Identification of jellyfish neuropeptides that act directly as oocyte maturation-inducing hormones

Abstract

Oocyte meiotic maturation is crucial for sexually reproducing animals, and its core cytoplasmic regulators are highly conserved between species. By contrast, the few known maturation-inducing hormones (MIHs) that act on oocytes to initiate this process are highly variable in their molecular nature. Using the hydrozoan jellyfish species and, which undergo oocyte maturation in response to dark-light and light-dark transitions, respectively, we deduced amidated tetrapeptide sequences from gonad transcriptome data and found that synthetic peptides could induce maturation of isolated oocytes at nanomolar concentrations. Antibody preabsorption experiments conclusively demonstrated that these W/RPRPamide-related neuropeptides account for endogenous MIH activity produced by isolated gonads. We show that the MIH peptides are synthesised by neural-type cells in the gonad, are released following dark-light/light-dark transitions, and probably act on the oocyte surface. They are produced by male as well as female jellyfish and can trigger both sperm and egg release, suggesting a role in spawning coordination. We propose an evolutionary link between hydrozoan MIHs and the neuropeptide hormones that regulate reproduction upstream of MIHs in bilaterian species.

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

“…3A, B) supported this idea. Strong expression was expressed in developing oocytes and in male gametes, consistent with the ability of MIH to induce male spawning [15]. Expression was also detected in clusters of small somatic cells located within each tentacle bulb.…”

“…cDNAs for each candidate were transfected into CHO-K1 cells along with an aequorin-GFP luminescence reporter that measures Ca2+ mobilization downstream of a promiscuous Gα protein [27,28]. We first screened the 16 candidate Clytia GPCRs against a mixture of 33 synthetic amidated peptides (including MIHs) predicted to be generated from previously identified putative Clytia neuropeptide precursors [15] and one additional one identified from transcriptome data (File S4).…”

“…3C]. These two precursors are expressed respectively exclusively in the manubrium and tentacle, as well as being co-expressed in scattered cells of the gonad [15]. As well as the cells in the gonad ectoderm that mediate spawning, the anti-PRPa antibody decorates cells in the tentacle especially at its junction with the circular gastrovascular canal, and in the endoderm of the manubrium feeding/digestive organ [15,16] (Fig.…”

“…Here we identify the MIH receptor (MIHR) in the hydrozoan jellyfish Clytia hemisphaerica as a GPCR likely working through Gα s , and determine its in vivo function. In Clytia and other hydrozoan species, MIH consists of PRPamide and related tetrapeptides that are released upon light stimulation from opsin-expressing gonad ectoderm cells, and act at the plasma membrane [15,16]. Neuropeptides such as these are of major importance in cnidarian biology, acting both as "neuroendocrine" mediators of physiological transitions such as metamorphosis, as well as in fast neuromuscular transmission regulating swimming and feeding mediated by ligand-gated ion channels [reviewed by 17,18].…”

Seasonal temperature, the lunar cycle and diurnal rhythms interact in a combinatorial manner to modulate genomic responses to the environment in a reef‐building coral

“…Circadian clocks are well understood and are based on transcription-initiated processes (Dunlap, 1999), but the molecular underpinnings of longer cycles remain elusive and much of our knowledge in this regard is limited to hormonal cycles that are probably the terminal mediators of these systems (e.g., Crowder, Meyer, Fan, & Weis, 2017;Kaniewska, Alon, Karako-Lampert, Hoegh-Guldberg, & Levy, 2015;Takeda et al, 2018;Tarrant, 2005;Thorndyke & Goldsworthy, 1988).…”