Ctenophores Research Articles

Rapid physiological integration of fused ctenophores

The mechanisms by which organisms recognize the 'self' from the 'non-self' remain poorly understood. Moreover, the capability of transplanted tissue to functionally integrate is unclear in many organisms. Here, we report that two injured Mnemiopsis leidyi individuals, a species of planktonic animals known as comb jellies or ctenophores, are capable of rapidly fusing into a single entity in which some physiological functions are integrated. Our results highlight two interesting phenomena. First, ctenophores may lack an allorecognition mechanism that prevents fusion events between conspecifics. Second, fused individuals rapidly integrate and share physiological functions and neurobehavioral outputs. Ctenophores are among the earliest-branching animal groups of extant metazoans1 and possess a unique nervous system with enigmatic homology to other phyla2. Our observations warrant further research into understanding the evolution of self-nonself recognition systems and the functional integration of neuronal structures in ctenophores.

Deep Strength: Why comb jellies withstand crushing depths but melt away on land.

Deep Strength: Why comb jellies withstand crushing depths but melt away on land.

Redescription of the deep-sea benthic ctenophore genus Tjalfiella from the North Atlantic (Class Tentaculata, Order Platyctenida, Family Tjalfiellidae)

Some of the most fascinating and poorly known animals on this planet are comb jellies of the phylum Ctenophora. About one-quarter of ctenophore richness is encompassed by the benthic species of the order Platyctenida, nearly all known from shallow waters. In this work, we integrate several systematic methods to elucidate an enigmatic genus, Tjalfiella, known previously only from deep waters near the western coastline of Greenland in the North Atlantic. For the first time, we employ microCT on museum specimens—one nearly 100 years old from the type locality of the only known species of the genus, T. tristoma—of extant ctenophores to visualize and compare their anatomy. With these data, we integrate in situ videography and genetic sequence data derived from newly collected deep sea specimens observed via NOAA Ship Okeanos Explorer in 2018 and 2022 at two distant localities in the North Atlantic, near North Carolina, USA, and the Azores, Portugal. The genetic data indicate that the newly collected specimens represent closely related but distinct species of Tjalfiella. However, neither can be named at this time because neither one could be definitively differentiated from T. tristoma, given that microCT and in situ imagery reveal striking morphological similarities and only variation in color and host preference. Despite the lack of new species descriptions, this work characterizes both the morphology and genetics of the benthic ctenophore genus Tjalfiella and specimens representing species within it, advancing our understanding of a rarely observed component of the deep-sea fauna.

Deep-sea comb jellies’ cells are primed to withstand pressure

Deep-sea comb jellies’ cells are primed to withstand pressure

Homeocurvature adaptation of phospholipids to pressure in deep-sea invertebrates.

Hydrostatic pressure increases with depth in the ocean, but little is known about the molecular bases of biological pressure tolerance. We describe a mode of pressure adaptation in comb jellies (ctenophores) that also constrains these animals' depth range. Structural analysis of deep-sea ctenophore lipids shows that they form a nonbilayer phase at pressures under which the phase is not typically stable. Lipidomics and all-atom simulations identified phospholipids with strong negative spontaneous curvature, including plasmalogens, as a hallmark of deep-adapted membranes that causes this phase behavior. Synthesis of plasmalogens enhanced pressure tolerance in Escherichia coli, whereas low-curvature lipids had the opposite effect. Imaging of ctenophore tissues indicated that the disintegration of deep-sea animals when decompressed could be driven by a phase transition in their phospholipid membranes.

Morphological and dietary changes encoded in the genome of Beroe ovata, a ctenophore-eating ctenophore.

