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Acetylome Analysis Reveals Population Differentiation of the Pacific Oyster Crassostrea gigas in Response to Heat Stress

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Abstract

Lysine acetylation of proteins is a highly conserved post-translational modification that plays an important regulatory role in almost every aspect of metabolic processes in both terrestrial and aquatic species. Pacific oyster, Crassostrea gigas, a model marine species, is distributed worldwide and is economically and ecologically important. However, little is known about the role of acetylation in the adaptive response of oyster to heterogeneous intertidal environments. Here, we conducted the first-ever lysine acetylome analysis in two genetically and physiologically differentiated oyster populations, using a highly sensitive immune-affinity purification and high-resolution mass spectrometry. Overall, we identified 1054 lysine acetylation sites in 664 proteins, which account for 2.37% of the oyster proteome analysed in the current study. The modified proteins are involved in a wide range of biological processes and are localised in multiple cellular compartments. Motif analysis revealed that hydrophilic and polar amino acids histidine, lysine and arginine were the most enriched residues in the positions + 1 and + 2 of the acetylated sites. Further, the two oyster populations exhibited divergent acetylomic regulations of several biological pathways, particularly energy metabolism and glycine and serine amino acid metabolism, in response to thermal stress and differentiated acetylation patters of candidate heat-responsive proteins, e.g. molecular chaperone and myosin. These observations suggest that lysine acetylation plays a critical role in different thermal responses of these two oyster populations. These findings provide an important resource for in-depth exploration of the physiological role of lysine acetylation in adaptive evolution of marine invertebrates.

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Data Accessibility

The proteome and acetylome data are available via the ProteomeXchange Consortium under the identifier PXD008057 (https://www.ebi.ac.uk/pride/ archive/projects/PXD008057).

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Acknowledgements

We are grateful to Mr. Runshan Du, Xuegang Wang and Dr. Xueying Tang for breeding the F1 progeny and culturing the oysters in the sea and in the laboratory.

Funding

This was supported by thr National Key R &D Program of China [2018YFD0900304 to L.L], Project funded by China Postdoctoral Science Foundation [2019TQ0324 to A. L.], the National Natural Science Foundation of China [31572620 to L.L], and the Modern Agro-industry Technology Research System [CARS-49 to L.L].

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L.L. and G.Z. conceived the study and helped draft the manuscript; A.L. performed the molecular laboratory work, participated in data analysis and drafted the manuscript; L.L. and W.W. collected oyster samples and were involved in the breeding of the F1 progeny. All authors gave final approval for the publication.

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Correspondence to Li Li.

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Li, A., Li, L., Wang, W. et al. Acetylome Analysis Reveals Population Differentiation of the Pacific Oyster Crassostrea gigas in Response to Heat Stress. Mar Biotechnol 22, 233–245 (2020). https://doi.org/10.1007/s10126-020-09947-6

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