Comparative proteome analysis revealed potential biomarkers and the underlying immune mechanisms in Vibrio-resistant hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂.

Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9881188 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2761 (Electronic) Linking ISSN: 01407775 NLM ISO Abbreviation: J Fish Dis Subsets: MEDLINE

Original Publication: Oxford, Blackwell Scientific Publications.

Fish Diseases*/immunology ; Fish Diseases*/microbiology ; Vibrio Infections*/veterinary ; Vibrio Infections*/immunology ; Proteome* ; Bass*/immunology ; Biomarkers* ; Disease Resistance* ; Fish Proteins*/immunology ; Fish Proteins*/genetics ; Vibrio alginolyticus*/physiology; Animals ; Tandem Mass Spectrometry/veterinary ; Immunity, Innate ; Vibrio/physiology

Vibrio alginolyticus is the causative agent of vibriosis, a common bacterial infection in grouper aquaculture that is associated with the development of haemorrhagic and non-haemorrhagic ulcerations on the fish. In the present study, comparative proteome analysis was performed on serum samples from Vibrio-resistant and Vibrio-susceptible grouper. Samples were analysed using high-throughput LC-MS/MS and identified 2770 unique peptides that corresponded to 344 proteins. Subsequent analysis identified 21 proteins that were significantly up-regulated in the resistant group compared to the control and the susceptible groups. Those proteins are associated with immunostimulatory effects, signalling and binding cascade, metabolism, and maintaining tissue integrity and physiological condition. Besides, potential protein biomarkers related to the immune system were identified, which could be associated with the disease-resistant phenotype. These data provide insights into the underlying immune mechanism of hybrid groupers upon Vibrio sp. infection.
(© 2024 John Wiley & Sons Ltd.)

