Cellular pathways during spawning induction in the starlet sea anemone Nematostella vectensis.
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ABSTRACT:
SUBMITTER: Reuven S
PROVIDER: S-EPMC8322078 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundAlthough much is known about how circadian systems control daily cycles in the physiology and behavior of Drosophila and several vertebrate models, marine invertebrates have often been overlooked in circadian rhythms research. This study focuses on the starlet sea anemone, Nematostella vectensis, a species that has received increasing attention within the scientific community for its potential as a model research organism. The recently sequenced genome of N. vectensis makes it an especially attractive model for exploring the molecular evolution of circadian behavior. Critical behavioral data needed to correlate gene expression patterns to specific behaviors are currently lacking in N. vectensis.Methodology/principal findingsTo detect the presence of behavioral oscillations in N. vectensis, locomotor activity was evaluated using an automated system in an environmentally controlled chamber. Animals exposed to a 24 hr photoperiod (12 hr light: 12 hr dark) exhibited locomotor behavior that was both rhythmic and predominantly nocturnal. The activity peak occurred in the early half of the night with a 2-fold increase in locomotion. Upon transfer to constant lighting conditions (constant light or constant dark), an approximately 24 hr rhythm persisted in most animals, suggesting that the rhythm is controlled by an endogenous circadian mechanism. Fourier analysis revealed the presence of multiple peaks in some animals suggesting additional rhythmic components could be present. In particular, an approximately 12 hr oscillation was often observed. The nocturnal increase in generalized locomotion corresponded to a 24 hr oscillation in animal elongation.Conclusions/significanceThese data confirm the presence of a light-entrainable circadian clock in Nematostella vectensis. Additional components observed in some individuals indicate that an endogenous clock of approximately 12 hr frequency may also be present. By describing rhythmic locomotor behavior in N. vectensis, we have made important progress in developing the sea anemone as a model organism for circadian rhythm research.
| S-EPMC3467289 | biostudies-literature
Project description:BackgroundThe recent combination of genomics and single cell transcriptomics has allowed to assess a variety of non-conventional model organisms in much more depth. Single cell transcriptomes can uncover hidden cellular complexity and cell lineage relationships within organisms. The recent developmental cell atlases of the sea anemone Nematostella vectensis, a representative of the basally branching Cnidaria, has provided new insights into the development of all cell types (Steger et al Cell Rep 40(12):111370, 2022; Sebé-Pedrós et al. Cell 173(6):1520-1534.e20). However, the mapping of the single cell reads still suffers from relatively poor gene annotations and a draft genome consisting of many scaffolds.ResultsHere we present a new wildtype resource of the developmental single cell atlas, by re-mapping of sequence data first published in Steger et al. (2022) and Cole et al. (Nat Commun 14(1):1747, 2023), to the new chromosome-level genome assembly and corresponding gene models in Zimmermann et al. (Nat Commun 14, 8270 (2023). https://doi.org/10.1038/s41467-023-44080-7 ). We expand the pre-existing dataset through the incorporation of additional sequence data derived from the capture and sequencing of cell suspensions from four additional samples: 24 h gastrula, 2d planula, an inter-parietal region of the bodywall from a young unsexed animal, and another adult mesentery from a mature male animal.ConclusionOur analyses of the full cell-state inventory provide transcriptomic signatures for 127 distinct cell states, of which 47 correspond to neuroglandular subtypes. We also identify two distinct putatively immune-related transcriptomic profiles that segregate between the inner and outer cell layers. Furthermore, the new gene annotation Nv2 has markedly improved the mapping on the single cell transcriptome data and will therefore be of great value for the community and anyone using the dataset.
| S-EPMC10946136 | biostudies-literature
Project description:We describe a protocol for microinjection of embryos for an emerging model system, the cnidarian sea anemone, Nematostella vectensis. In addition, we provide protocols for carrying out overexpression and knockdown of gene function through microinjection of in vitro-translated mRNAs or gene-specific oligonucleotide morpholinos (MOs), respectively. Our approach is simple, and it takes advantage of the natural adherence properties of the early embryo to position them in a single layer on a polystyrene dish. Embryos are visualized on a dissecting microscope equipped with epifluorescence and injected with microinjection needles using a picospritzer forced-air injection system. A micromanipulator is used to guide the needle to impale individual embryos. Injection takes ?1.5 h, and an experienced researcher can inject ?2,000 embryos in a single session. With the availability of the published Nematostella genome, the entire protocol, including cloning and transcription of mRNAs, can be carried out in ?1 week.