As the sister group to all other animals, ctenophores (comb jellies) are important for understanding the emergence and diversification of numerous animal traits. Efforts to explore the evolutionary processes that promoted diversification within Ctenophora are hindered by undersampling genomic diversity within this clade. To address this gap, we present the sequence, assembly and initial annotation of the genome of Beroe ovata. Beroe possess unique morphology, behavior, ecology and development. Unlike their generalist carnivorous kin, beroid ctenophores feed exclusively on other ctenophores. Accordingly, our analyses revealed a loss of chitinase, an enzyme critical for the digestion of most non-ctenophore prey, but superfluous for ctenophorivores. Broadly, our genomic analysis revealed that extensive gene loss and changes in gene regulation have shaped the unique biology of B. ovata. Despite the gene losses in B. ovata, our phylogenetic analyses on photosensitive opsins and several early developmental regulatory genes show that these genes are conserved in B. ovata. This additional sampling contributes to a more complete reconstruction of the ctenophore ancestor and points to the need for extensive comparisons within this ancient and diverse clade of animals. To promote further exploration of these data, we present BovaDB (http://ryanlab.whitney.ufl.edu/bovadb/), a portal for the B. ovata genome.

Evolutionary origin of the nervous system from Ctenophora prospective.

Nervous system is one of the key adaptations underlying the evolutionary success of the majority of animal groups. Ctenophores (or comb jellies) are gelatinous marine invertebrates that were probably the first lineage to diverge from the rest of animals. Due to the key phylogenetic position and multiple unique adaptations, the noncentralized nervous system of comb jellies has been in the center of the debate around the origin of the nervous system in the animal kingdom and whether it happened only once or twice. Here, we discuss the latest findings in ctenophore neuroscience and multiple challenges on the way to build a clear evolutionary picture of the origin of the nervous system.

Phylogenetic and functional analyses of Comb Jelly Shaker K+ channels reveal independent evolution of voltage-gated K+ channel diversity

Phylogenetic and functional analyses of Comb Jelly Shaker K+ channels reveal independent evolution of voltage-gated K+ channel diversity

The Choanocyte Cells from Phylum Porifera, Nematocysts Cells from Phylun Cnidaria and Colloblast Cells from Ctenophora like Analogues Structures

There are three basic structures belongs to Phylum Porifera, Phylum Cnidaria and Phylum Ctenophora very important because they have similar function like to catch food, but three of them have different origin and different structuration too. They are knowing like choanocyte (Porifera), nematocysts (Cnidaria) and colloblast (Ctenophora) so they are considered analogue structures and they have different positions in the animal; meanwhile the first one are localized in the general cavity (asconoid form, leuconoid form) of sponge, the second one are localized in different zones of the animal like tentacles, acontium , verrucae , vesicule, acrorargus and the last one is on tentacles.

Illustrated Neuroanatomy of Ctenophores: Immunohistochemistry.

Ctenophores or comb jellies are representatives of an enigmatic lineage of early branching metazoans with complex tissue and organ organization. Their biology and even microanatomy are not well known for most of these fragile pelagic and deep-water species. Here, we present immunohistochemical protocols successfully tested on more than a dozen ctenophores. This chapter also illustrates neural organization in several reference species of the phylum (Pleurobrachia bachei, P. pileus, Mnemiopsis leidyi, Bolinopsis microptera, Beroe ovata, and B. abyssicola) as well as numerous ciliated structures in different functional systems. The applications of these protocols illuminate a very complex diversification of cell types comparable to many bilaterian lineages.

Scanning Electron Microscopy of Ctenophores: Illustrative Atlas.

Scanning electron microscopy (SEM) is a powerful tool for ultrastructural analyses of biological specimens at their surface. With comb jellies being very soft and full of water, many methodological difficulties limit their microanatomical studies via SEM. Here, we describe SEM protocols and approaches successfully tested on ctenophores Pleurobrachia bachei and Beroe abyssicola. Our SEM investigation revealed the astonishing diversity of ciliated structures in all major functional systems, different receptor types, and complex muscular architecture. These protocols can also be practical for various basal bilaterian lineages such as cnidarians.

DNA Isolation Long-Read Genomic Sequencing in Ctenophores.

Long-read sequencing has proven the necessity for high-quality genomic assemblies of reference species, including enigmatic ctenophores. Obtaining high-molecular-weight genomic DNA is pivotal to this process and has proven highly problematic for many species. Here, we discuss different methodologies for gDNA isolation and present a protocol for isolating gDNA for several members of the phylum Ctenophora. Specifically, we describe a Pacific Biosciences library construction method used in conjunction with gDNA isolation methods that have proven successful in obtaining high-quality genomic assemblies in ctenophores.

Ctenophora: Illustrated Guide and Taxonomy.