Albarnaz, J. D., & Weekes, M. P. (2023). Proteomic analysis of antiviral innate immunity. Current Opinion in Virology, 58, 101291. https://doi.org/10.1016/j.coviro.2022.101291.
Bilal, S., Lie, K. K., Dalum, A. S., Karlsen, O. A., & Hordvik, I. (2019). Analysis of immunoglobulin and T cell receptor gene expression in ballan wrasse (Labrus bergylta) revealed an extraordinarily high IgM expression in the gut. Fish & Shellfish Immunology, 87, 650–658. https://doi.org/10.1016/j.fsi.2019.02.007.
Bullingham, O. M. N., Firkus, T. J., Goetz, F. W., Murphy, C. A., & Alderman, S. L. (2022). Lake charr (Salvelinus namaycush) clotting response may act as a plasma biomarker of sea lamprey (Petromyzon marinus) parasitism: Implications for management and wound assessment. Journal of Great Lakes Research, 48(1), 207–218. https://doi.org/10.1016/j.jglr.2021.11.005.
Bunlipatanon, P., & U‐taynapun, K. (2017). Growth performance and disease resistance against Vibrio vulnificus infection of novel hybrid grouper (Epinephelus lanceolatus × Epinephelus fuscoguttatus). Aquaculture Research, 48(4), 1711–1723. https://doi.org/10.1111/are.13008.
Cartwright, J. (2004). Isolation and characterisation of pentraxin‐like serum proteins from the common carp Cyprinus carpio. Developmental & Comparative Immunology, 28(2), 113–125. https://doi.org/10.1016/S0145‐305X(03)00123‐X.
Castro, R., Magadán, S., Jouneau, L., Mhana, V., Pham, H.‐P., Mariotti‐Ferrandiz, E., Six, A., Huetz, F., & Boudinot, P. (2022). Clonotypic IgH response against systemic viral infection in pronephros and spleen of a teleost fish. The Journal of Immunology, 208(11), 2573–2582. https://doi.org/10.4049/jimmunol.2200088.
Cerenius, L., Lee, B. L., & Söderhäll, K. (2008). The proPO‐system: Pros and cons for its role in invertebrate immunity. Trends in Immunology, 29(6), 263–271. https://doi.org/10.1016/j.it.2008.02.009.
Chen, J., Shi, Y., Li, M., Ding, W., & Niu, H. (2008). Molecular cloning of liver angiotensinogen gene in ayu (Plecoglossus altivelis) and mRNA expression changes upon Aeromonas hydrophila infection. Fish & Shellfish Immunology, 24(5), 659–662. https://doi.org/10.1016/j.fsi.2008.01.015.
Chuang, W.‐H., Lee, K.‐K., & Liu, P.‐C. (2013). Characterization of alpha‐2‐macroglobulin from groupers. Fish & Shellfish Immunology, 35(2), 389–398. https://doi.org/10.1016/j.fsi.2013.04.050.
Cook, M., Hayball, P., Nowak, B., & Hayball, J. (2005). The opsonising activity of a pentraxin‐like protein isolated from snapper (Sparidae) serum. Developmental & Comparative Immunology, 29(8), 703–712. https://doi.org/10.1016/j.dci.2004.05.009.
Cuesta, A., Meseguer, J., & Esteban, M. A. (2004). Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.). Veterinary Immunology and Immunopathology, 101(3–4), 203–210. https://doi.org/10.1016/j.vetimm.2004.04.021.
de Mezer, M., Rogaliński, J., Przewoźny, S., Chojnicki, M., Niepolski, L., Sobieska, M., & Przystańska, A. (2023). SERPINA3: Stimulator or inhibitor of pathological changes. Biomedicine, 11(1), 156. https://doi.org/10.3390/biomedicines11010156.
Dhuriya, Y. K., & Sharma, D. (2018). Necroptosis: A regulated inflammatory mode of cell death. Journal of Neuroinflammation, 15(1), 199. https://doi.org/10.1186/s12974‐018‐1235‐0.
Dong, M., Liang, Y., Ramalingam, R., Tang, S. W., Shen, W., Ye, R., Gopalakrishnan, S., Au, D. W. T., & Lam, Y. W. (2017). Proteomic characterization of the interactions between fish serum proteins and waterborne bacteria reveals the suppression of anti‐oxidative defense as a serum‐mediated antimicrobial mechanism. Fish & Shellfish Immunology, 62, 96–106. https://doi.org/10.1016/j.fsi.2017.01.013.
Dornburg, A., Ota, T., Criscitiello, M. F., Salinas, I., Sunyer, J. O., Magadán, S., Boudinot, P., Xu, Z., Flajnik, M. F., Singer, A., Gambón‐Deza, F., Hansen, J. D., & Yoder, J. A. (2021). From IgZ to IgT: A call for a common nomenclature for immunoglobulin heavy chain genes of ray‐finned fish. Zebrafish, 18(6), 343–345. https://doi.org/10.1089/zeb.2021.0071.
Freire, C., Fish, R. J., Vilar, R., Di Sanza, C., Grzegorski, S. J., Richter, C. E., Shavit, J. A., & Neerman‐Arbez, M. (2020). A genetic modifier of venous thrombosis in zebrafish reveals a functional role for fibrinogen AαE in early hemostasis. Blood Advances, 4(21), 5480–5491. https://doi.org/10.1182/bloodadvances.2020001472.
Gajahin Gamage, N. T., Miyashita, R., Takahashi, K., Asakawa, S., & Senevirathna, J. D. M. (2022). Proteomic applications in aquatic environment studies. Proteomes, 10(3), 32. https://doi.org/10.3390/proteomes10030032.
