DeSalle R., Gregory T. R., Johnston J. S. (2005). (B) The graph shows normalized responses from the same muscle cell indicating l-glutamate is the most potential excitatory molecule compared with d-glutamate or l/d-aspartate. Nitric oxide regulates swimming in the jellyfish. Resolving the metazoan tree of life with advanced bioinformatic pipelines and phylogenetic methods, http://www.sicb.org/meetings/2013/schedule/abstractdetails.php?id=235, http://www.sicb.org/meetings/2015/schedule/abstractdetails.php?id=466, http://sicb.org/meetings/2012/schedule/abstractdetails.php?id=527, http://www.sicb.org/meetings/2013/schedule/abstractdetails.php?id=1280, www.sicb.org/meetings/2015/schedule/abstractdetails.php?id=851. Not surprisingly, the recruitment of different secretory cell lineages for more localized neural-like signaling might have occurred multiple times in evolution. The presence of many components critical for synaptic function in bilaterians (e.g. Additional comparative genomic data, especially from different lineages of sponges and ctenophores, would be indispensable to better resolve deep metazoan phylogeny. Four of them are: Here, I define neurons as polarized secretory cells specialized for directional propagation of electrical signals leading to the release of extracellular messengers features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore. This tripartite synapse arrangement was used as a reliable electron microscopy marker for neurons (Hernandez-Nicaise, 1991). (D) The distributed neural networks around the mouth of Pleurobrachia. The phylum Ctenophora, or comb jellies, is of particular interest for two reasons. B., Citarella M. R., Kocot K. M., Bobkova Y. V., Halanych K. M., Moroz L. L. (2012). 8600 Rockville Pike 3). Below, I will expand and discuss some of these data and hypotheses. The anatomy of the aboral complex is well described (Aronova, 1974; Aronova, 1975; Aronova et al., 1979; Hernandez-Nicaise, 1991; Tamm, 1982; Tamm and Tamm, 2002). To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. c.v., cytoplasmic vesicles; co, dense coat on the postsynaptic membrane; e.r., endoplasmic reticulum; g, Golgi complex; l, intracleft dense line; M, mesoglea; mi, mitochondrion; mt, microtubules; n, nucleus; p, presynaptic dense projections; r, ribosomes; s.v., synaptic vesicle. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. Using capillary electrophoresis, we detected l/d-glutamate and l/d-aspartate as well as -aminobutyric acid (GABA) in all four ctenophore species investigated (Pleurobrachia, Beroe, Bolinopsis, and Mnemiopsis) (Moroz et al., 2014). Ali A., Leclre L., Jager M., Dayraud C., Chang P., Le Guyader H., Queinnec E., Manuel M. (2011). Although some phylogenomic studies still favor this classical classification (Nosenko et al., 2013; Philippe et al., 2009), independent analyses, including our recent large-scale phylogenomic studies on 10 ctenophore species (Moroz et al., 2014), reject the Coelenterata (Cnidaria and Ctenophrora) hypothesis (i.e. (C) GABA immunolabeling of muscle cells in Pleurobrachia. However, I would not exclude the presence of other small signal molecules, including those with no analogs in other metazoans. The sea gooseberry Pleurobrachia bachei (Fig. A simplified view of evolutionary relationships in the animal kingdom; the tree is combined with the presence or absence of a central nervous system (CNS) or brain in selected animal clades [modified and updated from Moroz (Moroz, 2009; Moroz, 2012; Moroz et al., 2014)]. For example, Ryan (Ryan, 2014) suggests a few lines of evidence uniting the nervous systems of ctenophores, cnidarians, and bilaterians. Interestingly, pannexins are apparently absent in sponges and placozoans, and this situation might represent secondary gene loss in these lineages. Phylogenomics meets neuroscience: how many times might complex brains have evolved? Superficially, the nervous system architecture in ctenophores looks like a simpler nerve net (Fig. In parallel, traditional hypotheses about the earliest relationships in the animal phylogeny have been challenged. Jager M., Chiori R., Ali A., Dayraud C., Quinnec E., Manuel M. (2011). However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. On the bright side, this controversy has helped us understand much more about the 'hidden' biology of comb jellies and sponges [6]: . The majority of canonical low molecular weight transmitters are absent in ctenophores consistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Neurons that connect