Metazoan Circadian Rhythm: Toward an Understanding of a Light-Based Zeitgeber in Sponges

Integrative and Comparative Biology Integrative and Comparative Biology, volume 53, number 1, pp. 103–117 doi:10.1093/icb/ict001 Society for Integrative and Comparative Biology SYMPOSIUM Metazoan Circadian Rhythm: Toward an Understanding of a Light-Based Zeitgeber in Sponges Werner E. G. Müller,1,* Heinz C. Schröder,* Dario Pisignano,†,‡ Julia S. Markl* and Xiaohong Wang2,*,§ From the symposium ‘‘Keeping Time During Animal Evolution: Conservation and Innovation of the Circadian Clock’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2013 at San Francisco, California. 1 2 E-mail: E-mail: Synopsis 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 30 -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. Introduction All organisms on earth are under the steady influence of environmental factors, e.g. daily or seasonal environmental changes, resulting from the planet’s rotation around its own axis and the sun. It is evident that these changes are driven by physical factors, e.g. light intensity, airflow, water currents, or food supply. It was first proposed in 1995, based on molecular biological data, that sponges evolved first from a common ancestor of all metazoan phyla (Müller 1995), from the Urmetazoa, about 600–1000 million years ago (reviewed by Müller et al. 2007a and Wang et al. 2010). This view was substantiated multifold (e.g., Harcet et al. 2010). Advanced Access publication March 8, 2013 ß The Author 2013. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: . *ERC Advanced Investigator Grant Research Group at Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, Duesbergweg 6, D-55128 Mainz, Germany; †Dipartimento di Matematica e Fisica ‘‘Ennio De Giorgi’’ and National Nanotechnology Laboratory of Istituto Nanoscienze-CNR, Università del Salento, via Arnesano, I-73100 Lecce, Italy; ‡Center for Biomolecular Nanotechnologies, Istituto Italiano di Tecnologia (I.I.T.), via Barsanti 1, I-73010 Arnesano-LE, Italy; §National Research Center for Geoanalysis, 26 Baiwanzhuang Dajie, CN-100037 Beijing, China 104 Light in the darkness of the aquatic environment Luminous planktonic bacteria frequently establish a symbiosis with fish, squid, and other organisms in the aquatic/marine environment (Harvey 1921; Belas et al. 1982) (Fig. 1A). Bacteria (Vibrio sp.) settle on a fish kept for 1–2 days in an open environment. Frequently, growing colonies of luminous bacteria can be photographed by their own light (Fig. 1A). This visible light is produced by living organisms and hence is termed bioluminescence, in contrast to luminescence emitted by a nonliving substance (Haddock et al. 2010). Bioluminescence and also Fig. 1 Bioluminescence (A and B) and biofluorescence in aquatic organisms (E). (A) Bacteria growing on a fish in the air during a 1- to 2-day period. (A-a) Daylight image. (A-b) Dark image. Right panel: a mask layered on top of the bacterial colony prevents bacteria-generated light (logo of the University Mainz). (B) Generation of light (bioluminescent flashing) by tissue from S. domuncula; (B-a) A cube of a dark adapted animal exposed to the detection film. (B-b) The emitted light from a chemiluminescent detection film. A dark spot on the film was resolved following development of the X-ray film. (C) Underwater image showing surface light as seen from the bottom of a tropical sea at a depth of 300 m; the light can be resolved into different qualities of blue. (D) Diving for the Baikalian sponge L. baicalensis, living under an ice cover 1–2 m thick. (E) Biofluorescence. (E-a) A photograph of L. baicalensis taken with a daylight flash and showing sponges with different color variations from green to whitish, dependent on the amount of chlorophyll contained in their algal symbionts. (E-b) Illumination of the same specimens in the dark. Under that condition the biofluorescence residing in the oscules can be monitored; a protruding lobe of the crust is marked (45). The signals emanating from these areas probably originate from symbiotic microorganisms. Partially modified from Wang et al. (2012b). biofluorescence (emission of light by an organic template that has absorbed light from the environment) are much more frequently seen in the marine environment than in freshwater. A well-established biofluorescence is seen in the Lake Baikal sponge Lubomirskia baicalensis (Wiens et al. 2009) (Fig. 1E). This endemic sponge lives in a symbiotic relationship with dinoflagellates (Müller et al. 2006a), an interaction that allows the sponges to survive for Careful studies of the different metabolic pathways in sponges revealed that these multicellular animals already comprise all basic structural and functional systems known from higher metazoan taxa, with the exception of the nervous and contractile systems (Müller et al. 2004). It is well established that in mammals there is a circadian syste (...truncated)