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ORIGINAL RESEARCH article

Front. Immunol.
Sec. Comparative Immunology
Volume 16 - 2025 | doi: 10.3389/fimmu.2025.1536562

Evidence for trans-generational immune priming against Vibrio splendidus in the oyster Crassostrea gigas

Provisionally accepted

The final, formatted version of the article will be published soon.

    Cumulative evidences have demonstrated the occurrence of trans-generational immune priming (TGIP) in invertebrates, while the detail substances transferred and the mechanism of this transmission remains unclear. In the present study, we tested firstly for TGIP in the larvae offspring of the oyster Crassostrea gigas after parental challenge with Vibrio splendidus during spawning season. Upon the maternal oyster primed with V. splendidus, the enzyme activities (lysozyme and SOD), NO level, the expressions of immune genes (CgTLR2, CgMACPF and CgFBG), as well as the antibacterial activities were significantly enhanced in the eggs from V. splendidus primed female oysters, indicating that V. splendidus stimulation promoted the immunity tendentiously transferred to eggs during spawning season. After fertilization, the enzyme activities of CAT, lysozyme and SOD were significantly enhanced in the maternal primed group (mVs-Sw (M)) during the early oyster ontogeny, while there were no detectable differences between control group (nSw-Sw (N)) and paternal primed group (pVs-Sw (P)). However, the expressions of immune genes (CgGalectin, CgMyd88 and CgLBP) were both increased in parental primed groups (mVs-Sw (M) and pVs-Sw (P)). After the larvae offspring exposed to the secondary V. splendidus stimulation, the mortality rates in parental TGIP groups (mVs-Vs (M1) and pVs-Vs (P1)) were significantly lower, while the hatching rates were significantly higher than that in the nSw-Vs (N1), confirming that parents' immunology experience enhanced their offspring survival rates as well as the resistance to pathogen infection. Transcriptome data revealed that differentially expressed genes are enriched in immunity, signal transduction, energy metabolism and development in parental TGIP groups. Notably, the expressions of three DNMTs were all significantly up-regulated during the early ontogeny in the maternal primed groups (mVs-Sw (M)), while sharply increased after entering into D-veliger larvae in the paternal primed group (pVs-Sw (P)), suggesting the potential regulation of DNA methylation during the oyster TGIP. Moreover, the expressions of E3 ligases (CgWWP1, CgSmurf2, CgNedd4, and CgMarch5) were significantly increased at D-veliger and early umbo larvae stage post V. splendidus stimulation, indicating their immune role during the oyster ontogeny. These results firstly showed evidence for bacteria induced TGIP and potential mechanism in molluscs.

    Keywords: Trans-generational immune priming, Crassostrea gigas, Transcriptomic analyses, DNA methyltransferases, E3 ligase

    Received: 29 Nov 2024; Accepted: 08 Jan 2025.

    Copyright: © 2025 Song, Wang, Dong, Liu, Yang, Wang and Song. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence: Lingling Wang, Dalian Ocean University, Dalian, China

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