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Multiple environmental stressors caused by global warming influence the regulation of proteins involved in various biological processes in aquatic organisms. As an important component of the marine ecosystem, sea cucumber is a suitable echinoderm species for researching stress responses. In this study, we have investigated the proteomic response of respiratory trees in the sea cucumber Apostichopus japonicus, challenged with environmental stresses by using the iTRAQ technique. Results showed that 262, 155 and 433 proteins were differentially regulated in response to heat, hypoxia, and heat plus hypoxia, respectively. Expression of key genes and proteins were measured by real-time PCR and western blot to validate the accuracy of the proteome files. Results showed that the interaction between these two stressors has an additive effect at the proteome level. Proteins involved in amino acid and carbohydrate metabolic processes were largely induced by heat while repressed by hypoxia. Exposure to multiple climate change stressors caused several proteins involved in lipid metabolic progress to be down-regulated and lipid catabolic processes were induced. Additionally, hypoxia and the combined stress induced proteins involved in iron homeostasis. ATP synthesis and gluconeogenesis were induced under heat and the combined stress, while ATP and glycogen synthesis were depressed under hypoxia. Proteins related with immune and defense response were largely induced and protein synthesis ability was depressed under all three stresses. Thus, sea cucumber may adopt different strategies to cope with varied environmental stress, and the situation in heat group is more similar with the combined treatment than hypoxia group. These proteomic changes in response to high-temperature and low-oxygen levels may provide insights into the defense strategies of sea cucumber in response to global climate changes.

Significance of the study: The study focused on comparative quantitative proteomics on Apostichopus japonicus respiratory tree using iTRAQ in responses to multiple climate change stressors: heat, hypoxia and the combined stress. Data showed that A. japonicus can have an acute reaction in diverse biological pathways to both individual and interacting environmental stress, including substance metabolism, signal transduction, protein synthesis, immune response and energy production. Results indicated that sea cucumber adopted different strategies to cope with varied environmental stress, and the interaction between these two stressors has an additive effect at the proteome level. These results offer insight into the molecular regulation of A. japonicus to multiple environmental stress and reveal possible molecular events in sea cucumber under climate changes. The understanding of adaptive variation under global climate changes in aquatic organisms could be improved.