{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T03:42:00Z","timestamp":1789098120252,"version":"build-2803163510"},"reference-count":42,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2026,4,1]],"date-time":"2026-04-01T00:00:00Z","timestamp":1775001600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"JSPS KAKENHI","award":["JP 22H02440"],"award-info":[{"award-number":["JP 22H02440"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Among accumulating knowledge of invertebrate immune-like responses, antiviral mechanisms in mollusks remain poorly understood. Pinctada birnavirus (PiBV) infects the mantle epithelial cells of the pearl oyster (Pinctada fucata), causing mass mortality of juveniles during high-temperature periods. Here, we examined immune memory-like responses of pearl oysters to PiBV reinfection. At a high temperature (24\u201325 \u00b0C), experimental infection caused ~80% mortality, whereas mortality remained &lt;30% and did not differ significantly from uninfected controls at a lower temperature (18\u201320 \u00b0C). Juveniles that survived infection at the low temperature and were subsequently reinfected at the higher temperature showed 10% mortality, which was significantly lower than the ~50% observed in na\u00efve oysters infected under the same conditions. At 28 days post-infection at the lower temperature, oysters exhibited gene expression profiles distinct from those of na\u00efve oysters. Ex vivo infection demonstrated significantly reduced PiBV replication in mantle explants from previously infected oysters compared with those from na\u00efve individuals. These findings indicate that P. fucata acquires resistance to PiBV reinfection, and at least part of this resistance is mediated within the mantle, independently of other tissues. Culture supernatants of mantle explants from previously infected oysters were positive for viral genomic RNA even without viral inoculation, suggesting that persistent infection may contribute to the maintenance of immune-like responses.<\/jats:p>","DOI":"10.3390\/pathogens15040380","type":"journal-article","created":{"date-parts":[[2026,4,2]],"date-time":"2026-04-02T07:57:55Z","timestamp":1775116675000},"page":"380","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Immune Memory-like Responses of Akoya Pearl Oyster to Pinctada Birnavirus"],"prefix":"10.3390","volume":"15","author":[{"given":"Tomomasa","family":"Matsuyama","sequence":"first","affiliation":[{"name":"Japan Fisheries Research and Education Agency, Pathology Division, Aquaculture Research Department, Fisheries Technology Institute, Minami-Ise 516-0193, Mie, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6550-6852","authenticated-orcid":false,"given":"Kousuke","family":"Umeda","sequence":"additional","affiliation":[{"name":"Japan Fisheries Research and Education Agency, Pathology Division, Aquaculture Research Department, Fisheries Technology Institute, Minami-Ise 516-0193, Mie, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takashi","family":"Atsumi","sequence":"additional","affiliation":[{"name":"Mie Prefecture Fisheries Research Institute, Shima 517-0404, Mie, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,4,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"7209","DOI":"10.4049\/jimmunol.179.11.7209","article-title":"Invertebrate immune systems\u2014Specific, quasi-specific, or nonspecific?","volume":"179","author":"Rowley","year":"2007","journal-title":"J. Immunol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"jeb246158","DOI":"10.1242\/jeb.246158","article-title":"The plasticity of immune memory in invertebrates","volume":"227","year":"2024","journal-title":"J. Exp. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Boraschi, D., and Italiani, P. (2018). Innate immune memory: Adopting correct terminology. Front. Immunol., 9.","DOI":"10.3389\/fimmu.2018.00799"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.fsi.2020.06.047","article-title":"Peculiarities of innate immune memory in crustaceans","volume":"104","author":"Low","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1111\/raq.12482","article-title":"Immune responses and immunoprotection in crustaceans with special reference to shrimp","volume":"13","author":"Kulkarni","year":"2021","journal-title":"Rev. Aquac."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"104528","DOI":"10.1016\/j.dci.2022.104528","article-title":"The honey bees immune memory","volume":"138","author":"Burciaga","year":"2023","journal-title":"Dev. Comp. Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.1111\/raq.12906","article-title":"Trained immunity in marine mollusc aquaculture","volume":"16","author":"Montagnani","year":"2024","journal-title":"Rev. Aquac."