Transcriptomics Analysis and Re-sequencing Reveal the Mechanism Underlying the Thermotolerance of an Artificial Selection Population of the Pacific Oyster.

Yulong Tan,Rihao Cong,Ying Pan,Li Li,Luping Wang,Haigang Qi,Guofan Zhang

doi:10.3389/fphys.2021.663023

Abstract

The Pacific oyster is a globally important aquaculture species inhabiting the intertidal environment, which experiences great temperature variation. Mass deaths in the summer pose a major challenge for the oyster industry. We initiated an artificial selection breeding program in 2017 using acute heat shock treatments of the parents to select for thermotolerance in oysters. In this study, we compared the respiration rate, summer survival rate, gene expression, and gene structure of F2 selected oysters and non-selected wild oysters. A transcriptional analysis revealed global divergence between the selected and control groups at the larval stage, including 4764 differentially expressed genes, among which 79 genes were heat-responsive genes. Five heat shock proteins were enriched, and four of the six genes (five heat stock genes in the enriched GO terms and KEGG pathways and BAG4) were differentially expressed in 1-year-old oysters. Integration of the transcriptomic and re-sequencing data of the selected and the control groups revealed 1090 genes that differentiated in both gene structure and expression. Two SNPs (single nucleotide polymorphism) that may mediate the expression of CGI_10022585 and CGI_10024709 were validated. In addition, the respiration rate of 1-year-old oysters varied significantly between the selected group and the control group at room temperature (20°C). And the summer survival rate of the selected population was significantly improved. This study not only shows that artificial selection has a significant effect on the gene structure and expression of oysters, but it also helps reveal the mechanism underlying their tolerance of high temperature as well as the ability of oysters to adapt to climate change.

Highlights

The Pacific oyster, Crassostrea gigas (Bivalvia: Ostreidae), is native to the Northwest Pacific Ocean and is widely distributed along the coasts of Japan, Korea, and northern China
One group was used as the parents of the control group, which was further cultured without any treatment; the other group was exposed to 42◦C heat shock for 1 h, and the survivors were used as the parents of the thermotolerance group
The phenotypes, population structure, and gene expression level for thermotolerance were evaluated for the F2 generation

Summary

Introduction

The Pacific oyster, Crassostrea gigas (Bivalvia: Ostreidae), is native to the Northwest Pacific Ocean and is widely distributed along the coasts of Japan, Korea, and northern China. Mass mortality of the Pacific oyster in summer has been observed in many countries since the middle of the 20th century. In the summer of 1992 and 1993, the Pacific oysters from several hatcheries in France had a high mortality rate (90–100%). Most larvae died on the 8th to 10th day, when the mortality rate reached 100% (Tristan et al, 1994a). Mass deaths of Pacific oysters aged 3–7 months, with a mortality rate of 80–90%, were first reported in July 1993 along the Atlantic coast of France (Tristan et al, 1994b). Large numbers of Pacific oysters in China have died because of high temperatures during the summer months since 1994. The individuals that survived showed slow growth, which led to low production (Ma Shaosai et al, 1997; Shui et al, 1997)

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