Single-Larva RNA Sequencing Reveals That Red Sea Urchin Larvae Are Vulnerable to Co-Occurring Ocean Acidification and Hypoxia

Abstract

Anthropogenic carbon dioxide emissions have been increasing rapidly in recent years, driving pH and oxygen levels to record low concentrations in the oceans. Eastern boundary upwelling systems such as the California Current System (CCS) experience exacerbated ocean acidification and hypoxia (OAH) due to the physical and chemical properties of the transported deeper waters. Research efforts have significantly increased in recent years to investigate the deleterious effects of climate change on marine species, but have not focused on the impacts of simultaneous OAH stressor exposure. Additionally, few studies have explored the physiological impacts of these environmental stressors on the earliest life stages, which are more vulnerable and represent natural population bottlenecks in organismal life cycles. The physiological response of the ecologically and commercially important red sea urchin (Mesocentrotus franciscanus) was assessed by exposing larvae to a variety of OAH conditions, mimicking the range of ecologically relevant conditions encountered currently and in the near future along the CCS. Skeleton dissolution, larval development, and gene expression show a response with clearly delineated thresholds that were related to OAH severity. Skeletal dissolution and the induction of Acid-sensing Ion Channel 1A at pH 7.94/5.70 DO mg/L provide particularly sensitive markers of OAH, with dramatic shifts in larval morphology and gene expression detected at the pH/DO transition of 7.71/3.71–7.27/2.72 mg/L. Experimental simulations that describe physiological thresholds and establish molecular markers of OAH exposure will provide fishery management with the tools to predict patterns of larval recruitment and forecast population dynamics.