The phenomena of enhanced protection of innate immunity responding to a pre-exposed pathogen have been reported in invertebrates. The underpinning molecular basis and mechanism for the enhanced immune protection are still missing. In order to explore the possible molecular basis for enhanced immune protection in molluscs, the transcriptomic analysis of oysters Crassostrea gigas hemocytes after twice stimulation of Vibrio splendidus were conducted, and a total of 403 M clean reads and 34254 differentially expressed genes (DEGs) were collected. There were 2964 common DEGs up-regulated in hemocytes after both the first and second immune stimulation, which were mostly enriched in metabolic processes and immune related pathways, such as endocytosis, MAPK signaling pathway and TLR signal pathway. Moreover, 187 and 55 DEGs were higher expressed at resting (0 h after stimulation) and activating state (12 h after stimulation) of the second immune response than that of the first response, respectively, mainly including immune recognition receptor scavenger receptor 2, signal molecule MAPK2, immune regulator IL17-d, apoptosis inhibitor IAP and effector cathepsin. More importantly, 13 DEGs were long-lastingly higher expressed at both the resting and activating state within the second immune response than that of the first, including TLR signal molecule MyD88, anti-virulent tissue inhibitor of metalloproteinase, anti-bacterial proline-rich transmembrane protein, which might play indispensable roles in enhanced immune protection against V. splendidus re-infection. The expression patterns of TLR signals (CgTLR6 and CgMyD88) and effector molecules (CgTIMP and CgPRTP) were further validated by RT-PCR, which were consistent to transcriptomic results. All the results provided an overall molecular basis of enhanced immune protection for hemocytes defensing against the second stimulation of V. splendidus in oyster, which would be valuable for understanding the protection mechanisms of pre-exposure in invertebrates.
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