| S-EPMC4805419 | biostudies-literature
Project description:BackgroundHomeodomain transcription factors are key components in the developmental toolkits of animals. While this gene superclass predates the evolutionary split between animals, plants, and fungi, many homeobox genes appear unique to animals. The origin of particular homeobox genes may, therefore, be associated with the evolution of particular animal traits. Here we report the first near-complete set of homeodomains from a basal (diploblastic) animal.ResultsPhylogenetic analyses were performed on 130 homeodomains from the sequenced genome of the sea anemone Nematostella vectensis along with 228 homeodomains from human and 97 homeodomains from Drosophila. The Nematostella homeodomains appear to be distributed among established homeodomain classes in the following fashion: 72 ANTP class; one HNF class; four LIM class; five POU class; 33 PRD class; five SINE class; and six TALE class. For four of the Nematostella homeodomains, there is disagreement between neighbor-joining and Bayesian trees regarding their class membership. A putative Nematostella CUT class gene is also identified.ConclusionThe homeodomain superclass underwent extensive radiations prior to the evolutionary split between Cnidaria and Bilateria. Fifty-six homeodomain families found in human and/or fruit fly are also found in Nematostella, though seventeen families shared by human and fly appear absent in Nematostella. Homeodomain loss is also apparent in the bilaterian taxa: eight homeodomain families shared by Drosophila and Nematostella appear absent from human (CG13424, EMXLX, HOMEOBRAIN, MSXLX, NK7, REPO, ROUGH, and UNC4), and six homeodomain families shared by human and Nematostella appear absent from fruit fly (ALX, DMBX, DUX, HNF, POU1, and VAX).
| S-EPMC1779571 | biostudies-literature
Project description:Coral conservation requires a mechanistic understanding of how environmental stresses disrupt biomineralization, but progress has been slow, primarily because corals are not easily amenable to laboratory research. Here, we highlight how the starlet sea anemone, Nematostella vectensis, can serve as a model to interrogate the cellular mechanisms of coral biomineralization. We have developed transgenic constructs using biomineralizing genes that can be injected into Nematostella zygotes and designed such that translated proteins may be purified for physicochemical characterization. Using fluorescent tags, we confirm the ectopic expression of the coral biomineralizing protein, SpCARP1, in Nematostella. We demonstrate via calcein staining that SpCARP1 concentrates calcium ions in Nematostella, likely initiating the formation of mineral precursors, consistent with its suspected role in corals. These results lay a fundamental groundwork for establishing Nematostella as an in vivo system to explore the evolutionary and cellular mechanisms of coral biomineralization, improve coral conservation efforts, and even develop novel biomaterials.
| S-EPMC10879693 | biostudies-literature
Project description:The cnidarian Nematostella vectensis has developed into a powerful model system to study the mechanisms underlying animal development, regeneration, and evolution. However, despite the significant progress in the molecular and genetic approaches in this sea anemone, endogenous protein tagging is still challenging. Here, we report a robust method for knock in for Nematostella using CRISPR/Cas9. As an outcome, we generate endogenously tagged proteins that label core molecular components of several cellular apparatus, including the nuclear envelope, cytoskeleton, cell adhesion, endoplasmic reticulum, cell trafficking, and extracellular matrix. Using live imaging, we monitor the dynamics of vesicular trafficking and endoplasmic reticulum in embryos, as well as cell contractility during the peristaltic wave of a primary polyp. This advancement in gene editing expands the molecular tool kit of Nematostella and enables experimental avenues to interrogate the cell biology of cnidarians.
| S-EPMC9910423 | biostudies-literature
Project description:PIWI-interacting RNAs (piRNAs) and associated proteins comprise a conserved pathway for silencing transposons in metazoan germlines. piRNA pathway components are also expressed in multipotent somatic stem cells in various organisms. piRNA functions have been extensively explored in bilaterian model systems, however, comprehensive studies in non-bilaterian phyla remain limited. Here we investigate the piRNA pathway during the development of Nematostella vectensis, a well-established model system belonging to Cnidaria, the sister group to Bilateria. To date, no population of somatic stem cells has been identified in this organism, despite its long life-span and regenerative capacities that require a constant cell-renewal. We show that Nematostella piRNA pathway components are broadly expressed in early developmental stages, while piRNAs themselves show differential expression, suggesting specific developmental roles of distinct piRNA families. In adults, piRNA associated proteins are enriched in the germline but also expressed in somatic cells, indicating putative stem cell properties. Furthermore, we provide experimental evidence that Nematostella piRNAs cleave transposable elements as well as protein-coding genes. Our results demonstrate that somatic expression of piRNA associated proteins as well as the roles of piRNAs in transposon repression and gene regulation are likely ancestral features that evolved before the split between Cnidaria and Bilateria.
