Exploring hypoxia-triggered edema in sea cucumbers: Molecular perspectives on environmental stress

Abstract

Intensified human activities in coastal zones (e.g. nutrient pollution, coastal development) and climate change reduce solubility and enhance water stratification, and have been driving the expansion and intensification of hypoxic zones globally. When exposed to hypoxic stress, some sea cucumbers become edematous (swollen with excessive fluid) and are more susceptible to mortality. However, the difference of specific phenotype indicators between edematous sea cucumber and non-edematous sea cucumber, and the mechanism underpinning edematous is not clear. Here, we exposed the ecologically valuable sea cucumbers species Apostichopus japonicus, which has an economic impact of >US$45 bn annually, to acute hypoxia (2 mg/L) to elucidate the physiological and molecular mechanisms which underpin edematous. We found that the percent of body wall weight (Wbw) in wet weight (Ww) was higher in normoxia sea cucumbers (53.49 %–53.80 %) than edematous sea cucumbers (43.32 %–44.80 %), indicating edematous sea cucumber contains excessive seawater inside the body to transport more oxygen to cope with hypoxia. The co-identified up-regulated mRNAs (i.e. ficolin-2, metalloproteinase inhibitor 3-like, and complement component C3) and down-regulated mRNAs (i.e. receptor-type tyrosine-protein phosphatase epsilon, PR domain zinc finger protein 2, and protein NLRC5-like) in both respiratory tree and tube foot were crucial. In edematous sea cucumbers, up-regulated genes were largely involved in “metabolism of cofactors and vitamins” and “folding, sorting and degradation,” while genes involved in “signal transduction” and “immune system” were largely down-regulated. Retinol metabolism and Phospholipase D signaling pathways participated in regulating sea cucumber edema but have varied patterns. Overall, we provide insights into the molecular mechanism underpinning sea cucumber edema and help to understand the response of sea cucumbers to increasingly oxygen-limited future oceans.