Venom system variation and the division of labor in the colonial hydrozoan Hydractinia symbiolongicarpus

Klompen, Anna M. L.; Sanders, Steven M.; Cartwright, Paulyn

doi:10.1016/j.toxcx.2022.100113

Cited by 4 publications

(23 citation statements)

References 70 publications

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“…A single-cell RNA-sequencing (scRNA-Seq) database has previously been generated for H. symbiolongicarpus gastrozooid polyps and is publicly available through the Hydractinia Genome Portal Project ( , accessed on September 2022) [ 33 ]. Given that previous transcriptomic studies identified three of the four Hydractinia JFT genes as relatively abundant in gastrozooids ( Table 1 ) [ 26 , 32 ], we searched the scRNA-Seq database to determine if JFT expression co-occurs with the expression of a known nematocyst-specific marker. The scRNA-Seq database revealed two discernable clusters expressing the nematocyst-specific marker Ncol-1 (for ease of communication, these will be referred to as Cluster 1 and Cluster 2) ( Supplementary Figure S2 ).…”

Section: Resultsmentioning

confidence: 99%

“…Previous work using RNA-sequencing (RNA-Seq) has demonstrated that this division of labor in H. symbiolongicarpus is complemented by the differential expression of toxins [ 26 ]. One set of differentially expressed toxins are the so-called “jellyfish toxins” (JFTs), which are well known as the dominant class of pore-forming toxins in several species of medically relevant box jellyfish (class Cubozoa) (reviewed in [ 27 , 28 ]), including the infamous Chironex fleckeri (Southcott, 1956) [ 29 , 30 , 31 ].…”

Section: Introductionmentioning

confidence: 99%

“…One set of differentially expressed toxins are the so-called “jellyfish toxins” (JFTs), which are well known as the dominant class of pore-forming toxins in several species of medically relevant box jellyfish (class Cubozoa) (reviewed in [ 27 , 28 ]), including the infamous Chironex fleckeri (Southcott, 1956) [ 29 , 30 , 31 ]. Klompen et al [ 26 ] found two different JFTs upregulated in the gastrozooid and dactylozooid, respectively, when compared to toxin expression across all three polyp types. These two toxins are HsymJFT1c-I (upregulated in gastrozooids) and HsymJFT1c-II (upregulated in dactylozooids) ( Table 1 ) (see Supplementary Figure S1 ).…”

Section: Introductionmentioning

confidence: 99%

“…While this phylogenetic placement does not necessarily imply Hydractinia JFTs share similar potency, this well supported relationship does suggest that these putative pore-forming toxins are true venom proteins, and that the recruitment of JFTs in cnidarian venoms occurred before the split of Hydrozoa from the rest of the medusozoans [ 32 ]. Two other H. symbiolongicarpus JFTs were identified in Klompen et al [ 26 , 32 ], here called HsymJFT2a and HsymJFT2 ( Table 1 ; Supplementary Figure S1 ). Both toxin sequences fall within clades of putative JFT sequences to which no homolog has been previously characterized; thus, their role as true venom toxins is unclear [ 32 ].…”

Section: Introductionmentioning

confidence: 99%

“…Gastrozooid tentacles possess mostly adherent desmonemes, which are not thought to contain toxins, as well as small euryteles found evenly scattered throughout the gastrozooid tentacles and encircling the mouth (hypostome). In contrast, dactylozooids, as well as gonozooids, possess large euryteles concentrated in the capitate tentacles, yet despite this shared nematocyst type, HsymJFT1c-II is only significantly upregulated in dactylozooids ( Table 1 ) [ 26 ].…”

Section: Introductionmentioning

confidence: 99%

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Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan

