Photoreceptor control of <i>Platynereis</i> growth and lifespan via evolutionarily conserved molecular pathways.

Abstract

Natural light is severely affected by human impact on Earth, yet little is known about the roles light receptors have outside vision and rhythmic processes, despite their tremendously wide abundance. Here we show that loss-of-function of the <i>light-receptive cryptochrome</i> (<i>l-cry</i>) in marine bristleworms significantly increases lifespan and adult size, similarly to wild-types reared in constant darkness. Quantitative transcriptomics revealed hormonal players crucial for invertebrate and vertebrate sexual development and reproduction affected in <i>l-cry</i> mutants. These include <i>nr0b1/2</i>, ortholog of <i>dax-1</i> (<i>nr0b1</i>) and <i>shp</i> (<i>nr0b2</i>), long considered vertebrate novelties. Depending on moon-phase, <i>nr0b1/2</i> is up- or down-regulated in <i>l-cry</i> mutants. Matching the complex regulation, data consistent with loss of <i>nr0b1/2</i> function partially recapitulate <i>l-cry</i> phenotypes. Molecularly, <i>Platynereis</i> Nr0b1/2 affects steroidogenic and other endocrine pathways, nuclear receptor signaling, and transcription factor orthologs involved in sexual developmental, reproductive, and timing processes in other organisms. Thus, our study suggests profound and direct effects of light on adult animal life-time, likely at least in part via conserved endocrine pathways involved in sexual maturation and reproduction in annelids and vertebrates.