The succinylome of Pinctada fucata martensii implicates lysine succinylation in the allograft-induced stress response

Lysine succinylation is a novel protein post-translational modification associated with the regulation of a variety of cellular processes. Post-translational modifications may regulate the immune response of Pinctada fucata martensii, a marine bivalve used to produce cultured pearls, in response to the surgical implantation of the seed pearl. This allograft-induced stress response may lead to transplant rejection or host death. However, the reg-ulatory effects of post-translational modifications following nucleus insertion surgery in P.f. martensii remain largely unknown. Here, we used 4D label-free quantitative proteomics (4D-LFQ) with LC-MS/MS to explore the effects of nucleus implantation on lysine succinylation in P.f. martensii. We identified 4430 succinylated sites on 964 succinylated proteins in P.f. martensii after nucleus insertion surgery, and seven conserved motifs were identified upstream and downstream of these sites. In total, 269 succinylation sites were differentially expressed in response to implantation (|fold-change| > 1.5 and FDR <1%; 211 upregulation and 58 downregulation), corresponding to 163 differentially expressed succinylated proteins (DESPs; 124 upregulated and 39 down -regulated). The terms over-enriched in the DESPs included cellular processes, metabolic pathways, and binding activity, while the significantly enriched pathways included ECM-receptor interaction, PI3K-Akt signaling, and focal adhesion. EGF-like structural domains, platelet-responsive protein type 1 structural domains, and laminin EGF-like (domains III and V) domains were overrepresented in the DESPs. Parallel reaction-monitoring (PRM) analysis validated 13 DESPs from the proteomics data. The succinylome of P.f. martensii (generated here for the first time) helps to clarify the biological role of large-scale succinylation in this bivalve after nucleus insertion surgery, providing a theoretical basis for further investigations of stress-induced post-translational modifications in other mollusks and extending our knowledge of the molluscan succinylated proteome.

Automated summary

This study explored the effects of nucleus implantation on lysine succinylation in the marine bivalve Pinctada fucata martensii. The researchers identified differentially expressed succinylation sites and proteins in response to implantation and identified overrepresented motifs and pathways associated with the succinylated proteins. The findings provide insights into the biological role of large-scale succinylation in this bivalve after nucleus insertion surgery.