Circadian Clocks in the Cnidaria: Environmental Entrainment, Molecular Regulation, and Organismal Outputs

Integrative and Comparative Biology Integrative and Comparative Biology, volume 53, number 1, pp. 118–130 doi:10.1093/icb/ict024 Society for Integrative and Comparative Biology SYMPOSIUM Circadian Clocks in the Cnidaria: Environmental Entrainment, Molecular Regulation, and Organismal Outputs Adam M. Reitzel,1,* Ann M. Tarrant† and Oren Levy‡ The first two authors contributed equally to this work. 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 E-mail: Synopsis The circadian clock is a molecular network that translates predictable environmental signals, such as light levels, into organismal responses, including behavior and physiology. Regular oscillations of the molecular components of the clock enable individuals to anticipate regularly fluctuating environmental conditions. Cnidarians play important roles in benthic and pelagic marine environments and also occupy a key evolutionary position as the likely sister group to the bilaterians. Together, these attributes make members of this phylum attractive as models for testing hypotheses on roles for circadian clocks in regulating behavior, physiology, and reproduction as well as those regarding the deep evolutionary conservation of circadian regulatory pathways in animal evolution. Here, we review and synthesize the field of cnidarian circadian biology by discussing the diverse effects of daily light cycles on cnidarians, summarizing the molecular evidence for the conservation of a bilaterian-like circadian clock in anthozoan cnidarians, and presenting new empirical data supporting the presence of a conserved feed-forward loop in the starlet sea anemone, Nematostella vectensis. Furthermore, we discuss critical gaps in our current knowledge about the cnidarian clock, including the functions directly regulated by the clock and the precise molecular interactions that drive the oscillating gene-expression patterns. We conclude that the field of cnidarian circadian biology is moving rapidly toward linking molecular mechanisms with physiology and behavior. Introduction In many habitats, light is a predictable signal that provides information about the environment on daily, lunar, and seasonal time-scales. The need to anticipate and prepare for periodic changes in the environment is strong, evidenced by the nearly universal presence of molecular timekeeping mechanisms in both unicellular and multicellular organisms. Circadian rhythms in behavior and physiology are driven by daily cycles in expression of, interactions between, and degradation of the underlying molecular components. The genes forming the core timing mechanism are not shared among distantly related organisms, for example, bacteria (Xu et al. 2003), plants (Pruneda-Paz and Kay 2010), fungi (Salichos and Rokas 2010), and animals (Harmer et al. 2001; Panda et al. 2002), which suggests that circadian regulation has evolved independently within these lineages (Rosbash 2009). Three main hypotheses have been put forward regarding the driving forces that led to the evolution of circadian clocks. The first hypothesis is that clocks arose primarily to minimize UV damage to DNA by ensuring that replication occurred in the dark. Evidence comes from the presence of blue lightsensitive cryptochromes in plants (Somers et al. 1998) and many animals, including insects (Zhu et al. 2008) and cnidarians (Levy et al. 2007; Reitzel et al. 2010). Light-sensitive cryptochromes provide input to the central clock and are thought Advanced Access publication April 25, 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: . *Department of Biology, University of North Carolina at Charlotte, Charlotte, NC 28223, USA; †Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA; ‡The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, 52900, Israel 119 Cnidarian circadian clock Why cnidarians? Cnidarians, the ‘‘stinging-celled animals’’ that include hydras, jellyfish, corals, and anemones, are intriguing models for circadian research for several reasons. First, the lineages leading to bilaterians and cnidarians diverged early in metazoan evolution, prior to the divergence of protostomes and deuterostomes. The presence of shared regulatory mechanisms between cnidarians and bilaterians should provide insight into the early origins of circadian regulation in animals. By studying early-diverging animals, such as cnidarians, fundamental questions can be addressed regarding the evolution of photosensing, entrainment of circadian clocks, and transduction of light signals to the circadian clock. Second, cnidarians are an ecologically important group, and light regulates the distribution, behavior, and physiology of many cnidarian species (as discussed in the following section). Understanding how cnidarians anticipate, detect, and respond to light and other environmental cues will lead to a more complete understanding of their physiology and ecology. In addition, many reef-building corals and other cnidarians live in symbiotic relationships with photosynthetic dinoflagellates in the genus Symbiodinium. Photosynthesis, growth, and bioluminescence can all exhibit circadian periodicity, both in free-living dinoflagellates (reviewed by Hastings 2007) and in those living within cnidarians or other animal hosts (Sorek and Levy 2012). Many aspects of the physiology of dinoflagellates and their cnidarian hosts are deeply integrated. To give two examples, corals’ calcification rates vary on a daily cycle along with changes in the carbonate chemistry associated with photosynthesis by the symbionts (reviewed by Tambutté et al. 2011), and activities of antioxidant enzymes in scleractinian corals are correlated with rates of photosynthesis in the symbionts (Levy et al. 2006). It is not currently known whether the hosts and/or the symbionts use circadian mechanisms to anticipate some of these daily changes. Furthermore, it is not known whether the two timekeeping pathways (i.e., the host and symbiont clocks) are entirely separate or interact with one another in any way. Organismal responses of cnidarians to light Several aspects of cnidarian biology vary on daily cycles, including vertical migration, larval phototaxis, settlement behavior, expansion and retraction of the body column, and feeding behaviors, including extension of the tentacles (reviewed in Taddei-Ferretti and Musio 2000; Hendricks et al. 2012). Some of these behaviors are directly cued by light or other external signals. For example, simultaneous diel vertical migration of jellyfish has been modeled to result from individual responses to light intensity (Dup (...truncated)