Hypoxia Disrupts Sex-Specific Physiology and Gene Expression Leading to Decreased Fitness in the Estuarine Sea Anemone Nematostella vectensis

Abstract

Coastal seawater hypoxia is increasing in temperate estuaries under global climate change, yet it is unknown how low oxygen conditions affect most estuarine species. We found that hypoxia has increased since the 1990s in an estuary hosting the sea anemone Nematostella vectensis (Jacques Cousteau National Estuarine Research Reserve, New Jersey, USA). Adult N. vectensis bred from anemones collected in this estuary exposed to three consecutive nights of hypoxia (dissolved oxygen = 0.5–1.5 mg L⁻¹ for ~12 h night⁻¹) during gametogenesis displayed decreased aerobic respiration rates and biomass, indicating metabolic disruption. Physiological declines were correlated with changes in the expression of genes related to oxygen-dependent metabolic processes, many of which are targets of hypoxia-inducible factor 1α (HIF1α), demonstrating the activity of this transcription factor for the first time in this early-diverging metazoan. The upregulation of genes involved in the unfolded protein response and endoplasmic reticulum and Golgi apparatus homeostasis suggested that misfolded proteins contributed to disrupted physiology. Notably, these responses were more pronounced in females, demonstrating sex-specific sensitivity that was also observed in reproductive outcomes, with declines in female but not male fecundity following hypoxia exposure. However, sperm from exposed males had higher mitochondrial membrane potential, indicating altered spermatogenesis. Further, crosses performed with gametes from hypoxia-exposed adults yielded strikingly low developmental success (~2%), yet larvae that did develop displayed similar respiration rates and accelerated settlement compared to controls. Overall, hypoxia depressed fitness in N. vectensis by over 95%, suggesting that even stress-tolerant estuarine species may be threatened by coastal deoxygenation.