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2471","DOI":"10.1099\/jgv.0.000244","article-title":"Antiviral immunity in marine molluscs","volume":"96","author":"Green","year":"2015","journal-title":"J. Gen. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"13143","DOI":"10.1038\/s41598-017-13564-0","article-title":"Long-lasting antiviral innate immune priming in the lophotrochozoan Pacific oyster, Crassostrea gigas","volume":"7","author":"Lafont","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e02777-19","DOI":"10.1128\/mBio.02777-19","article-title":"A sustained immune response supports long-term antiviral immune priming in the Pacific oyster Crassostrea gigas","volume":"11","author":"Lafont","year":"2020","journal-title":"mBio"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"de Kantzow, M., Hick, P.M., and Whittington, R.J. (2023). Immune priming of Pacific oysters to induce resistance to OsHV-1. Viruses, 15.","DOI":"10.3390\/v15091943"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Morga, B., M\u00e8ge, M., Faury, N., D\u00e9gremont, L., Petton, B., P\u00e9pin, J.-F., Renault, T., and Montagnani, C. (2024). Antiviral protection against OsHV-1 using UV-inactivated virus. Front. Mar. Sci., 11.","DOI":"10.3389\/fmars.2024.1378511"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Agius, J.R., Ackerly, D., Watson, A.C., Smith, M.L., Beddoe, T., and Helbig, K.J. (2025). Reducing the impact of HaHV-1 in Australian abalone: The role of age and immune priming. bioRxiv, preprint.","DOI":"10.1101\/2025.04.14.648835"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.jip.2017.01.009","article-title":"Viruses infecting marine molluscs","volume":"147","author":"Arzul","year":"2017","journal-title":"J. Invertebr. Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e12180","DOI":"10.7717\/peerj.12180","article-title":"Mass mortality of pearl oyster (Pinctada fucata) in Japan in 2019\u20132020 is caused by an unidentified infectious agent","volume":"9","author":"Matsuyama","year":"2021","journal-title":"PeerJ"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e17321","DOI":"10.7717\/peerj.17321","article-title":"A novel birnavirus identified as the causative agent of summer atrophy of pearl oyster (Pinctada fucata)","volume":"12","author":"Matsuyama","year":"2024","journal-title":"PeerJ"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"740218","DOI":"10.1016\/j.aquaculture.2023.740218","article-title":"Electron probe microanalysis and gene expression analysis of melanization caused by summer atrophy virus in Akoya pearl oyster","volume":"579","author":"Sano","year":"2024","journal-title":"Aquaculture"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Matsuyama, T., Atsumi, T., Kiryu, I., Umeda, K., and Morimoto, N. (2025). Ex vivo propagation of Pinctada birnavirus using mantle tissue fragment culture. Pathogens, 14.","DOI":"10.3390\/pathogens14010076"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/s12562-024-01834-6","article-title":"Effects of water temperature and infection history on the severity of summer atrophy in juvenile Akoya pearl oyster Pinctada fucata martensii","volume":"91","author":"Hashimoto","year":"2025","journal-title":"Fish. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"143","DOI":"10.3147\/jsfp.59.143","article-title":"Monitoring survey of summer atrophy in juvenile Akoya pearl oyster Pinctada fucata in the central Uwajima Sea area","volume":"59","author":"Shinomiya","year":"2024","journal-title":"Fish Pathol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"20160857","DOI":"10.1098\/rspb.2016.0857","article-title":"Cementing mussels to oysters in the pteriomorphian tree: A phylogenomic approach","volume":"283","author":"Lemer","year":"2016","journal-title":"Proc. R. Soc. B"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"dsac035","DOI":"10.1093\/dnares\/dsac035","article-title":"A high-quality, haplotype-phased genome reconstruction reveals unexpected haplotype diversity in a pearl oyster","volume":"29","author":"Takeuchi","year":"2022","journal-title":"DNA Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A scaling normalization method for differential expression analysis of RNA-seq data","volume":"11","author":"Robinson","year":"2010","journal-title":"Genome Biol."},{"key":"ref_24","unstructured":"R Core Team (2025). