material eluted from Sephadex G-50 in several components emerging shortly before or after position of authentic FMRFamide. The presence of FMRFamide-like material in coelenterates shows that this family of peptides is of great antiquity.

Nervous system transplantation in hydra

AbstractCnidarians are the most primitive metazoans possessing a nervous system. The hydroid nervous system consists of single sensory, neurosecretory and ganglionic cells concentrated at the extremities of the animal. Present evidence suggests that nerve tissue arises from the differentiation of interstitial cells.Exposure of hydra to nitrogen mustard (methyl bis (beta‐chloro ethyl) amine hydrochloride) causes the selective elimination of interstitial cells (Diehl and Burnett, '64). Cells which normally arise from interstitial cell differentiation subsequently become depleted. Distoproximal grafts between normal hydra and nitrogen mustard treated animals of a different species result in interstitial cell migration across the graft junction. Autoradiographic evidence demonstrates that the host hydra accepts the donor's interstitial cells which proliferate and differentiate into nerve tissue and functional cnidocytes.Although newly established cnidocyte populations are normal in seven day old grafts, nerve and interstitial cell populations are reduced. Furthermore, there is an abnormal apico‐basal distribution of interstitial cells in these grafts.A comparison of “nervous system transplant” animals with those treated with nitrogen mustard for a similar time period but not grafted suggests that the transplanted nervous system is functional. The ultimate death of experimental animals supports speculation that nitrogen mustard causes irrevocable gastrodermal damage.Various parameters germane to the function of the nervous system in hydra are being established, including developmental, behavioral and electrophysiological correlates. Once nervous system transplant chimeras are reared in sufficient numbers, a comparison of these with host and donor species should provide insight into the functional nature of hydra's nervous system.