Ctenophores Research Articles

Marine gelatinous zooplankton of the Egyptian waters: a review

Gelatinous plankton is formed by representatives of cnidarians (true jellyfish), ctenophores (comb jellies) and tunicates (salps). Gelatinous groups are a conspicuous, but relatively little studied component of marine ecosystems; in recent years its importance in pelagic food webs has gained increased awareness. They are essential components of the marine food web, relaying primary production from microbial algae to fish and seabirds. Gelatinous zooplankton may cause substantial mortality of fish eggs and larvae. This may play an important role in decreasing fishing stock of commercial fisheries, and they are an important variable in fisheries science and that it cannot be overlooked. The objective of this paper is to review a current knowledge on gelatinous zooplankton in the Egyptian waters of Mediterranean and Red Seas.

Cannibalism makes invasive comb jelly, Mnemiopsis leidyi, resilient to unfavourable conditions

The proliferation of invasive marine species is often explained by a lack of predators and opportunistic life history traits. For the invasive comb jelly Mnemiopsis leidyi, it has remained unclear how this now widely distributed species is able to overcome long periods of low food availability, particularly in their northernmost exotic habitats in Eurasia. Based on both field and laboratory evidence, we show that adult comb jellies in the western Baltic Sea continue building up their nutrient reserves after emptying the prey field through a shift to cannibalizing their own larvae. We argue, that by creating massive late summer blooms, the population can efficiently empty the prey field, outcompete intraguild competitors, and use the bloom events to build nutrient reserves for critical periods of prey scarcity. Our finding that cannibalism makes a species with typical opportunistic traits more resilient to environmental fluctuations is important for devising more effective conservation strategies.

Some comb jellies survive the winter by eating their young

Some comb jellies survive the winter by eating their young

Partitioning of diet between species and life history stages of sympatric and cryptic snappers (Lutjanidae) based on DNA metabarcoding

Lutjanus erythropterus and L. malabaricus are sympatric, sister taxa that are important to fisheries throughout the Indo-Pacific. Their juveniles are morphologically indistinguishable (i.e. cryptic). A DNA metabarcoding dietary study was undertaken to assess the diet composition and partitioning between the juvenile and adult life history stages of these two lutjanids. Major prey taxa were comprised of teleosts and crustaceans for all groups except adult L. erythropterus, which instead consumed soft bodied invertebrates (e.g. tunicates, comb jellies and medusae) as well as teleosts, with crustaceans being notably absent. Diet composition was significantly different among life history stages and species, which may be associated with niche habitat partitioning or differences in mouth morphology within adult life stages. This study provides the first evidence of diet partitioning between cryptic juveniles of overlapping lutjanid species, thus providing new insights into the ecological interactions, habitat associations, and the specialised adaptations required for the coexistence of closely related species. This study has improved our understanding of the differential contributions of the juvenile and adult diets of these sympatric species within food webs. The diet partitioning reported in this study was only revealed by the taxonomic resolution provided by the DNA metabarcoding approach and highlights the potential utility of this method to refine the dietary components of reef fishes more generally.

Microbiota Differences of the Comb Jelly Mnemiopsis leidyi in Native and Invasive Sub-Populations

The translocation of non-indigenous species around the world, especially in marine systems, is a matter of concern for biodiversity conservation and ecosystem functioning. While specific traits are often recognized to influence the success in the establishment of non-indigenous species, the impact of the associated microbial community for the fitness, performance and invasion success of basal marine metazoans remains vastly unknown. In this study, we compared bacterial composition patterns of the invasive ctenophore Mnemiopsis leidyi in different native and invasive sub-populations along with the genetic structure of the host (polymorphic microsatellite markers). Amplicon sequencing of the 16S rRNA gene (V1-V2 hypervariable regions) revealed that M. leidyi as representative of the phylum Ctenophora, the sister group to all metazoans, harbored a distinct microbiota compared to the ambient seawater, which significantly differed across two major tissues, namely epidermis and gastrodermis. Moreover, we identified significant differences in bacterial community compositions between native and invasive sub-populations of M. leidyi indicating, that the microbiota community is likely influenced by the genotypic background of the host.

CTENO64 Is Required for Coordinated Paddling of Ciliary Comb Plate in Ctenophores.

