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

Xinghai Zhu; Junhao Zhang; Moli Li; Xiujiang Hou; Ancheng Liu; Xuecheng Dong; Wen Wang; Qiang Xing; Xiaoting Huang; Shi Wang; Jingjie Hu; Zhenmin Bao

doi:10.1016/j.scitotenv.2023.163594

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

Sci Total Environ. 2023 Jul 15:882:163594. doi: 10.1016/j.scitotenv.2023.163594. Epub 2023 Apr 23.

Authors

Xinghai Zhu¹, Junhao Zhang¹, Moli Li¹, Xiujiang Hou¹, Ancheng Liu¹, Xuecheng Dong¹, Wen Wang¹, Qiang Xing², Xiaoting Huang¹, Shi Wang³, Jingjie Hu⁴, Zhenmin Bao¹

Affiliations

¹ MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
² MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China. Electronic address: qiangxing@ouc.edu.cn.
³ MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China; Fang Zongxi Center for Marine Evo Devo, Ocean University of China, Qingdao, China.
⁴ MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China; Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution of the Ocean University of China (SOI-OUC), Sanya, China.

PMID: 37094688
DOI: 10.1016/j.scitotenv.2023.163594

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.

MeSH terms

Animals
Gene Expression Profiling
Gene Regulatory Networks*
Pectinidae* / metabolism
Proteins / metabolism
Transcriptome

Substances

Proteins