Cardiac performance and heart gene network provide dynamic responses of bay scallop Argopecten irradians irradians exposure to marine heatwaves

Abstract

The increased frequency of marine heat waves (MHWs) caused by global climate change is predicted to threaten the survival of economic bivalves, therefore having severely adverse effects on local ecological communities and aquaculture production. However, the study of scallops facing MHWs is still scarce, particularly in the scallop Argopecten irradians irradians, which has a significant share of "blue foods" in northern China. In the present study, bay scallop heart was selected to detect its cardiac performance, oxidative impairment and dynamic molecular responses, accompanied by assessing survival variations of individuals in the simulated scenario of MWHs (32 °C) with different time points (0 h, 6 h, 12 h, 24 h, 3 d, 6 d and 10 d). Notably, cardiac indices heart rate (HR), heart amplitude (HA), rate-amplitude product (RAP) and antioxidant enzyme activities superoxide dismutase (SOD) and catalase (CAT) all peaked at 24 h but sharply dropped on 3 d, coinciding with mortality. Transcriptome analysis revealed that the heart actively defended against heat stress at the acute stage (<24 h) via energy supply, misfolded proteins correction and enhanced signal transduction, whereas regulation of the defense response and apoptotic process combined with twice transcription initiation were the dominant responses at the chronic stage (3-10 d). In particular, HSP70 (heat shock protein 70), HSP90 and CALR (calreticulin) in the endoplasmic reticulum were identified as the hub genes (top 5 %) in the HR-associated module via WGCNA (weighted gene co-expression network analysis) trait-module analysis, followed by characterization of their family members and diverse expression patterns under heat exposure. Furthermore, RNAi-mediated knockdown of CALR expression (after 24 h) significantly weakened the thermotolerance of scallops, as evidenced by a drop of 1.31 °C in ABT (Arrhenius break temperature) between the siRNA-injected group and the control group. Our findings elucidated the dynamic molecular responses at the transcriptome level and verified the cardiac functions of CALR in bay scallops confronted with stimulated MHWs.

Keywords: Argopecten irradians irradians; CALR; Marine heat waves; RNAi; Thermotolerance; Transcriptional regulation.