Ctenophores, or comb jellies, are one of the earliest branching basal metazoan groups, whose phylogenetic position continues to be controversial. They have eight rows of iridescent structures, called comb plates, which are huge multiciliated paddle-like structures used for locomotion and uniquely found in this group of animals [1]. Despite a number of morphological and physiological studies over the past 50 years, the molecular nature of comb plates remains completely unknown. Here, we identified a protein CTENO64 that is specifically localized in the comb plates. This protein is only found in ctenophores and not in other animals or eukaryotic species that possess multiciliary cells or tissues. It is localized to regions, called compartmenting lamella (CL), which are uniquely seen in ctenophore multicilia, connecting adjacent cilia in the comb plates. Knockdown of the CTENO64 gene did not affect the formation of comb plates but caused the loss or misformation of CLs and the disruption of ciliary orientation, resulting in aberrant and non-planar waveforms in the mid-distal region of the comb plates. We propose that CLs have been convergently acquired in ctenophores to overcome the hydrodynamic constraints of possessing extremely long multicilia. Our findings provide the initial step in unveiling the molecular structure and evolutionary significance of ciliary comb plates and shed light not only on the hidden biology of ctenophores but also on the unique evolutionary pathway of these animals. VIDEO ABSTRACT.

Combing Transcriptomes for Secrets of Deep-Sea Survival: Environmental Diversity Drives Patterns of Protein Evolution.

Ctenophores, also known as comb jellies, live across extremely broad ranges of temperature and hydrostatic pressure in the ocean. Because various ctenophore lineages adapted independently to similar environmental conditions, Phylum Ctenophora is an ideal system for the study of protein adaptation to extreme environments in a comparative framework. We present such a study here, using a phylogenetically-informed method to compare sequences of four essential metabolic enzymes across gradients of habitat depth and temperature. This method predicts convergent adaptation to these environmental parameters at the amino acid level, providing a novel view of protein adaptation to extreme environments and demonstrating the power and relevance of phylogenetic comparison applied to multi-species transcriptomic datasets from early-diverging metazoa. Across all four enzymes analyzed, 46 amino acid sites were associated with depth-adaptation, 59 with temperature-adaptation, and 56 with both. Sites predicted to be depth- and temperature-adaptive occurred consistently near Rossmann fold cofactor binding motifs and disproportionately in solvent-exposed regions of the protein. These results suggest that the hydrophobic effect and ligand binding may mediate efficient enzyme function at different hydrostatic pressures and temperatures. Using predicted adaptive site maps, such mechanistic hypotheses can now be tested via mutagenesis.

CTENO64 is Required for Coordinated Paddling of Ciliary Comb Plate in Ctenophores

Motile cilia are oscillating nanomachinery that are essential for cell locomotion and the generation of extracellular fluid flow. They typically comprise an axoneme with a 9+2 microtubule structure with dynein arms on each microtubule doublet that generate force by sliding between adjacent microtubules. These structures are efficient for motility and have therefore been conserved in cellular-level aquatic microflow throughout eukaryotic evolution. Diversity in the ciliary structures is seen in the basic microtubule arrangements but also in the bundling of multiple cilia, such as compound cilia. Studies on the structural diversity of cilia shed light on the mechanisms underlying ciliary formation and the biological adaptation to different aquatic environments. Ctenophores (comb jellies) have eight rows of iridescent comb plates that facilitate locomotion. A comb plate consists of tens of thousands of cilia to form a “puddle-like” ciliary plate with lengths of up to 1 mm. It exhibits structural color by light diffraction and is reported to have properties similar to photonic crystals. Here we identified a protein specific to the construction of comb plates (CTENO64). This protein is specifically present in ctenophore species and is localized on the compartmenting lamella (CL), which is the structure connecting adjacent cilia on the comb plates. Knockdown of the CTENO64 gene caused loss or misformation of CLs, resulting in aberrant waveforms in the comb plates. Our findings provide the initial characterization of a protein involved in the bundling of cilia into giant compound ciliary comb plates.

Cambrian Sessile, Suspension Feeding Stem-Group Ctenophores and Evolution of the Comb Jelly Body Plan

