Comprehensive whole transcriptome analysis reveals specific lncRNA, circRNA and miRNA-mRNA networks of pearl oyster (Pinctada fucata martensii) in response to hypoxia stress

Hypoxia is a prevalent environmental stressor in both natural and aquaculture environments. Pinctada fucata martensii , a commercially valuable pearl oyster species, is particularly susceptible to hypoxic stress in aquaculture. To explore its molecular response to short-term hypoxia, whole-transcriptome sequencing was performed on gill tissues under normoxic and hypoxic conditions. A total of 721 differentially expressed mRNAs (DEmRNAs), 259 long non-coding RNAs (DElncRNAs), 55 circular RNAs (DEcircRNAs), and 17 microRNAs (DEmiRNAs) were identified. Based on predicted interactions among these differentially expressed RNAs, a competing endogenous RNA (ceRNA) network was constructed, consisting of 9 DElncRNAs, 10 DEcircRNAs, 3 DEmiRNAs, and 6 DEmRNAs. Six DElncRNAs and three DEcircRNAs were predicted to interact with miR-152, and the axis-mediated activation of target genes—ALDH5A1 and SLC23A2, FAT4 and CCDC97, and LAC—was implicated in the modulation of metabolic pathways, enzyme activity, antioxidant defenses, thereby promoting antioxidant capacity and suppressing cell growth as part of an adaptive survival strategy. This ceRNA network reveals a key molecular hub that links hypoxia sensing to immunomodulatory mechanisms. Moreover, the co-repression of stress-response genes HSP20 and HSP70 in this network enhances hypoxic tolerance increased energy utilization efficiency and regulation of RNA. Functional analysis of the network revealed enrichment in pathways related to energy metabolism, antioxidant defense, and RNA splicing regulation. These findings provide novel insights into transcriptomic regulation and adaptive mechanisms in bivalves under hypoxic stress. • Construct a ceRNA network with 9 DElncRNAs, 10 DEcircRNAs, 3 DEmiRNAs, and 6 DEmRNAs. • CeRNA networks are critically involved in the molecular response to hypoxia. • Hypoxia drives ceRNA-based regulation of metabolism, antioxidation, and RNA splicing.