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/s41592-021-01101-x","article-title":"Sensitive protein alignments at tree-of-life scale using DIAMOND","volume":"18","author":"Buchfink","year":"2021","journal-title":"Nat. Methods"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1093\/bioinformatics\/btu031","article-title":"InterProScan 5: Genome-scale protein function classification","volume":"30","author":"Jones","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1089\/omi.2011.0118","article-title":"clusterProfiler: An R package for comparing biological themes among gene clusters","volume":"16","author":"Yu","year":"2012","journal-title":"OMICS"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1093\/nar\/gkn176","article-title":"High-throughput functional annotation and data mining with the Blast2GO suite","volume":"36","author":"Terol","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Agius, J.R., Corbeil, S., and Helbig, K.J. (2020). Immune control of herpesvirus infection in molluscs. Pathogens, 9.","DOI":"10.3390\/pathogens9080618"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.jip.2017.05.004","article-title":"Detection of Ostreid herpesvirus-1 microvariants in healthy Crassostrea gigas following disease events and their possible role as reservoirs of infection","volume":"148","author":"Evans","year":"2017","journal-title":"J. Invertebr. Pathol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.aquaculture.2019.04.035","article-title":"Prior exposure to Ostreid herpesvirus 1 (OsHV-1) at 18 \u00b0C is associated with improved survival of juvenile Pacific oysters (Crassostrea gigas) following challenge at 22 \u00b0C","volume":"507","author":"Whittington","year":"2019","journal-title":"Aquaculture"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Liu, O.M., Hick, P.M., and Whittington, R.J. (2023). The resistance to lethal challenge with Ostreid herpesvirus-1 of Pacific oysters (Crassostrea gigas) previously exposed to this virus. Viruses, 15.","DOI":"10.3390\/v15081706"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1016\/j.fsi.2013.04.051","article-title":"Poly I:C Induces a Protective Antiviral Immune Response in the Pacific Oyster (Crassostrea gigas) against Subsequent Challenge with Ostreid Herpesvirus (OsHV-1 \u03bcVar)","volume":"35","author":"Green","year":"2013","journal-title":"Fish Shellfish Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Delisle, L., Rolton, A., and Vignier, J. (2023). Inactivated Ostreid Herpesvirus-1 Induces an Innate Immune Response in the Pacific Oyster, Crassostrea gigas, Hemocytes. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1161145"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.molimm.2016.09.002","article-title":"Primed for success: Oyster parents treated with poly(I:C) produce offspring with enhanced protection against Ostreid herpesvirus 1 infection","volume":"78","author":"Green","year":"2016","journal-title":"Mol. Immunol."},{"key":"ref_36","first-page":"3671","article-title":"Long dsRNAs promote an antiviral response in Pacific oyster hampering Ostreid herpesvirus 1 replication","volume":"220","author":"Pauletto","year":"2017","journal-title":"J. Exp. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Segarra, A., Mauduit, F., Faury, N., Trancart, S., D\u00e9gremont, L., Tourbiez, D., Haffner, P., Barbosa-Solomieu, V., P\u00e9pin, J.-F., and Travers, M.-A. (2014). Dual Transcriptomics of Virus-Host Interactions: Comparing Two Pacific Oyster Families Presenting Contrasted Susceptibility to Ostreid Herpesvirus 1. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-580"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e00011-22","DOI":"10.1128\/msphere.00011-22","article-title":"ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations","volume":"7","author":"Rosani","year":"2022","journal-title":"mSphere"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Picot, S., Faury, N., Pelletier, C., Arzul, I., Chollet, B., D\u00e9gremont, L., Renault, T., and Morga, B. (2022). Monitoring Autophagy at Cellular and Molecular Level in Crassostrea gigas during an Experimental Ostreid Herpesvirus 1 (OsHV-1) Infection. Front. Cell. Infect. Microbiol., 12.","DOI":"10.3389\/fcimb.2022.858311"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/j.fsi.2022.10.058","article-title":"Diverse transcriptomic responses of Pinctada fucata martensii after different PAMP stimulation","volume":"131","author":"Lu","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"109091","DOI":"10.1016\/j.fsi.2023.109091","article-title":"Toll-like receptor involvement in acquired immune response of Pinctada fucata","volume":"141","author":"Bai","year":"2023","journal-title":"Fish Shellfish Immunol."},{"key":"ref_42","first-page":"414","article-title":"Review of factors affecting microbial survival in groundwater","volume":"77","author":"John","year":"2011","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/4\/380\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,2]],"date-time":"2026-04-02T08:10:21Z","timestamp":1775117421000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/4\/380"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,1]]},"references-count":42,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2026,4]]}},"alternative-id":["pathogens15040380"],"URL":"https:\/\/doi.org\/10.3390\/pathogens15040380","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,1]]}}}