The origin of ctenophores (comb jellies) is obscured by their controversial phylogenetic position, with recent phylogenomic analyses resolving either sponges or ctenophores as the sister group of all other animals. Fossil taxa can provide morphological evidence that may elucidate the origins of derived characters and shared ancestries among divergent taxa, providing a means to "break" long branches in phylogenetic trees. Here we describe new fossil material from the early Cambrian Chengjiang Biota, Yunnan Province, China, including the putative cnidarian Xianguangia, the new taxon Daihua sanqiong gen et sp. nov., and Dinomischus venustus, informally referred to as "dinomischids" here. "Dinomischids" possess a basal calyx encircled by 18 tentacles that surround the mouth. The tentacles carry pinnules, each with a row of stiff filamentous structures interpreted as very large compound cilia of a size otherwise only known in ctenophores. Together with the Cambrian tulip animal Siphusauctum and the armored Cambrian scleroctenophores, they exhibit anatomies that trace ctenophores to a sessile, polypoid stem lineage. This body plan resembles the polypoid, tentaculate morphology of cnidarians, including a blind gastric cavity partitioned by mesenteries. We propose that comb rows are derived from tentacles with paired sets of pinnules that each bear a row of compound cilia. The scleroctenophores exhibit paired comb rows, also observed in Siphusauctum, in addition to an organic skeleton, shared as well by Dinomischus, Daihua, and Xianguangia. We formulate a hypothesis in which ctenophores evolved from sessile, polypoid suspension feeders, sharing similarities with cnidarians that suggest either a close relationship between these two phyla, a striking pattern of early convergent evolution, or an ancestral condition for either metazoans or eumetazoans.

Effects of pulsed magnetic fields on cilia of comb jelly

Marine comb jellies utilize cilia, arrays of bundled protein microtubules, for propulsion in water. Previous studies have reported on the orientation of the microtubules in steady electric and magnetic fields. Here, the effects of pulsed magnetic fields up to 2.2 Tesla on cilia fragments was investigated by examining changes in light scattering. Specifically, a comb jelly was placed in electromagnetic coils and illuminated with 472-nm laser light. Light scattering by isolated intact cilia was collected with an optical fiber and ported to a spectrophotometer. After pulsed magnetic field exposure, light scattered parallel to the field oscillated or decreased, depending on the initial cilia alignment with respect to the angle of the incident light. Changes in scattering were also detected for cilia that had been fixed with formalin and had no neural activity. Real-time observations indicated that they were caused by bending of cilia under induced electric fields, suggesting an electromechanical actuator in the comb jelly.

A ctenophore (comb jelly) employs vortex rebound dynamics and outperforms other gelatinous swimmers.

Gelatinous zooplankton exhibit a wide range of propulsive swimming modes. One of the most energetically efficient is the rowing behaviour exhibited by many species of schyphomedusae, which employ vortex interactions to achieve this result. Ctenophores (comb jellies) typically use a slow swimming, cilia-based mode of propulsion. However, species within the genus Ocyropsis have developed an additional propulsive strategy of rowing the lobes, which are normally used for feeding, in order to rapidly escape from predators. In this study, we used high-speed digital particle image velocimetry to examine the kinematics and fluid dynamics of this rarely studied propulsive mechanism. This mechanism allows Ocyropsis to achieve size-adjusted speeds that are nearly double those of other large gelatinous swimmers. The investigation of the fluid dynamic basis of this escape mode reveals novel vortex interactions that have not previously been described for other biological propulsion systems. The arrangement of vortices during escape swimming produces a similar configuration and impact as that of the well-studied ‘vortex rebound’ phenomenon which occurs when a vortex ring approaches a solid wall. These results extend our understanding of how animals use vortex–vortex interactions and provide important insights that can inform the bioinspired engineering of propulsion systems.

Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark photophores

Counterilluminating animals produce a ventral light to hide their silhouette in the water column. This midwater camouflage technique requires a fine and dynamic control of the wavelength, angular distribution, and intensity of their luminescence, which needs to continuously match ambient downwelling light. Recently, extraocular opsins have been suggested to play a role in the bioluminescence control of several organisms, such as squids, comb jellies, or brittle stars, providing a way for photogenic structures to perceive their own light output. By analysing a growing embryonic series of the velvet belly lanternshark, Etmopterus spinax, we show that the development of lanternshark luminescence competence is associated with the expression of encephalopsin within epidermal cells and in the light-regulating structure of the photogenic organs. Such an intra-uterine expression of encephalopsin strongly supports this blue-sensitive extraocular opsin to allow bioluminescence perception in lanternshark photophores and suggests a clear physiological interaction between photoemission and photoperception.

The gluey tentacles of comb jellies may have revealed when nerve cells first evolved

The gluey tentacles of comb jellies may have revealed when nerve cells first evolved

Catecholic Compounds in Ctenophore Colloblast and Nerve Net Proteins Suggest a Structural Role for DOPA-Like Molecules in an Early-Diverging Animal Lineage.