| S-EPMC5731801 | biostudies-literature
Project description:In cnidarians, axial patterning is not restricted to embryogenesis but continues throughout a prolonged life history filled with unpredictable environmental changes. How this developmental capacity copes with fluctuations of food availability and whether it recapitulates embryonic mechanisms remain poorly understood. Here we utilize the tentacles of the sea anemone Nematostella vectensis as an experimental paradigm for developmental patterning across distinct life history stages. By analyzing over 1000 growing polyps, we find that tentacle progression is stereotyped and occurs in a feeding-dependent manner. Using a combination of genetic, cellular and molecular approaches, we demonstrate that the crosstalk between Target of Rapamycin (TOR) and Fibroblast growth factor receptor b (Fgfrb) signaling in ring muscles defines tentacle primordia in fed polyps. Interestingly, Fgfrb-dependent polarized growth is observed in polyp but not embryonic tentacle primordia. These findings show an unexpected plasticity of tentacle development, and link post-embryonic body patterning with food availability.
| S-EPMC7467937 | biostudies-literature
Project description:Cnidarians, the extant sister group to bilateria, are well known for their impressive regenerative capacity. The sea anemone Nematostella vectensis is a well-established system for the study of development and evolution that is receiving increased attention for its regenerative capacity. Nematostella is able to regrow missing body parts within five to six days after its bisection, yet studies describing the morphological, cellular, and molecular events underlying this process are sparse and very heterogeneous in their experimental approaches. In this study, we lay down the basic framework to study oral regeneration in Nematostella vectensis. Using various imaging and staining techniques we characterize in detail the morphological, cellular, and global molecular events that define specific landmarks of this process. Furthermore, we describe in vivo assays to evaluate wound healing success and the initiation of pharynx reformation. Using our described landmarks for regeneration and in vivo assays, we analyze the effects of perturbing either transcription or cellular proliferation on the regenerative process. Interestingly, neither one of these experimental perturbations has major effects on wound closure, although they slightly delay or partially block it. We further show that while the inhibition of transcription blocks regeneration in a very early step, inhibiting cellular proliferation only affects later events such as pharynx reformation and tentacle elongation.
| S-EPMC4691047 | biostudies-literature
Project description:The starlet sea-anemone Nematostella vectensis has emerged as a model organism in developmental biology. Still, our understanding of various biological features, including reproductive biology of this model species are in its infancy. Consequently, through histological sections, we study here key stages of the oogenesis (oocyte maturation/fertilization), as the state of the gonad region immediately after natural spawning. Germ cells develop in a secluded mesenterial gastrodermal zone, where the developing oocytes are surrounded by mucoid glandular cells and trophocytes (accessory cells). During vitellogenesis, the germinal vesicle in oocytes migrates towards the animal pole and the large polarized oocytes begin to mature, characterized by karyosphere formation. Then, the karyosphere breaks down, the chromosomes form the metaphase plate I and the eggs are extruded from the animal enclosed in a sticky, jelly-like mucoid mass, along with numerous nematosomes. Fertilization occurs externally at metaphase II via swimming sperm extruded by males during natural spawning. The polar bodies are ejected from the eggs and are situated within a narrow space between the egg's vitelline membrane and the adjacent edge of the jelly coat. The cortical reaction occurs only at the polar bodies' ejection site. Several spermatozoa can penetrate the same egg. Fertilization is accompanied by a strong ooplasmatic segregation. Immediately after spawning, the gonad region holds many previtellogenic and vitellogenic oocytes, though no oocytes with karyosphere. Above are the first histological descriptions for egg maturation, meiotic chromosome's status at fertilization, fertilization and the gonadal region's state following spawning, also documenting for the first time the ejection of the polar body.
| S-EPMC5552035 | biostudies-other