Klompen

Travert

Cartwright

2023

Toxins

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Hydractinia symbiolongicarpus is a colonial hydrozoan that displays a division of labor through morphologically distinct and functionally specialized polyp types. As with all cnidarians, their venoms are housed in nematocysts, which are scattered across an individual. Here, we investigate the spatial distribution of a specific protein family, jellyfish toxins, in which multiple paralogs are differentially expressed across the functionally specialized polyps. Jellyfish toxins (JFTs) are known pore-forming toxins in the venoms of medically relevant species such as box jellyfish (class Cubozoa), but their role in other medusozoan venoms is less clear. Utilizing a publicly available single-cell dataset, we confirmed that four distinct H. symbiolongicarpus JFT paralogs are expressed in nematocyst-associated clusters, supporting these as true venom components in H. symbiolongicarpus. In situ hybridization and immunohistochemistry were used to localize the expression of these JFTs across the colony. These expression patterns, in conjunction with known nematocyst type distributions, suggest that two of these JFTs, HsymJFT1c-I and HsymJFT1c-II, are localized to specific types of nematocysts. We further interpret JFT expression patterns in the context of known regions of nematogenesis and differential rates of nematocyst turnover. Overall, we show that JFT expression patterns in H. symbiolongicarpus are consistent with the subfunctionalization of JFT paralogs across a partitioned venom system within the colony, such that each JFT is expressed within a specific set of functionally distinct polyp types and, in some cases, specific nematocyst types.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan

Klompen

Travert

Cartwright

2023

Toxins

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A positive feedback loop between germ cells and gonads induces and maintains cnidarian sexual reproduction

Curantz,

Doody,

Horkan

et al. 2024

Preprint

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The fertile gonad includes cells of two distinct developmental origins: the somatic mesoderm and the germline. How somatic and germ cells interact to develop and maintain fertility is not well understood. Here, using grafting experiments and transgenic reporter animals, we find that a specific part of the gonad-the germinal zone-acts as a sexual organizer to induce and maintain de novo germ cells and somatic gonads in non-sexual tissue in the cnidarian Hydractinia symbiolongicarpus. We further show that germ cells express a novel member of the BMP family (Gonadless, Gls) that induces somatic gonad morphogenesis. Loss of Gls resulted in animals lacking somatic gonadal structures but having few, non-proliferative germ cells. We propose a model according to which a small number of primary germ cells drive gonad development though Gls morphogen secretion. The germinal zone in the newly formed gonad, in turn, provides positive feedback to induce secondary germ cells by activating Tfap2 (the master regulator of germ cell fate) in resident pluripotent stem cells. De novo induction of germ cells by gonads in adult life is absent in bilaterians with a sequestered germline. However, the contribution of germ cell signaling to the patterning of somatic gonadal tissue, as observed in Hydractinia, may be a general animal feature.

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TheHydractiniacell atlas reveals cellular and molecular principles of cnidarian coloniality

Salamanca-Díaz,

Horkan,

García-Castro

et al. 2024

Preprint

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Coloniality is a widespread growth form in cnidarians, tunicates, and bryozoans, among others. Despite being modular, composed of multiple zooids and supporting tissues, colonies function as a single physiological unit. A major question in the biology of colonies is the cellular mechanism of generating structurally and functionally distinct colony parts. The cnidarianHydractiniaestablishes colonies with different types of zooids (polyps), interconnected by a gastrovascular system that is attached to the substrate and known as stolons. We obtained single cell transcriptomic profiles of ∼200KHydractiniacells, including isolated stolons and two polyp types. We characterised the majorHydractiniacell types and quantified their abundance across colony parts. Overall, we find that distinct colony parts are characterised primarily by distinct combinations of shared cell types and to a lesser extent by part-specific cell types. Therefore, we propose that both cell type combinations, as well as rarer cell type innovations, have been the main mechanism in the evolution of coloniality in cnidarians. We identified cell type-specific transcription factors (TFs) and gene networks expressed within these cell types. Notably, we discovered a previously unidentified, stolon-specific cell type, which expresses enzymes related to biomineralization and chitin synthesis, reminiscent of molluscan shell matrix proteins that may represent a crucial adaptation to the animal’s habitat. In summary, theHydractiniacell atlas elucidates the fundamental cellular and molecular mechanisms underlying coloniality.

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Venom system variation and the division of labor in the colonial hydrozoan Hydractinia symbiolongicarpus

Cited by 4 publications

References 70 publications

Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan

Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan

A positive feedback loop between germ cells and gonads induces and maintains cnidarian sexual reproduction

TheHydractiniacell atlas reveals cellular and molecular principles of cnidarian coloniality

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