without synapses | Science Yet, as our capillary electrophoresis data suggest, these PH-related enzymes, if functional, do not produce any known catecholamines in ctenophores. modified muscles and cilia), also highly abundant in these structures. Borowiec M. L., Lee E. K., Chiu J. C., Plachetzki D. C. (2015). Nosenko T., Schreiber F., Adamska M., Adamski M., Eitel M., Hammel J., Maldonado M., Mller W. E., Nickel M., Schierwater B., et al. Striedter G. F., Belgard T. G., Chen C. C., Davis F. P., Finlay B. L., Gntrkn O., Hale M. E., Harris J. Dunn C. W., Hejnol A., Matus D. Q., Pang K., Browne W. E., Smith S. A., Seaver E., Rouse G. W., Obst M., Edgecombe G. D., et al. The pacific lobate Bolinopsis infundibulum has the second smallest genome (~220 Mb) whereas Beroe abyssicola has one of the largest genomes within the group: ~1 Gb. Thus, the corollary of the hypothesis of independent origins or parallel evolution of neurons might be independent origins or parallel evolution of synapses with different types of secretory specificity (Moroz, 2015), initially encoded in the ancestral cell lineages and later preserved in more complex neural systems. (2014). These data suggest both well-developed glutamate signaling and its remarkable parallel evolution in ctenophores. A diversity of secretory signal peptides and their receptors (including expansion of ASSCs/DEGs/ENaCs) may have also been recruited for this role in ctenophores independently from other metazoans, paralleled by the diversification of gap junction proteins most profoundly expressed in the apical organ of extant ctenophores. April 20, 2023 at 2:00 pm Shimmering, gelatinous comb jellies wouldn't appear to have much to hide. 1). This fundamental work led to the most well-known hypothesis of nervous system evolution (Parker, 1919). Third, we do find a number of genes encoding presumed pre- and post-synaptic proteins in the Pleurobrachia genome that are shared with Choanoflagellates and Capsaspora, suggesting a single-cell origin of the backbone of the canonical synaptic machinery revealed in proteomic studies on bilaterians (Ryan and Grant, 2009). These muscles are used to control hydroskeleton tone, body shape and feeding, which might be original functions of muscle elements in animal ancestors. Several of these ctenophore-specific precursors are expressed in polarized cells around the mouth, in tentacles and polar fields (e.g. Only a few cnidarian species have distinct striated muscles, suggesting their independent origins (Steinmetz et al., 2012). This is an example of a Ctenophore in the daylight. Mackie G. O., Mills C. E., Singla C. L. (1992). My oldest sister is a sea walnut? Sherwood T. W., Frey E. N., Askwith C. C. (2012). Ryan J. F., Pang K., Schnitzler C. E., Nguyen A. D., Moreland R. T., Simmons D. K., Koch B. J., Francis W. R., Havlak P., Smith S. A., et al.NISC Comparative Sequencing Program (2013b). The first fossil ctenophore from the lower Devonian of West Germany, Maintenance of isolated smooth muscle cells of the ctenophore. Classical Eumetazoans (i.e animals with nervous systems, Cnidaria, Ctenophora and Bilateria) are the polyphyletic clade (, Ctenophores have reduced complements of canonical neurogenic, synaptic, muscle, immune and developmental genes, as well as the apparent absence of, Many bilaterian/cnidarian neuron-specific genes and genes of classical neurotransmitter pathways are either absent or, if present, are not expressed in neurons. More than 550 million years of their evolutional history resulted in multiple unique innovations supported by at least 10,000 ctenophore-specific genes controlling highly deterministic development and other systemic functions (Moroz et al., 2014). We have brains that send messages almost instantly throughout the body through a connection of nerves, they do not have that. Scale bar: 100 nm. Our data also imply that classical low molecular weight transmitter systems such as cholinergic, GABAergic and three classes of monoaminergic systems (serotonergic, histaminergic, dopaminergicadrenergic) were recruited for neuronal functions in cnidarian/bilaterians lineages. . Glutamate and aspartate as neuromuscular transmitter candidates in the ctenophore Pleurobrachia bachei. There is a possibility that the last common ancestor of extant ctenophores shared neuronal toolkits with other eumetazoans (Cnidaria and Bilateria) but this scenario, regardless of phylogenetic reconstructions (Moroz, 2014), still implies a situation whereby modern ctenophores developed a very distinct molecular make-up and lost(?) (2009). Ryan J. F., Pang K., Mullikin J. C., Martindale M. Q., Baxevanis A. D. (2010). Gap junctions suggest epithelial conduction within the comb plates of the ctenophore. For example, we found that GABA immunoreactivity is localized in muscles (. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of germline genes with stemness, Cholinergic and monoaminergic mechanisms associated with control of bioluminescence in the ctenophore, Mechanism of photoinactivation and reactivation in the bioluminescence system of the ctenophore, The electrophysiology of single smooth muscle cells isolated from, Physiology of a bidirectional, excitatory, chemical synapse, Three-dimensional structure of bidirectional, excitatory chemical synapses in the jellyfish, Electron microscopic observation of the aboral organ of Ctenophora. (2014) The ctenophore genome and the . Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. NSF workshop report: discovering general principles of nervous system organization by comparing brain maps across species, Mechanisms of ciliary co-ordinations in ctenophores, Mechanical synchronization of ciliary beating within comb plates of ctenophores, Unilateral ciliary reversal and motor responses during prey capture by the ctenophore, Ciliary reversal without rotation of axonemal structures in ctenophore comb plates, Massive actin bundle couples macrocilia to muscles in the ctenophore, A giant nerve net with multi-effector synapses underlying epithelial adhesive strips in the mouth of, Novel bridge of axon-like processes of epithelial cells in the aboral sense organ of ctenophores. Regardless of evolutionary interpretations, the sequenced Pleurobrachia genome, combined genomic, metabolomic and physiological data on 10 different species revealed extraordinary and unique molecular diversity of developmental and neural signaling pathways. The presynaptic component is usually interpretable as a nerve fiber, but realistic synapses have also been found with a muscle cell as the presynaptic element (Horridge, 1974). Combined, these data support a hypothesis of parallel evolution of synaptic organization in ctenophores, which also reflects the development of their unique neurotransmitter organization. Gregory T. R., Nicol J. Ctenophore | Types, Characteristics & Adaptations | Britannica Hernandez-Nicaise M. L., Mackie G. O., Meech R. W. (1980). As ctenophores possess an elaborate and centralized nervous system (contrary to poriferans), this radically changes current perspectives on the early evolution of neurons and nervous systems and raises a number of possibilities with regard to the evolutionary origin (s) of neurons. Duration of the recording in A is 50 s. In the past, ctenophores and cnidarians were considered as two sister lineages forming the clade Coelenterata. For example, Pleurobrachia has voltage-gated sodium and many potassium channels that were apparently absent in sponges and a greater diversity of aquaporins (water channels) (Papadopoulos and Verkman, 2013) than all other basal metazoans combined. The comparative data suggest that at least some neuronal cell types and complex integrative structures (such as the aboral organ) evolved independently in the ctenophore lineage (Moroz, 2012; Moroz et al., 2014). Animals Alien-like comb jellies have a nervous system like nothing ever seen before News By Stephanie Pappas published 15 May 2023 Strange sea creatures called ctenophores have a fused. 3C) (Jager et al., 2011; Moroz et al., 2014). Lentz, 1968; Mackie, 1970; Mackie, 1990; Miller, 2009; Moroz, 2009; Parker, 1919; Sakharov, 1974) and recently (Marlow and Arendt, 2014; Moroz, 2014; Moroz et al., 2014), I will emphasize the alternative polygenesis scenario in this communication. Were the First Animals Sponge-Like?: Complexity in the animal tree of All ctenophores possess a pair of small anal pores located adjacent to the apical sensory organ thought to control osmotic pressure. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. A., Ernstrom G. G., Nix P., Davis M. W., Jorgensen E. M. (2008). Even early synapses might use more than one secretory product. Importantly, Hernandez-Nicaise (Hernandez-Nicaise, 1991) indicated that reciprocal and symmetrical synapses are less abundant than polarized synapses, except at the aboral organ and the core of tentacles. Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. Jager M., Quinnec E., Houliston E., Manuel M. (2006). As such, multiple origins of neurons from different classes of secretory cells might occur more than once during ~600 million years of animal evolution a part of transition from temporal to spatial differentiation (Mikhailov et al., 2009). PDF Magazine R1119 - Cell Press In collaboration with T. R. Gregory (Guelph University, Canada), we screened various ctenophore species using flow cytometry and densitometry, searching for small genome sizes following previously published protocols (DeSalle et al., 2005). (2007). Second, we also found that orthologs of bilaterian and cnidarian pan-neuronal markers are not expressed in ctenophore neurons, suggesting that they perform different functions. Not surprisingly, the name of the phylum is derived from the Greek cteno-phora, or comb-bearers. The hidden biology of sponges and ctenophores - ScienceDirect open access Highlights Keywords ctenophores sponges comparative biology genomics morphology Viewing all animals through a bilaterian lens distorts the view of animal evolution We have two windows on early animal evolution: fossils and living animal diversity. 4 in Ryan (Ryan et al., 2013b)]. Jager M., Dayraud C., Mialot A., Quinnec E., le Guyader H., Manuel M. (2013). Colored circles indicate possible events of multiple origins of neurons: blue, the origin of neurons in Ctenophores; red, the origin of neurons in Bilateria/Cnidaria clade; it is also possible that some neural populations could originate in bilaterian lineages (yellow, orange and pink circles). The activity of cilia is under control of the aboral organ composed of several cell types with gravity sensors and a statolith consisting of about 100 lithocytes (Tamm, 1973; Tamm, 1982). (2011). Below, I will further clarify three controversial points following the discussion on the origin and early evolution of neural systems. Earlier work on the neurobiology of ctenophores performed by Horridge (Bullock and Horridge, 1965; Horridge, 1965c; Horridge, 1974), Tamm (Moss and Tamm, 1986; Moss and Tamm, 1987; Tamm, 1982; Tamm, 1984; Tamm and Moss, 1985; Tamm and Tamm, 1981; Tamm and Tamm, 1987) and others (Haddock, 2007; Satterlie and Case, 1978) revealed a very complex behavioral repertoire in these marine predators. Login . The ctenophore genome and the evolutionary origins of neural systems, Electrophysiological control of ciliary motor responses in the ctenophore, A calcium regenerative potential controlling ciliary reversal is propagated along the length of ctenophore comb plates. (3) How chemically heterogeneous are neuronal populations in ctenophores? Moreover, neural transmitter systems are not only characterized by the presence of specific synthesis enzymes the heterogeneity of secretory specificity of neurons is one of the most fundamental features of any nervous system. Typical responses of ctenophore muscle cells to local pulses of a transmitter application were externally recorded both as individual action potentials and video contractions from a single muscle cell (D). The first proto-neurons could mediate their action via volume transmission without structurally differentiated synapses. An independent origin Ctenophores' distinct nerve net supports the idea that their nervous system could have evolved independently of that of other animals. If so, what is the functional role of this non-neuronal transmitter secretion? When Chun separated blastomers in two-cell embryos, he found that each half-embryo developed exactly half of adult structures in ctenophores suggesting the presence of highly deterministic mechanisms even after the first division during the cleavage. Structure and activity of the acid-sensing ion channels. As a library, NLM provides access to scientific literature. The second category is a group of genes that are specifically expressed in the Pleurobrachia neurons but are not specifically expressed in neurons in other eumetazoans (e.g. The structural relationships and functional interactions among different neural elements are mostly unknown. This explains the recruitment in ctenophores of certain RNA binding proteins, which act as a cargo to transport selected localized RNA (e.g. The author thanks FHL for facilities during animal collection and support Marine Genomics apprenticeships; Dr A. Highstein S. M., Holstein G. R., Mann M. A., Rabbitt R. D. (2014). Insights from Tlx expression in a ctenophore. As a result, there is little information about nervous organization in Ctenophora, and not a single transmitter has been reliably identified in representatives of this important phylum. It appears that the origin of major