Environmental sensing and response genes in cnidaria: the chemical defensome in the sea anemone Nematostella vectensis

Abstract

The starlet sea anemone Nematostella vectensis has been recently established as a new model system for the study of the evolution of developmental processes, as cnidaria occupy a key evolutionary position at the base of the bilateria. Cnidaria play important roles in estuarine and reef communities, but are exposed to many environmental stressors.Here I describe the genetic components of a 'chemical defensome' in the genome of N. vectensis, and review cnidarian molecular toxicology. Gene families that defend against chemical stressors and the transcription factors that regulate these genes have been termed a 'chemical defensome,' and include the cytochromes P450 and other oxidases, various conjugating enyzymes, the ATPdependent efflux transporters, oxidative detoxification proteins, as well as various transcription factors. These genes account for about 1% (266/27200) of the predicted genes in the sea anemone genome, similar to the proportion observed in tunicates and humans, but lower than that observed in sea urchins. While there are comparable numbers of stress-response genes, the stress sensor genes appear to be reduced in N. vectensis relative to many model protostomes and deuterostomes. Cnidarian toxicology is understudied, especially given the important ecological roles of many cnidarian species. New genomic resources should stimulate the study of chemical stress sensing and response mechanisms in cnidaria, and allow us to further illuminate the evolution of chemical defense gene networks.

Activation of the cnidarian oxidative stress response by ultraviolet light, polycyclic aromatic hydrocarbons and crude oil

“…Catalase-like activity has also been identified within microperoxisomes (Hand, 1976) and regenerating foot cells (Hoffmeister and Schaller, 1985) of Hydra spp. At the sequence level, searches of genomic and expressed sequence tag (EST) databases of the sea anemones Nematostella vectensis (Goldstone, 2008;Reitzel et al, 2008b) and Aiptasia pallida (Sunagawa et al, 2009), the coral Acropora digitifera (Shinzato et al, 2012) and the hydrozoan Hydra magnapapillata (Shinzato et al, 2012) have demonstrated the presence of multiple genes encoding antioxidant enzymes, including CuZnSODs, MnSODs, catalase, thioredoxins and glutathione peroxidases. Two CuZnSODs have been cloned from A. viridis (Plantivaux et al, 2004), and an extracellular CuZnSOD and a mitochondrial MnSOD have been identified in the freshwater hydrozoan Hydra vulgaris (Dash et al, 2007).…”

Differential Regulation by Heat Stress of Novel Cytochrome P450 Genes from the Dinoflagellate Symbionts of Reef-Building Corals

“…In the phylum Cnidaria, the presence of CYP genes has been demonstrated using expressed sequence tag (EST) sequences from freshwater Hydra sp. (48), and in the sea anemone Nematostella vectensis, CYPs have been recognized as a "chemical defensome" because of their role in protection against chemical stressors (25). In the scleractinian corals, CYP CO (carbon monoxide) difference spectra have been observed for the species Favia fragum, Siderastrea siderea, and Montastraea faveolata (22,47).…”

“…Corals exposed to heat stress produce reactive oxygen species (ROS), mainly in symbiotic dinoflagellates, which destabilize the functionality of the coralalga symbiosis (38,73). The cytochrome P450 hemoproteins are involved in cell detoxification and protection from oxidative stress (25), and therefore we hypothesized that Symbiodinium CYP enzymes would be upregulated in response to thermal stress in the reef-building coral Acropora millepora. In the present study, we aimed to identify cytochrome P450 monooxygenase genes in the coral dinoflagellates and to evaluate the effect of a range of thermal stress scenarios on the expression of CYP genes and their role in the cnidariandinoflagellate symbiosis.…”

An Ancient Model Organism to Test In Vivo Novel Functional Nanocrystals

“…During animal evolution, an array of gene families and pathways (also known as "environmental genes") have evolved to face physical, chemical, and biological stressors. While the immune system responds to biotic stressors such as pathogens (Miller et al, 2007), another set of genes named "chemical defensome" (Goldstone, 2008), has been identified to sense, transform, and eliminate potentially toxic chemicals. Hydra is sensitive to a range of pollutants and has been used to tests on water contamination by heavy metals (Holdway et al, 2001;Pascoe et al, 2003;Pollino and Holdway, 1999).…”

“…In addition, the new genomic resources open the way to the molecular toxicology field. Several gene families that defend against chemical stressors have been identified in other cnidarians and include oxidases, various conjugating enzymes, ATP-dependent efflux transporters, oxidative detoxification proteins, as well as various transcription factors (Goldstone, 2008;Goldstone et al, 2006). The modulation of their expression in Hydra exposed to the new class of stressors, i.e.…”