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Contribution of HIF-1α to Heat Shock Response by Transcriptional Regulation of HSF1/HSP70 Signaling Pathway in Pacific Oyster, Crassostrea gigas

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Abstract

Ocean temperature rising drastically threatens the adaptation and survival of marine organisms, causing serious ecological impacts and economic losses. It is crucial to understand the adaptive mechanisms of marine organisms in response to high temperature. In this study, a novel regulatory mechanism that is mediated by hypoxia-inducible factor-1α (HIF-1α) was revealed in Pacific oyster (Crassostrea gigas) in response to heat stress. We identified a total of six HIF-1α genes in the C. gigas genome, of which HIF-1α and HIF-1α-like5 were highly induced under heat stress. We found that the HIF-1α and HIF-1α-like5 genes played critical roles in the heat shock response (HSR) through upregulating the expression of heat shock protein (HSP). Knocking down of HIF-1α via RNA interference (RNAi) inhibited the expression of heat shock factor 1 (HSF1) and HSP70 genes in C. gigas under heat stress. Both HIF-1α and HIF-1α-like5 promoted the transcriptional activity of HSF1 by binding to hypoxia response elements (HREs) within the promoter region. Furthermore, the survival of C. gigas under heat stress was significantly decreased after knocking down of HIF-1α. This work for the first time revealed the involvement of HIF-1α/HSF1/HSP70 pathway in response to heat stress in the oyster and provided an insight into adaptive mechanism of bivalves in the face of ocean warming.

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Funding

This study was supported by grant from the National Key Research and Development Program of China (2022YFD2400300), the Key Research and Development Program of Shandong Province (No. 2021ZLGX03), the National Natural Science Foundation of China (Nos. 41976098 and 42276112) and the Agriculture Research System of China Project (CARS-49).

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Authors and Affiliations

  1. Key Laboratory of Mariculture (Ocean University of China), Ministry of Education and College of Fisheries, Ocean University of China, Qingdao, 266003, China

    Huiru Fu, Yongjing Li, Jing Tian, Ben Yang, Yin Li, Qi Li & Shikai Liu

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Qi Li & Shikai Liu

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  1. Huiru Fu
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  2. Yongjing Li
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Contributions

S.L. conceived the study and obtained the funding. H.F., Y.L., and J.T. performed the experiment. H.F., B.Y., and Y.L. analyzed the data. F.H. drafted the manuscript, and S.L. revised the manuscript. Q.L. supervised the work. All authors reviewed manuscript.

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Correspondence to Shikai Liu.

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The C. gigas, C. angulata, and their reciprocal hybrids are neither an endangered nor protected species. All experiments in this study were conducted according to national and institutional guidelines.

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Fu, H., Li, Y., Tian, J. et al. Contribution of HIF-1α to Heat Shock Response by Transcriptional Regulation of HSF1/HSP70 Signaling Pathway in Pacific Oyster, Crassostrea gigas. Mar Biotechnol 25, 691–700 (2023). https://doi.org/10.1007/s10126-023-10231-6

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