bilaterian groups occurred within a relatively short geological time (probably within 20 million years or even less). Expression of multiple sox genes through embryonic development in thectenophore. Acoelomorph flatworms are deuterostomes related to. Pennisi E., Society for Integrative and Comparative Biology Annual Meeting (2013). II. The gravity receptor, [Electronmicroscopic study of the gravity receptors in ctenophores]. These species are perfectly amenable to various experimental manipulations, including reliable fixation (most other ctenophores simply disintegrate in the majority of common fixatives), development, neurobiological and behavioral tests (Tamm, 1982; Tamm, 1984; Tamm and Moss, 1985), as well as molecular manipulations (Ali et al., 2010; Jager et al., 2008; Moroz et al., 2014). The results of Pleurobrachia whole-genome sequencing were formally reported at the SICB meeting in Charleston (SC) in January 2012 (Moroz et al., 2012), suggesting convergent evolution of ctenophore neural systems. Ctenophora have a diffuse ectodermal nervous system, which consists of a nerve net. Aboral side is located in the upper part of the photo. Ultrastructure of the giant smooth muscle fiber of the ctenophore. Cnidarians and ctenophores have nervous systems without a brain, whereas the bilaterians have a ventral nervous system and an anterior, dorsal brain . The hidden biology of sponges and comb jellies. Our surprising immunohistochemical finding of GABA accumulation in muscle cells (Fig. organisms with nervous systems). Wemmie J. Many original results referred to in this review were parts of the large-scale ctenophore genome/transcriptome projects reported in Nature doi:10.1038/nature13400. Nervous system and senses. King N., Westbrook M. J., Young S. L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., et al. Ctenophores have a relatively complicated nervous system consisting of a peripheral nerve net and the apical sensory organ used to sense gravity, and possibly light as well. Putnam N. H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V. V., et al. PDF The phylogenetic position of ctenophores and the origin(s) of nervous The postsynaptic density and active zones, however, are less prominent in ctenophore synapses. Convergent evolution of neural systems in ctenophores - PMC The origin of Metazoa: a transition from temporal to spatial cell differentiation, Origins. New insights on ctenophore neural anatomy: immunofluorescence study in. Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers, Die actinien anatomisch und histologisch mit besonderer Berucksichtigung des Nervenmuskelsystems untersucht, Die actinien anatomisch und histologisch mit besonderer bercksichtigung des nervenmuskelsystems untersucht. The two phyla were traditionally joined together in one group, termed Coelenterata, based on the presence of a single gastrovascular system serving both nutrient supply and gas exchange among the body parts. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Axon-like processes of epithelial cells in the aboral organ resemble neurons; a fact that might be used to support earlier hypotheses about the possible evolution of nerves from epithelial conduction tissue (Tamm and Tamm, 2002). Even in Mollusca, this centralization of the nervous system might occur 45 times in parallel (Kocot et al., 2011; Moroz, 2012). Chen J. Y., Bergstrom J., Lindstrom M., Hou X. G. (1991). Did the ctenophore nervous system evolve independently? No genes encoding enzymes for synthesis of acetylcholine (i.e. 6 ). Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. (A) l-glutamate (0.51 mmol l1) induced action potentials in mechanically isolated muscle cells whereas other transmitter candidates were ineffective even at concentrations up to 5 mmol l1. Since this structure serves both digestive and circulatory functions, it is known as a gastrovascular cavity. 2013 Society for Integrative and Comparative Biology Annual Meeting. The . The nervous elements of the mesoglea of beroids and cydippids (author's transl)], The nervous system of ctenophores. Nervous System - Ctenophora A similarly small genome size was reported for Mnemiopsis leidyi. The majority of described neuronal cell bodies and their processes form a polygonal lattice on the body surface known as a subepidermal nerve net (Fig. Furthermore, acetylcholine, classical catecholamines (dopamine, noradrenaline, adrenaline), serotonin and histamine were not detected in ctenophores using direct microchemical assays (Moroz et al., 2014).