Ctenophores or comb jellies represent the first diverging lineage of extant animals - sister to all other Metazoa. As a result, they occupy a unique place in the biological sciences. Despite their importance, this diverse group of marine predators has remained relatively poorly known, with both the species and higher-level taxonomy of the phylum in need of attention. We present a checklist of the phylum based on a review of the current taxonomic literature and illustrate their diversity with images. The current classification presented remains substantially in conflict with recent phylogenetic results, and many of the taxa are not monophyletic or untested. This chapter summarizes the existing classification focusing on recognized families and genera with 185 currently accepted, extant species listed. We provide illustrative examples of ctenophore diversity covering all but one of the 33 families and 47 of the 48 genera, as well as about 25-30 undescribed species. We also list the 14 recognized ctenophore fossil species and note others that have been controversially attributed to the phylum. Analyses of unique ctenophore adaptations are critical to understanding early animal evolution and adaptive radiation of this clade of basal metazoans.

Bioluminescence of ctenophore Pleurobrachia pileus (O.F. Muller, 1776) in the summer period

The capability of bioluminescence has been found in many marine hydrobionts, including almost all representatives of the phylum Ctenophora. The glow of species and bioluminescent substrates isolated from them is actively used in biology, ecology, and medicine to study the physiological state of an organism or to identify unfavorable environmental parameters. The parameters of luminescence of the Black Sea ctenophores Mne-miopsis leidyi A. Agassiz, 1865 (Lobata) and Berce ovata Bruguicre, 1789 (Beroida) are used to study the effects of toxicants, such as liquid hydrocarbons, PCBs, and heavy metals. Some researchers casted doubt on the capability of the Black Sea autochthonous inhabitant, ctenophore Pleurobrachia pileus (O. F Muller, 1776) to produce bioluminescent light. The objective of this work was to ensure scientific support for the light-producing ability of species under study and to choose the optimal time for conducting experiments on the factors that affect bioluminescence. It was found that mechanical and chemical stimulation triggered a bioluminescent response in all size groups of species under study at any time of day. Upon chemical stimulation of the studied species, the signal energy value was several times greater than that observed after mechanical stimulation. It was revealed that the optimal time interval for conducting biophysical research is the time from 8 pm to 6 am, because the values of luminescence activity are the greatest in this time interval within a day.

Ancient gene linkages support ctenophores as sister to other animals

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1–6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7–11. Here we develop chromosome-scale gene linkage, also known as synteny, as a phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba and an ichthyosporean) that serve as outgroups for phylogenetic analysis. We find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns, whereas sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.

Comb jellies, not sponges, might be the oldest animal group

Comb jellies, not sponges, might be the oldest animal group

Independent Innexin Radiation Shaped Signaling in Ctenophores.

Innexins facilitate cell-cell communication by forming gap junctions or nonjunctional hemichannels, which play important roles in metabolic, chemical, ionic, and electrical coupling. The lack of knowledge regarding the evolution and role of these channels in ctenophores (comb jellies), the likely sister group to the rest of animals, represents a substantial gap in our understanding of the evolution of intercellular communication in animals. Here, we identify and phylogenetically characterize the complete set of innexins of four ctenophores: Mnemiopsis leidyi, Hormiphora californensis, Pleurobrachia bachei, and Beroe ovata. Our phylogenetic analyses suggest that ctenophore innexins diversified independently from those of other animals and were established early in the emergence of ctenophores. We identified a four-innexin genomic cluster, which was present in the last common ancestor of these four species and has been largely maintained in these lineages. Evidence from correlated spatial and temporal gene expression of the M. leidyi innexin cluster suggests that this cluster has been maintained due to constraints related to gene regulation. We describe the basic electrophysiological properties of putative ctenophore hemichannels from muscle cells using intracellular recording techniques, showing substantial overlap with the properties of bilaterian innexin channels. Together, our results suggest that the last common ancestor of animals had gap junctional channels also capable of forming functional innexin hemichannels, and that innexin genes have independently evolved in major lineages throughout Metazoa.

Improving Orthologous Signal and Model Fit in Datasets Addressing the Root of the Animal Phylogeny.

