Comparative proteomics reveal the humoral immune rejection of pearl oyster Pinctada fucata to xenograft from Pinctada maxima

Abstract

To investigate the mechanism underlying immune rejection in pearl oyster Pinctada fucata following allograft (P. fucata mantle pieces) and xenograft (P. maxima mantle pieces) transplantations, we analyzed serum samples collected at multiple time points (6, 12, 24, 48, 96, 144, and 192 h) after transplantation using a proteomics approach. We identified 2127 proteins with high confidence according to the selected peptides (false discovery rate = 0.01), among which 1148 exhibited quantitative differences. Functional enrichment analysis revealed significant changes in protein functional categories, including signal transduction, translation, cytoskeleton, and post-translational modifications. Immune-related proteins, such as the ubiquitin-conjugating enzyme E2, apoptosis-linked gene, heat shock protein, and apoptosis inhibitor 5 were associated with allografts and xenografts. Notably, the PI3K-Akt signaling, focal adhesion, and extracellular matrix (ECM)-receptor interaction pathways were enriched among upregulated proteins (xenograft vs. allograft), while the ribosome pathway was enriched among downregulated proteins. These findings suggest that implantation stress may affect protein biosynthesis or activate multiple molecular pathways involved in key immune proteins. Furthermore, the xenograft group demonstrated greater sensitivity in recognizing and responding to foreign substances compared to the allograft group. This heightened responsiveness enabled the xenograft group to rapidly activate humoral immune factors, which triggered the signaling pathway responsible for suppressing the inflammatory response. This study provides novel insights into the immune reactions of host oysters to grafted mantle pieces, particularly xenografts, and may offer strategies to improve xenograft transplantation technologies in the pearl culture industry.