A chromosome-scale genome assembly and karyotype of the ctenophore Hormiphora californensis

Here, we present a karyotype, a chromosome-scale genome assembly, and a genome annotation from the ctenophore Hormiphora californensis (Ctenophora: Cydippida: Pleurobrachiidae). The assembly spans 110 Mb in 44 scaffolds and 99.47% of the bases are contained in 13 scaffolds. Chromosome micrographs and Hi-C heatmaps support a karyotype of 13 diploid chromosomes. Hi-C data reveal three large heterozygous inversions on chromosome 1, and one heterozygous inversion shares the same gene order found in the genome of the ctenophore Pleurobrachia bachei. We find evidence that H. californensis and P. bachei share thirteen homologous chromosomes, and the same karyotype of 1n = 13. The manually curated PacBio Iso-Seq-based genome annotation reveals complex gene structures, including nested genes and trans-spliced leader sequences. This chromosome-scale assembly is a useful resource for ctenophore biology and will aid future studies of metazoan evolution and phylogenetics.

Colloblasts act as a biomechanical sensor for suitable prey in Pleurobrachia

Ctenophores are a group of largely-planktonic, gelatinous carnivores whose most common method of prey capture is nearly a phylum-defining trait. Tentaculate ctenophores release an unknown proteinaceous adhesive from specialized colloblast cells lining their tentacles following prey contact with the tentacles. There exist no extant studies of the mechanical properties of colloblast adhesive. We use live microscopy techniques to visualize adhesion events between Pleurobrachia pileus colloblasts and probes of different surface chemistries in response to probing with varying contact areas. We further define two mechanisms of adhesion termination upon probe retraction. Adapting a technique for measuring surface tension, we examine the adhesive strength of tentacles in the ctenophore Pleurobrachia bachei under varying pH and bonding time conditions, and demonstrate the destructive exhaustion of colloblast adhesive release. We find that colloblast-mediated adhesion is rapid, and that the bonding process is robust against shifts in ambient pH. However, we find that the Pleurobrachia colloblast adhesive system is among the weakest biological adhesive systems yet described. We place this surprising observation into a broader ecophysiological context by modeling prey capture for prey of a range of sizes. We find that limited use of colloblast adhesive with high surface area contact is suitable both for capturing appropriately sized prey and rejecting, by detachment, prey above a certain size threshold. This allows Pleuro-brachia, lacking a mechanism to directly “see” potential prey they are interacting with, to invest in capturing only prey of an appropriate size, decreasing the risk of injury.Summary statementCtenophore colloblast adhesive is found to be strong, but few colloblasts are simultaneously active, producing a weakly-adhering system. A physical model demonstrates how such a system may filter unsuitable prey.

Atlas of Neuromuscular Organization in the Ctenophore, Pleurobrachia bachei (A. Agassiz, 1860)

Enigmatic ctenophores are descendants of one of the earliest branching metazoan lineage. Their nervous systems are equally elusive. The lack of convenient neurogenic molecules and neurotransmitters suggests an extensive parallel evolution and independent origins of neurons and synapses. However, the field is logged behind due to the lack of microanatomical data about the neuro-muscular systems in this group of animals. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of both muscular and nervous systems in the sea gooseberry, Pleurobrachia bachei, from North Pacific. The diffused neural system of Pleurobrachia consists of two subsystems: the subepithelial neural network and the mesogleal net with about 5000-7000 neurons combined. Our data revealed the unprecedented complexity of neuromuscular organization in this basal metazoan lineage. The anatomical diversity of cell types includes at least nine broad categories of neurons, five families of surface receptors and more than two dozen types of muscle cells as well as regional concentrations of neuronal elements to support ctenophore feeding, complex swimming, escape and prey capture behaviors. In summary, we recognize more than 80 total morphological cell types. Thus, in terms of cell type specification and diversity, ctenophores significantly exceed what we currently know about other prebilaterian groups (placozoan, sponges, and cnidarians), and some basal bilaterians.

Polymorphism within the mitochondrial genome of the ctenophore, Pleurobrachia bachei and its ongoing rapid evolution

The mitochondrial genomes in ctenophores are among the most compact in the animal kingdom with multiple rearrangements and examples of gene loss. Here, by resequencing of the Pleurobrachia bachei mitochondrial genome, we show that the high level of polymorphism (>10%) in Pleurobrachia might contribute to the ongoing fast evolution of ctenophores including the presence of truncated versions of apparently canonical genes such as cox1. Second, the codon interpretations in ctenophores, without robust proteomic data related to mitochondrial genes, is still a challenging issue, which is open for future experimental analyses.

The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi

Ctenophores are important members of planktonic communities that are often abundant in dysaerobic environments. Previous studies have shown that ctenophores are not adversely affected by extended periods of hypoxia. The three species used in this study, Pleurobrachia bachei, Bolinopsis infundibulum, and Mnemiopsis leidyi, were all able to oxyregulate to very low partial pressures of oxygen (PO2s). These species were found to have mean critical oxygen tensions of 7.7, 10.6, and 7.2 hPa respectively. In general, ctenophores are better oxyregulators than medusae and many species of shrimps, fish and squid. Intragel oxygen was measured using a fibre optic oxygen optode. All these ctenophores have intragel subsurface [O2]s of 5–10% below that of the surrounding seawater. Intragel oxygen measurements of P. bachei showed a gradient of decreasing PO2 from surface tissues to the gut. Specimens of P. bachei over 14 mm in diameter had anaerobic guts. Survival times in anoxia ranged from 0 h for M. leidyi to up to 6 h for P. bachei. Ctenophores rely on aerobic metabolism to tolerate hypoxia.