Histamine is a modulator of metamorphic competence in Strongylocentrotus purpuratus(Echinodermata: Echinoidea)

Sutherby, Josh; Giardini, Jamie-Lee; Nguyen, Julia; Wessel, Gary M.; Leguía, Mariana; Heyland, Andreas

doi:10.1186/1471-213x-12-14

Cited by 41 publications

(56 citation statements)

References 75 publications

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“…In echinoids, however, multiple studies have addressed and rejected the potential for biased outcomes due to elevated potassium. In all cases examined, rates of settlement and survival following KCl exposure closely resemble those arising in the presence of a potent natural inducer (28,(35)(36)(37)(38). The successful, turbulencecaused metamorphic transition we observe therefore stands in marked contrast to consequences of transient exposure to other physical or chemical stimulants (e.g., H 2 S, petrochemicals, hypoxia).…”

Section: Discussionmentioning

confidence: 61%

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Turbulent shear spurs settlement in larval sea urchins

Gaylord

Hodin

Ferner

2013

Proc. Natl. Acad. Sci. U.S.A.

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Marine invertebrates commonly produce larvae that disperse in ocean waters before settling into adult shoreline habitat. Chemical and other seafloor-associated cues often facilitate this latter transition. However, the range of effectiveness of such cues is limited to small spatial scales, creating challenges for larvae in finding suitable sites at which to settle, especially given that they may be carried many kilometers by currents during their planktonic phase. One possible solution is for larvae to use additional, broader-scale environmental signposts to first narrow their search to the general vicinity of a candidate settlement location. Here we demonstrate strong effects of just such a habitat-scale cue, one with the potential to signal larvae that they have arrived in appropriate coastal areas. Larvae of the purple sea urchin (Strongylocentrotus purpuratus) exhibit dramatic enhancement in settlement following stimulation by turbulent shear typical of wave-swept shores where adults of this species live. This response manifests in an unprecedented fashion relative to previously identified cues. Turbulent shear does not boost settlement by itself. Instead, it drives a marked developmental acceleration that causes "precompetent" larvae refractory to chemical settlement inducers to immediately become "competent" and thereby reactive to such inducers. These findings reveal an unrecognized ability of larval invertebrates to shift the trajectory of a major life history event in response to fluid-dynamic attributes of a target environment. Such an ability may improve performance and survival in marine organisms by encouraging completion of their life cycle in advantageous locations. competence | energy dissipation rate | metamorphosis | surf zone | turbulence N early 80% of marine invertebrate species that dwell along the shore possess a two-phase life cycle (1). Such life cycles typically are composed of an adult stage resident on the seafloor and a dispersing larval stage that develops in the plankton before returning to, and settling within, shoreline habitat. Because planktonic larval stages foster demographic connectivity among populations (2-4) and because the transition to the substratum often is irreversible and fraught with high mortality (5), considerable attention has focused on cues used by larvae to identify and settle in quality locations. In particular, research has centered on chemical compounds that induce settlement. A rich array of dissolved and surface-bound chemicals have been implicated, including amino acids and proteins, fatty acids, and carbohydrates (6-8). Such substances often are associated with food, prey, adults of the same species, or biofilms composed of microorganisms. Other habitat properties also may be assessed by larvae once they contact the seafloor. For example, larvae often prefer certain substratum textures and topographies, light intensities, or local water velocities (9-13).Despite their clear importance as signals for larvae, chemical and other seafloor-associated cues p...

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Section: Discussionmentioning

confidence: 61%

“…Following turbulence treatments, settlement was assayed by exposing larvae to 70 mM excess KCl in MFSW for 1 h at 14°C, followed by recovery in MFSW, as in standard protocols (27,(36)(37)(38). A larva was scored as settled after this 1-h exposure if it had begun to withdraw skin from the tips of the larval skeletal rods (Fig.…”

Section: Methodsmentioning

confidence: 99%

Turbulent shear spurs settlement in larval sea urchins

Gaylord

Hodin

Ferner

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…And it is also known that histamine can act as an intracellular messenger in echinoderm fertilization [35]. Furthermore, recent evidence shows an involvement of HA in sea urchin metamorphosis [36], [37], [38].…”

Section: Introductionmentioning

confidence: 98%

Novel Insights into the Echinoderm Nervous System from Histaminergic and FMRFaminergic-Like Cells in the Sea Cucumber Leptosynapta clarki

