The transformation of energy metabolism and Endoplasmic Reticulum stress regulation in Pacific oyster Crassostrea gigas under air exposure

The Pacific oyster Crassostrea gigas is an important species living in the intertidal zones. It is of great significance to study the mechanism of oysters to adapt air exposure. In the present study, weighted gene co-expression network analysis (WGCNA) with the transcriptome data of gills and adductor muscle was conducted to investigate the metabolic transformation of C. gigas under air exposure. GO enrichment of modules specifically expressed in adductor muscle of oysters exposed to air for five, seven and nine days revealed the phased expression of respiratory chain, protein turnover and lipid metabolism, indicating the conversion of energy metabolism. During air exposure, “respiratory chain” and “ribosome biogenesis” were enriched in the muscle on the fifth day, suggesting that glycogen metabolism was dominant in the early stages of air exposure. On the seventh day, many terms about the regulation of proteolysis were enriched, indicating that carbohydrates were not be able to meet the metabolic needs in the oyster adductor muscle, and proteins began to be degraded for energy supply. The processes related to lipid metabolism were enriched on the ninth day. The extremely high glycogen content of C. gigas allowed it to maintain a basic metabolic activity for a long time with a conservative compensation strategy. GO and KEGG enrichments of the modules sensitive to air exposure in gills were mainly involved in “response to endoplasmic reticulum stress”, “Endoplasmic Reticulum (ER) to Golgi transport vesicle membrane” and “protein processing in endoplasmic reticulum”. It revealed that the mechanism of oyster adapting to air exposure was a complex regulatory network depending on the ER. Hub gene network and PPI network analyses found that some transcription factors containing zinc finger domains regulated the biochemical reactions for stress adaptation, indicating that the ER, as a regulatory element sensitive to external stress, could regulate apoptosis, autophagy and protein degradation in gills of C. gigas under air exposure. These results would provide new insights into the adaptation of C. gigas to air exposure in terms of energy metabolism and homeostasis.