Ctenophores, or comb jellies, are among the earliest-diverging extant animal lineages. Several recent phylogenomic studies suggest that they may even be the sister group to all other animals. This unexpected finding remains difficult to contextualize, particularly given ctenophores' unique and sometimes poorly understood physiology. Colloblasts, a ctenophore-specific cell type found on the surface of these animals' tentacles, are emblematic of this difficulty. The exterior of the colloblast is dotted with granules that burst and release an adhesive on contact with prey, ensnaring it for consumption. To date, little is known about the fast-acting underwater adhesive that these cells secrete or its biochemistry. We present evidence that proteins in the colloblasts of the ctenophore Pleurobrachia bachei incorporate catecholic compounds similar to the amino acid l-3,4-dihydroxyphenylalanine. These compounds are associated with adhesive-containing granules on the surface of colloblasts, suggesting that they may play a role in prey capture, akin to dihydroxyphenylalanine-based adhesives in mussel byssus. We also present unexpected evidence of similar catecholic compounds in association with the subepithelial nerve net. There, catecholic compounds are present in spatial patterns similar to those of l-3,4-dihydroxyphenylalanine and its derivatives in cnidarian nerves, where they are associated with membranes and possess unknown functionality. This "structural" use of catecholic molecules in ctenophores represents the earliest-diverging animal lineage in which this trait has been observed, though it remains unclear whether structural catechols are deeply rooted in animals or whether they have arisen multiple times.

Friday briefing: To really understand animals, embrace the ctenophores, the sponges and the placozoans

Friday briefing: To really understand animals, embrace the ctenophores, the sponges and the placozoans

Integrating Embryonic Development and Evolutionary History to Characterize Tentacle-Specific Cell Types in a Ctenophore.

The origin of novel traits can promote expansion into new niches and drive speciation. Ctenophores (comb jellies) are unified by their possession of a novel cell type: the colloblast, an adhesive cell found only in the tentacles. Although colloblast-laden tentacles are fundamental for prey capture among ctenophores, some species have tentacles lacking colloblasts and others have lost their tentacles completely. We used transcriptomes from 36 ctenophore species to identify gene losses that occurred specifically in lineages lacking colloblasts and tentacles. We cross-referenced these colloblast- and tentacle-specific candidate genes with temporal RNA-Seq during embryogenesis in Mnemiopsis leidyi and found that both sets of candidates are preferentially expressed during tentacle morphogenesis. We also demonstrate significant upregulation of candidates from both data sets in the tentacle bulb of adults. Both sets of candidates were enriched for an N-terminal signal peptide and protein domains associated with secretion; among tentacle candidates we also identified orthologs of cnidarian toxin proteins, presenting tantalizing evidence that ctenophore tentacles may secrete toxins along with their adhesive. Finally, using cell lineage tracing, we demonstrate that colloblasts and neurons share a common progenitor, suggesting the evolution of colloblasts involved co-option of a neurosecretory gene regulatory network. Together these data offer an initial glimpse into the genetic architecture underlying ctenophore cell-type diversity.

Early metazoan cell type diversity and the evolution of multicellular gene regulation.

A hallmark of metazoan evolution is the emergence of genomic mechanisms that implement cell type-specific functions. However, the evolution of metazoan cell types and their underlying gene regulatory programs remain largely uncharacterized. Here, we use whole-organism single-cell RNA-seq to map cell type-specific transcription in Porifera (sponges), Ctenophora (comb jellies) and Placozoa species. We describe the repertoires of cell types in these non-bilaterian animals, uncovering diverse instances of previously unknown molecular signatures, such as multiple types of peptidergic cells in Placozoa. Analysis of the regulatory programs of these cell types reveal variable levels of complexity. In placozoans and poriferans, sequence motifs in the promoters are predictive of cell type-specific programs. In contrast, the generation of a higher diversity of cell types in ctenophores is associated to lower specificity of promoter sequences and to the existence of distal regulatory elements. Our findings demonstrate that metazoan cell types can be defined by networks of TFs and proximal promoters, and indicate that further genome regulatory complexity may be required for more diverse cell type repertoires.

Extensive mitochondrial gene rearrangements in Ctenophora: insights from benthic Platyctenida

