Microevolution of the oxidative stress response: organismal and transcriptomic effects of peroxide exposure in the starlet sea anemone Nematostella vectensis

The starlet sea anemone, Nematostella vectensis (phylum Cnidaria, class Anthozoa), inhabits tidal marshes along the Atlantic coast of North America. These shallow coastal habitats are subject to extreme environmental variability, including fluctuating levels of reactive oxygen species (ROS). High ROS concentrations can be cytotoxic and lead to oxidative stress. Given the importance of tidal marshes for marine biodiversity and their susceptibility to oxidative stress, it is important to study how resident organisms counteract oxidative stress. N. vectensis is an excellent model system for addressing the evolution of oxidative stress mechanisms because (1) this anemone exhibits tolerance to a variety of environmental stressors, (2) there is clear evidence of local adaptation to stress in different populations and sub-populations, and (3) protein-coding polymorphisms have been identified, some in proteins that are implicated in stress response. I exposed fifteen different clone lines of N. vectensis collected from four estuaries to biologically relevant levels of hydrogen peroxide. Pronounced differences are apparent between clone lines collected from Meadowlands, NJ, Baruch, SC, and Kingsport, NS, as well as among twelve clones collected at a single Cape Cod marsh. This is the first study that demonstrates intraspecific variation in the oxidative stress response of N. vectensis. To understand how the peroxide response of these clones might differ at the level of gene expression, I sequenced the transcriptomes of 7 clone lines under control conditions and when exposed to survivable levels of peroxide for 24 h. I found survivable peroxide exposure induces robust and repeatable changes in gene expression, including the up-regulation of genes shown to be associated with cellular responses to oxidative stress, thermal stress, and UV stress, and down-regulation of genes that promote generation of ROS, including the enzymes involved in oxidative phosphorylation. Additionally, I identified pronounced differences in the peroxide-induced transcriptional profiles between genets of N. vectensis. The existence of a conserved oxidative stress response has major implications for studies on how other cnidarians, particularly corals, will withstand the impacts of climate change. Indeed, the proximal cause of coral bleaching--the major threat to corals worldwide--is oxidative stress