Metazoan circadian rhythm: toward an understanding of a light-based zeitgeber in sponges.

ABSTRACT

In all eukaryotes, the 24-h periodicity in the environment contributed to the evolution of the molecular circadian clock. We studied some elements of a postulated circadian clock circuit in the lowest metazoans, the siliceous sponges. First, we identified in the demosponge Suberites domuncula the enzyme luciferase that generates photons. Then (most likely), the photons generated by luciferase are transmitted via the biosilica glass skeleton of the sponges and are finally harvested by cryptochrome in the same individual; hence, cryptochrome is acting as a photosensor. This information-transduction system, generation of light (luciferase), photon transmission (through the siliceous spicules), and photon reception (cryptochrome), all occur in the same individual. Therefore, we propose that this photoreception/phototransduction process might function as a nerve-cell-like signal transmitting system. This was corroborated by the fact that S. domuncula reacts to different wavelengths of light, originating from the sponge environment, with a differential gene expression of the transcription factor SOX. Recently, we succeeded in demonstrating that in sponges a light/dark controlled gene is expressed, which encodes for nocturnin, a protein showing poly(A)-specific 3'-exoribonuclease activity. Quantitative real-time polymerase chain reaction analyses revealed that primmorphs, 3D cell aggregates of sponge cells, after transfer from light to dark, show a 10-fold increased expression of the nocturnin gene. In contrast, the expression level of the gene encoding glycogenin decreases in the dark by three- to four-fold. It is concluded that sponges are provided with the molecular circadian clock protein nocturnin which is highly expressed in the dark. This finding together with the proposed light-transduction and spicule-based signaling system strongly supports the view that already the lowest metazoans, the sponges, have elements of a circadian rhythm, characteristic of higher metazoans.