A gonad-expressed opsin mediates light-induced spawning in the jellyfish Clytia

Abstract

Across the animal kingdom, environmental light cues are widely involved in regulating gamete release, but the molecular and cellular bases of the photoresponsive mechanisms are poorly understood. In hydrozoan jellyfish, spawning is triggered by dark-light or light-dark transitions acting on the gonad, and is mediated by oocyte maturation-inducing neuropeptide hormones (MIHs) released from the ectoderm. We determined in Clytia hemisphaerica that blue-cyan light triggers spawning in isolated gonads. A candidate opsin (Opsin9) was found co-expressed with MIH within specialised ectodermal cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, a phenotype reversible by synthetic MIH. Gamete maturation and release in Clytia is thus regulated by gonadal photosensory-neurosecretory cells that secrete MIH in response to light via Opsin9. Similar cells in ancestral eumetazoans may have allowed tissue-level photo-regulation of diverse behaviours, a feature elaborated in cnidarians in parallel with expansion of the opsin gene family.

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

“…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. 3C).…”

“…An important criterion for the selection of MIH-receptor candidates from the class-A GPCR list was enrichment in oocytes ( Fig.1A). We mapped Illumina HiSeq mRNA reads previously obtained from Clytia gonad tissues [16] and life cycle stage [26] against all putative GPCR sequences. Profile clustering revealed three groups of sequences with oocyte-enriched expression ( Fig.…”

“…To determine the function of MIHR in vivo we generated Clytia MIHR knockout (KO) polyp colonies using CRISPR/Cas9 mutagenesis (see Methods). This gene-editing technique is very effective in Clytia, allowing extensive bi-allelic mutation of target genes already in F0 polyp colonies [16,63].…”

“…5B). A light cue triggers MIH release from neuroendocrinetype cells in the gonad ectoderm via an essential opsin protein [16]. The MIH peptides act on MIHR at the oocyte surface to promote Gα s activation, stimulating adenylate cyclase and thus promoting an increase in cytoplasmic cAMP concentration, essential for the transition into meiotic M phase.…”

“…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].…”