BackgroundComplete mitochondrial (mt) genomes have been sequenced for thousands of animals and represent a molecule of choice for many evolutionary studies. Nevertheless, some animal groups have remained under-sampled. Ctenophora (comb jellies) is one such example, with only two complete mt sequences determined hitherto for this phylum, which encompasses ca. 150–200 described species. This lack of data derives from the extremely fast mt evolutionary rate in this lineage, complicating primer design and DNA amplification. Indeed, in the two ctenophore mt genomes sequenced to date, i.e. those of Mnemiopsis leidyi (order Lobata) and Pleurobrachia bachei (order Cydippida), both rRNA and protein coding genes exhibit an extraordinary size reduction and have highly derived sequences. Additionally, all tRNAs, and the atp6 and atp8 genes are absent. In order to determine whether these characteristics are shared by other ctenophores, we obtained the complete mt genomes of three benthic ctenophores belonging to the so far unsampled order of Platyctenida: Coeloplana loyai, Coeloplana yulianicorum and Vallicula multiformis.ResultsThe mt genomes of benthic ctenophores reveal the same peculiarities found in Mnemiopsis and Pleurobrachia, demonstrating that the fast evolutionary rate is a general trait of the ctenophore mt genomes. Our results also indicate that this high evolutionary rate not only affects the nucleotide substitution but also gene rearrangements. Indeed, gene order was highly rearranged among representatives of the different taxonomic orders in which it was close to random, but also quite variable within Platyctenida, in which the genera Coeloplana and Vallicula share only four conserved synteny blocks. However, the two congeneric Coeloplana species display exactly the same gene order. Because of the extreme evolutionary rate, our phylogenetic analyses were unable to resolve the phylogenetic position of ctenophores within metazoans or the relationships among the different Ctenophora orders. Comparative sequence-analyses allowed us to correct the annotation of the Pleurobrachia mt genome, confirming the absence of tRNAs, the presence of both rRNA genes, and the existence of a reassignment of codon TGA from tryptophan to serine for this species.ConclusionsSince Platyctenida is an early diverging lineage among Ctenophora, our findings suggest that the mt traits described above are ancestral characteristics of this phylum.

Dispersal and speciation: The cross Atlantic relationship of two parasitic cnidarians

How dispersal strategies impact the distribution of species and subsequent speciation events is a fundamental question in evolutionary biology. Sedentary benthic marine organisms, such as corals or sea anemones usually rely on motile larval stages for dispersal and therefore have a relatively restricted distribution along coasts. Edwardsiella lineata and Edwardsiella carnea are virtually indistinguishable edwardsiid sea anemones native to the east American and the Northern European coast, respectively. E. lineata is a facultative parasite to the ctenophore Mnemiopsis leidyi, while the life cycle of E. carnea is unknown. Recently M. leidyi was found in the Skagerrak carrying Edwardsiella sp. parasites, which raised the intriguing possibility that the invasive comb jellies acted as cargo for the facultative E. lineata parasites to establish a new population in Northern Europe. Here, we assessed the genetic differences between these two cryptic Edwardsiella species and isolated parasites from the invasive comb jelly M. leidyi in Sweden by comparing rRNA, whole transcriptomes, SNPs, ITS2 sequences and the gene complements of key developmental regulators, the Wnt gene family. We show that E. carnea and the parasite transcriptomes are more than 99% identical, hence demonstrating that E. carnea has a previously unknown parasitic life stage. ITS2 sequence analysis of E. carnea and E. lineata suggest that they may not be reproductively isolated. The transcriptomes of E. lineata and E. carnea are ∼97% identical. We also estimate that the species diverged between 18.7 and 21.6 million years ago.

Comparative Genomics of the Zic Family Genes.

Zic family genes encode five C2H2-type zinc finger domain-containing proteins that have many roles in animal development and maintenance. Recent phylogenetic analyses showed that Zic family genes are distributed in metazoans (multicellular animals), except Porifera (sponges) and Ctenophora (comb jellies). The sequence comparisons revealed that the zinc finger domains were absolutely conserved among the Zic family genes. Zic zinc finger domains are similar to, but distinct from those of the Gli, Glis, and Nkl gene family, and these zinc finger protein families are proposed to have been derived from a common ancestor gene. The Gli-Glis-Nkl-Zic superfamily and some other eukaryotic zinc finger proteins share a tandem CWCH2 (tCWCH2) motif, a hallmark for inter-zinc finger interaction between two adjacent C2H2 zinc fingers. In Zic family proteins, there exist additional evolutionally conserved domains known as ZOC and ZFNC, both of which may have appeared before cnidarian-bilaterian divergence. Comparison of the exon-intron boundaries in the Zic zinc finger domains revealed an intron (A-intron) that was absolutely conserved in bilaterians (metazoans with bilateral symmetry) and a placozoan (a simple nonparasitic metazoan). In vertebrates, there are five to seven Zic paralogs among which Zic1, Zic2, and Zic3 are generated through a tandem gene duplication and carboxy-terminal truncation in a vertebrate common ancestor, sharing a conserved carboxy-terminal sequence. Several hypotheses have been proposed to explain the Zic family phylogeny, including their origin, unique features in the first and second zinc finger motif, evolution of the nuclear localization signal, significance of the animal taxa-selective degeneration, gene multiplication in the vertebrate lineage, and involvement in the evolutionary alteration of the animal body plan.