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Abstract The third iteration of the Cnidarian Model Systems Meeting (Cnidofest) was held August 14–17th, 2024 at Lehigh University in Bethlehem, PA. The meeting featured presentations from laboratories representing 11 countries, covering a broad range of topics related to cnidarian species. The research highlighted diverse topics, with sessions focused on regeneration, evo-devo, genomics, symbiosis, cell biology, physiology, neurobiology, and development. A notable shift at this meeting was the extent to which established cnidarian model systems have caught up with the classical laboratory models such asDrosophilaand vertebrates, with modern genomic, genetic, and molecular tools now routinely applied. In addition, more cnidarian systems are now being developed for functional studies by the community, enhancing our ability to gain fundamental insights into animal biology that are otherwise difficult in the complex bilaterian model systems. Together, the integration of cnidarian and bilaterian model systems provides researchers with a broader toolkit for selecting animal models best suited to address their specific biological questions. 

Abstract Adult pluripotent stem cells are found in diverse animals, including cnidarians, acoels, and planarians, and confer remarkable abilities such as whole-body regeneration. The mechanisms by which these pluripotent stem cells orchestrate the replacement of all lost cell types, however, remains poorly understood. Underlying heterogeneity within the stem cell populations of these animals is often obscured when focusing on certain tissue types or life history stages, which tend to have indistinguishable spatial expression patterns of stem cell marker genes. Here, we focus on the adult pluripotent stem cells (i-cells) ofHydractinia symbiolongicarpus, a colonial marine cnidarian with distinct polyp types and stolonal tissue. Recently, a single-cell expression atlas was generated forH. symbiolongicarpuswhich revealed two distinct clusters with i-cell signatures, potentially representing heterogeneity within this species’ stem cell population. Considering this finding, we investigated eight new putative stem cell marker genes from the atlas including five expressed in both i-cell clusters (Pcna,Nop58,Mcm4,Ubr7, andUhrf1) and three expressed in one cluster or the other (Pter, FoxQ2-like,andZcwpw1). We characterized their expression patterns in various contexts–feeding and sexual polyps, juvenile feeding polyps, stolon, and during feeding polyp head regeneration–revealing context-dependent gene expression patterns and a transcriptionally dynamic i-cell population. We uncover previously unknown differences within the i-cell population ofHydractiniaand demonstrate that its colonial nature serves as an excellent system for investigating and visualizing heterogeneity in pluripotent stem cells. 

Abstract The second annual Cnidarian Model Systems Meeting, aka “Cnidofest”, took place in Davis, California from 7 to 10th of September, 2022. The meeting brought together scientists using cnidarians to study molecular and cellular biology, development and regeneration, evo-devo, neurobiology, symbiosis, physiology, and comparative genomics. The diversity of topics and species represented in presentations highlighted the importance and versatility of cnidarians in addressing a wide variety of biological questions. In keeping with the spirit of the first meeting (and its predecessor, Hydroidfest), almost 75% of oral presentations were given by early career researchers (i.e., graduate students and postdocs). In this review, we present research highlights from the meeting. 

Nucleostemin ( NS ) is a vertebrate gene preferentially expressed in stem and cancer cells, which acts to regulate cell cycle progression, genome stability and ribosome biogenesis. NS and its paralogous gene, GNL3-like ( GNL3L ), arose in the vertebrate clade after a duplication event from their orthologous gene, G protein Nucleolar 3 ( GNL3 ). Research on invertebrate GNL3 , however, has been limited. To gain a greater understanding of the evolution and functions of the GNL3 gene, we have performed studies in the hydrozoan cnidarian Hydractinia symbiolongicarpus , a colonial hydroid that continuously generates pluripotent stem cells throughout its life cycle and presents impressive regenerative abilities. We show that Hydractinia GNL3 is expressed in stem and germline cells. The knockdown of GNL3 reduces the number of mitotic and S-phase cells in Hydractinia larvae of different ages. Genome editing of Hydractinia GNL3 via CRISPR/Cas9 resulted in colonies with reduced growth rates, polyps with impaired regeneration capabilities, gonadal morphological defects, and low sperm motility. Collectively, our study shows that GNL3 is an evolutionarily conserved stem cell and germline gene involved in cell proliferation, animal growth, regeneration and sexual reproduction in Hydractinia , and sheds new light into the evolution of GNL3 and of stem cell systems. 

Abstract BackgroundSex determination occurs across animal species, but most of our knowledge about its mechanisms comes from only a handful of bilaterian taxa. This limits our ability to infer the evolutionary history of sex determination within animals. ResultsIn this study, we generated a linkage map of the genome of the colonial cnidarianHydractinia symbiolongicarpusand used it to demonstrate that this species has an XX/XY sex determination system. We demonstrate that the X and Y chromosomes have pseudoautosomal and non-recombining regions. We then use the linkage map and a method based on the depth of sequencing coverage to identify genes encoded in the non-recombining region and show that many of them have male gonad-specific expression. In addition, we demonstrate that recombination rates are enhanced in the female genome and that the haploid chromosome number inHydractiniaisn = 15. ConclusionsThese findings establishHydractiniaas a tractable non-bilaterian model system for the study of sex determination and the evolution of sex chromosomes. 

