Exploring Endoplasmic Reticulum Stress Pathways in Apostichopus japonicus Under Heat Stress Based on Transcriptome Analysis

Abstract

Abstract Background High summer temperatures caused by changes in the global environment have significant impacts on marine organisms. The sea cucumber Apostichopus japonicus is a representative marine benthic organism and an economically important shallow-sea aquaculture species in China, and thus it is necessary to explore its response to environmental heat stress. Results Endoplasmic reticulum stress is an important regulatory strategy for organisms to respond to changes in the environment, and thus we analyzed the histology, ultrastructure, and transcriptome of the digestive tract of A. japonicus at three temperatures: normal (18°C), summer dormant (25°C), and lethal (32°C). Histological and ultrastructural results showed that heat stress caused morphological changes in the digestive tract of A. japonicus and inflicted alterations and damage to the endoplasmic reticulum of the enterocytes. Totals of 603 and 4615 differentially expressed genes were identified by transcriptome sequencing in the T25-vs-T18 and the T32-vs-T25 group comparisons, respectively. The GO results showed that DEGs in both group comparisons were significantly enriched in protein folding, chaperonin-mediated protein folding, and other protein-related GO terms. Also, KEGG enrichment analysis showed that both groups activated the pathway of protein processing in the endoplasmic reticulum and induced the endoplasmic reticulum stress response. The endoplasmic reticulum molecular chaperones, including BiP, GRP94, and Hsp70, were all up-regulated in expression. At 32°C, in addition to the above endoplasmic reticulum molecular chaperones, the endoplasmic reticulum molecular receptors PERK, TRAF2, and XBP, which are downstream of endoplasmic reticulum stress in the unfolded protein response, were also up-regulated. Conclusions This study has characterized the internal molecular regulatory process of A. japonicus under heat stress from the perspective of endoplasmic reticulum stress and provides clues regarding the mechanisms behind homeostatic regulation in invertebrates under stress from the environment.