There is conflicting evidence as to whether Porifera (sponges) or Ctenophora (comb jellies) comprise the root of the animal phylogeny. Support for either a Porifera-sister or Ctenophore-sister tree has been extensively examined in the context of model selection, taxon sampling, and outgroup selection. The influence of dataset construction is comparatively understudied. We re-examine five animal phylogeny datasets that have supported either root hypothesis using an approach designed to enrich orthologous signal in phylogenomic datasets. We find that many component orthogroups in animal datasets fail to recover major lineages as monophyletic with the exception of Ctenophora, regardless of the supported root. Enriching these datasets to retain orthogroups recovering ≥3 major lineages reduces dataset size by up to 50% while retaining underlying phylogenetic information and taxon sampling. Site-heterogeneous phylogenomic analysis of these enriched datasets recovers both Porifera-sister and Ctenophora-sister positions, even with additional constraints on outgroup sampling. Two datasets which previously supported Ctenophora-sister support Porifera-sister upon enrichment. All enriched datasets display improved model fitness under posterior predictive analysis. While not conclusively rooting animals at either Porifera or Ctenophora, we do see an increase in signal for Porifera-sister and a decrease in signal for Ctenophore-sister when data are filtered for orthologous signal. Our results indicate that dataset size and construction as well as model fit influence animal root inference.

Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans).

How to make a neuron, a synapse, and a neural circuit? Is there only one 'design' for a neural architecture with a universally shared genomic blueprint across species? The brief answer is "No." Four early divergent lineages from the nerveless common ancestor of all animals independently evolved distinct neuroid-type integrative systems. One of these is a subset of neural nets in comb jellies with unique synapses; the second lineage is the well-known Cnidaria + Bilateria; the two others are non-synaptic neuroid systems in sponges and placozoans. By integrating scRNA-seq and microscopy data, we revise the definition of neurons as synaptically-coupled polarized and highly heterogenous secretory cells at the top of behavioral hierarchies with learning capabilities. This physiological (not phylogenetic) definition separates 'true' neurons from non-synaptically and gap junction-coupled integrative systems executing more stereotyped behaviors. Growing evidence supports the hypothesis of multiple origins of neurons and synapses. Thus, many non-bilaterian and bilaterian neuronal classes, circuits or systems are considered functional rather than genetic categories, composed of non-homologous cell types. In summary, little-explored examples of convergent neuronal evolution in representatives of early branching metazoans provide conceptually novel microanatomical and physiological architectures of behavioral controls in animals with prospects of neuro-engineering and synthetic biology.

Phylogenomics and the first higher taxonomy of Placozoa, an ancient and enigmatic animal phylum

Placozoa is an ancient phylum of extraordinarily unusual animals: miniscule, ameboid creatures that lack most fundamental animal features. Despite high genetic diversity, only recently have the second and third species been named. While prior genomic studies suffer from incomplete placozoan taxon sampling, we more than double the count with protein sequences from seven key genomes and produce the first nuclear phylogenomic reconstruction of all major placozoan lineages. This leads us to the first complete Linnaean taxonomic classification of Placozoa, over a century after its discovery: This may be the only time in the 21st century when an entire higher taxonomy for a whole animal phylum is formalized. Our classification establishes 2 new classes, 4 new orders, 3 new families, 1 new genus, and 1 new species, namely classes Polyplacotomia and Uniplacotomia; orders Polyplacotomea, Trichoplacea, Cladhexea, and Hoilungea; families Polyplacotomidae, Cladtertiidae, and Hoilungidae; and genus Cladtertia with species Cladtertia collaboinventa, nov. Our likelihood and gene content tree topologies refine the relationships determined in previous studies. Adding morphological data into our phylogenomic matrices suggests sponges (Porifera) as the sister to other animals, indicating that modest data addition shifts this node away from comb jellies (Ctenophora). Furthermore, by adding the first genomic protein data of the exceptionally distinct and branching Polyplacotoma mediterranea, we solidify its position as sister to all other placozoans; a divergence we estimate to be over 400 million years old. Yet even this deep split sits on a long branch to other animals, suggesting a bottleneck event followed by diversification. Ancestral state reconstructions indicate large shifts in gene content within Placozoa, with Hoilungia hongkongensis and its closest relatives having the most unique genetics.