Hydractiniais a colonial marine hydroid that shows remarkable biological properties, including the capacity to regenerate its entire body throughout its lifetime, a process made possible by its adult migratory stem cells, known as i-cells. Here, we provide an in-depth characterization of the genomic structure and gene content of twoHydractiniaspecies,Hydractinia symbiolongicarpusandHydractinia echinata, placing them in a comparative evolutionary framework with other cnidarian genomes. We also generated and annotated a single-cell transcriptomic atlas for adult maleH. symbiolongicarpusand identified cell-type markers for all major cell types, including key i-cell markers. Orthology analyses based on the markers revealed thatHydractinia’s i-cells are highly enriched in genes that are widely shared amongst animals, a striking finding given thatHydractiniahas a higher proportion of phylum-specific genes than any of the other 41 animals in our orthology analysis. These results indicate thatHydractinia’s stem cells and early progenitor cells may use a toolkit shared with all animals, making it a promising model organism for future exploration of stem cell biology and regenerative medicine. The genomic and transcriptomic resources forHydractiniapresented here will enable further studies of their regenerative capacity, colonial morphology, and ability to distinguish self from nonself. 

Most colonial marine invertebrates are capable of allorecognition, the ability to distinguish between themselves and conspecifics. One long-standing question is whether invertebrate allorecognition genes are homologous to vertebrate histocompatibility genes. In the cnidarian Hydractinia symbiolongicarpus, allorecognition is controlled by at least two genes, Allorecognition 1 ( Alr1 ) and Allorecognition 2 ( Alr2 ), which encode highly polymorphic cell-surface proteins that serve as markers of self. Here, we show that Alr1 and Alr2 are part of a family of 41 Alr genes, all of which reside in a single genomic interval called the Allorecognition Complex (ARC). Using sensitive homology searches and highly accurate structural predictions, we demonstrate that the Alr proteins are members of the immunoglobulin superfamily (IgSF) with V-set and I-set Ig domains unlike any previously identified in animals. Specifically, their primary amino acid sequences lack many of the motifs considered diagnostic for V-set and I-set domains, yet they adopt secondary and tertiary structures nearly identical to canonical Ig domains. Thus, the V-set domain, which played a central role in the evolution of vertebrate adaptive immunity, was present in the last common ancestor of cnidarians and bilaterians. Unexpectedly, several Alr proteins also have immunoreceptor tyrosine-based activation motifs and immunoreceptor tyrosine-based inhibitory motifs in their cytoplasmic tails, suggesting they could participate in pathways homologous to those that regulate immunity in humans and flies. This work expands our definition of the IgSF with the addition of a family of unusual members, several of which play a role in invertebrate histocompatibility. 

The epithelial and interstitial stem cells of the freshwater polyp Hydra are the best-characterized stem cell systems in any cnidarian, providing valuable insight into cell type evolution and the origin of stemness in animals. However, little is known about the transcriptional regulatory mechanisms that determine how these stem cells are maintained and how they give rise to their diverse differentiated progeny. To address such questions, a thorough understanding of transcriptional regulation in Hydra is needed. To this end, we generated extensive new resources for characterizing transcriptional regulation in Hydra , including new genome assemblies for Hydra oligactis and the AEP strain of Hydra vulgaris , an updated whole-animal single-cell RNA-seq atlas, and genome-wide maps of chromatin interactions, chromatin accessibility, sequence conservation, and histone modifications. These data revealed the existence of large kilobase-scale chromatin interaction domains in the Hydra genome that contain transcriptionally coregulated genes. We also uncovered the transcriptomic profiles of two previously molecularly uncharacterized cell types: isorhiza-type nematocytes and somatic gonad ectoderm. Finally, we identified novel candidate regulators of cell type–specific transcription, several of which have likely been conserved at least since the divergence of Hydra and the jellyfish Clytia hemisphaerica more than 400 million years ago. 

Neurogenesis is the generation of neurons from stem cells, a process that is regulated by SoxB transcription factors (TFs) in many animals. Although the roles of these TFs are well understood in bilaterians, how their neural function evolved is unclear. Here, we use Hydractinia symbiolongicarpus , a member of the early-branching phylum Cnidaria, to provide insight into this question. Using a combination of mRNA in situ hybridization, transgenesis, gene knockdown, transcriptomics, and in vivo imaging, we provide a comprehensive molecular and cellular analysis of neurogenesis during embryogenesis, homeostasis, and regeneration in this animal. We show that SoxB genes act sequentially at least in some cases. Stem cells expressing Piwi1 and Soxb1 , which have broad developmental potential, become neural progenitors that express Soxb2 before differentiating into mature neural cells. Knockdown of SoxB genes resulted in complex defects in embryonic neurogenesis. Hydractinia neural cells differentiate while migrating from the aboral to the oral end of the animal, but it is unclear whether migration per se or exposure to different microenvironments is the main driver of their fate determination. Our data constitute a rich resource for studies aiming at addressing this question, which is at the heart of understanding the origin and development of animal nervous systems.