2012

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Understanding of the echinoderm nervous system is limited due to its distinct organization in comparison to other animal phyla and by the difficulty in accessing it. The transparent and accessible, apodid sea cucumber Leptosynapta clarki provides novel opportunities for detailed characterization of echinoderm neural systems. The present study used immunohistochemistry against FMRFamide and histamine to describe the neural organization in juvenile and adult sea cucumbers. Histaminergic- and FMRFaminergic-like immunoreactivity is reported in several distinct cell types throughout the body of L. clarki. FMRFamide-like immunoreactive cell bodies were found in the buccal tentacles, esophageal region and in proximity to the radial nerve cords. Sensory-like cells in the tentacles send processes toward the circumoral nerve ring, while unipolar and bipolar cells close to the radial nerve cords display extensive processes in close association with muscle and other cells of the body wall. Histamine-like immunoreactivity was identified in neuronal somatas located in the buccal tentacles, circumoral nerve ring and in papillae distributed across the body. The tentacular cells send processes into the nerve ring, while the processes of cells in the body wall papillae extend to the surface epithelium and radial nerve cords. Pharmacological application of histamine produced a strong coordinated, peristaltic response of the body wall suggesting the role of histamine in the feeding behavior. Our immunohistochemical data provide evidence for extensive connections between the hyponeural and ectoneural nervous system in the sea cucumber, challenging previously held views on a clear functional separation of the sub-components of the nervous system. Furthermore, our data indicate a potential function of histamine in coordinated, peristaltic movements; consistent with feeding patterns in this species. This study on L. clarki illustrates how using a broader range of neurotransmitter systems can provide better insight into the anatomy, function and evolution of echinoderm nervous sytems.

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“…It is hypothesized that metamorphosis evolved multiple times among metazoans, yet common signaling systems were independently coopted to coordinate the metamorphic transition (12)(13)(14)(15). These systems include hormones (16)(17)(18), neurotransmitters (19)(20)(21), and nitric oxide (22)(23)(24). Additionally, diverse animals regulate metamorphosis at the transcriptional and posttranslational levels, such as differential expression of metamorphosis-associated genes (25)(26)(27) and MAPK signaling (28)(29)(30)(31), respectively.…”

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confidence: 99%

Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

Shikuma

Antoshechkin

Medeiros

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Diverse animal taxa metamorphose between larval and juvenile phases in response to bacteria. Although bacteria-induced metamorphosis is widespread among metazoans, little is known about the molecular changes that occur in the animal upon stimulation by bacteria. Larvae of the tubeworm Hydroides elegans metamorphose in response to surface-bound Pseudoalteromonas luteoviolacea bacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing the Hydroides genome and transcripts during five developmental stages revealed that MACs induce the regulation of groups of genes important for tissue remodeling, innate immunity, and mitogen-activated protein kinase (MAPK) signaling. Using two MAC mutations that block P. luteoviolacea from inducing settlement or metamorphosis and three MAPK inhibitors, we established a sequence of bacteria-induced metamorphic events: MACs induce larval settlement; then, particular properties of MACs encoded by a specific locus in P. luteoviolacea initiate cilia loss and activate metamorphosis-associated transcription; finally, signaling through p38 and c-Jun N-terminal kinase (JNK) MAPK pathways alters gene expression and leads to morphological changes upon initiation of metamorphosis. Our results reveal that the intricate interaction between Hydroides and P. luteoviolacea can be dissected using genomic, genetic, and pharmacological tools. Hydroides' dependency on bacteria for metamorphosis highlights the importance of external stimuli to orchestrate animal development. The conservation of Hydroides genome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis in Hydroides may have conserved features in diverse animals. As a major biofouling agent, insight into the triggers of Hydroides metamorphosis might lead to practical strategies for fouling control.genome | phage | symbiosis | biofouling | development

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Histamine is a modulator of metamorphic competence in Strongylocentrotus purpuratus(Echinodermata: Echinoidea)

Cited by 41 publications

References 75 publications

Turbulent shear spurs settlement in larval sea urchins

Turbulent shear spurs settlement in larval sea urchins

Novel Insights into the Echinoderm Nervous System from Histaminergic and FMRFaminergic-Like Cells in the Sea Cucumber Leptosynapta clarki

Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

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