Gericke, B., Schecker, N., Amiri, M., & Naim, H. Y. (2017). Structure‐function analysis of human sucrase‐isomaltase identifies key residues required for catalytic activity. The Journal of Biological Chemistry, 292(26), 11070–11078. https://doi.org/10.1074/jbc.M117.791939.
González‐Soto, N., Hatfield, J., Katsumiti, A., Duroudier, N., Lacave, J. M., Bilbao, E., Orbea, A., Navarro, E., & Cajaraville, M. P. (2019). Impacts of dietary exposure to different sized polystyrene microplastics alone and with sorbed benzo[a]pyrene on biomarkers and whole organism responses in mussels Mytilus galloprovincialis. Science of the Total Environment, 684, 548–566. https://doi.org/10.1016/j.scitotenv.2019.05.161.
Grove, S., Tryland, M., Press, C. M., & Reitan, L. J. (2006). Serum immunoglobulin M in Atlantic halibut (Hippoglossus hippoglossus): Characterisation of the molecule and its immunoreactivity. Fish & Shellfish Immunology, 20(1), 97–112. https://doi.org/10.1016/j.fsi.2005.05.002.
Guo, H., Chen, T., Liang, Z., Fan, L., Shen, Y., & Zhou, D. (2021). iTRAQ and PRM‐based comparative proteomic profiling in gills of white shrimp Litopenaeus vannamei under copper stress. Chemosphere, 263, 128270. https://doi.org/10.1016/j.chemosphere.2020.128270.
Gutzeit, C., Magri, G., & Cerutti, A. (2014). Intestinal IgA production and its role in host‐microbe interaction. Immunological Reviews, 260(1), 76–85. https://doi.org/10.1111/imr.12189.
Harikrishnan, R., Balasundaram, C., & Heo, M.‐S. (2010). Molecular studies, disease status and prophylactic measures in grouper aquaculture: Economic importance, diseases and immunology. Aquaculture, 309(1–4), 1–14. https://doi.org/10.1016/j.aquaculture.2010.09.011.
He, Z., Mei, L., Connell, M., & Maxwell, C. A. (2020). Hyaluronan mediated motility receptor (HMMR) encodes an evolutionarily conserved homeostasis, mitosis, and meiosis regulator rather than a hyaluronan receptor. Cells, 9(4), 819. https://doi.org/10.3390/cells9040819.
Hook, S. E., Gallagher, E. P., & Batley, G. E. (2014). The role of biomarkers in the assessment of aquatic ecosystem health. Integrated Environmental Assessment and Management, 10(3), 327–341. https://doi.org/10.1002/ieam.1530.
Huang, Y., Han, X., Peng, H., Li, A., & Li, R. (2021). Expression profile of the fish immune enzyme l‐amino acid oxidase (LAAO) after Streptococcus agalactiae infection in zebrafish (Danio rerio). Developmental & Comparative Immunology, 119, 104040. https://doi.org/10.1016/j.dci.2021.104040.
Hwang, S. D., Bae, J.‐S., Jo, D. H., Kim, K. I., Cho, M. Y., Jee, B. Y., Park, M.‐A., & Park, C.‐I. (2015). Gene expression and functional characterization of serum amyloid P component 2 in rock bream, Oplegnathus fasciatus. Fish & Shellfish Immunology, 47(1), 521–527. https://doi.org/10.1016/j.fsi.2015.09.048.
Ibrahim, N. L., Webb, C., Nazarudin, M. F., Min, C. C., Din, M. S. M., Robinson, C., & Abdullah, M. (2022). α‐2‐macroglobulin, an infection‐resistant biomarker in Epinephelus fuscoguttatus (Forsskål, 1775). Aquaculture Research, 53(16), 5618–5627. https://doi.org/10.1111/are.16043.
Jaiswal, S., Rasal, K. D., Chandra, T., Prabha, R., Iquebal, M. A., Rai, A., & Kumar, D. (2023). Proteomics in fish health and aquaculture productivity management: Status and future perspectives. Aquaculture, 566, 739159. https://doi.org/10.1016/j.aquaculture.2022.739159.
Jones, K., Savulescu, A. F., Brombacher, F., & Hadebe, S. (2020). Immunoglobulin M in health and diseases: How far have we come and what next? Frontiers in Immunology, 11, 595535. https://doi.org/10.3389/fimmu.2020.595535.
Kasai, K., Nakano, M., Ohishi, M., Nakamura, T., & Miura, T. (2021). Antimicrobial properties of L‐amino acid oxidase: Biochemical features and biomedical applications. Applied Microbiology and Biotechnology, 105(12), 4819–4832. https://doi.org/10.1007/s00253‐021‐11381‐0.
Kruse, A., Fattah‐Hosseini, S., Saha, S., Johnson, R., Warwick, E., Sturgeon, K., Mueller, L., MacCoss, M. J., Shatters, R. G., & Cilia Heck, M. (2017). Combining omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut. PLoS One, 12(6), e0179531. https://doi.org/10.1371/journal.pone.0179531.
Lee, P. T., Bird, S., Zou, J., & Martin, S. A. M. (2017). Phylogeny and expression analysis of C‐reactive protein (CRP) and serum amyloid‐P (SAP) like genes reveal two distinct groups in fish. Fish & Shellfish Immunology, 65, 42–51. https://doi.org/10.1016/j.fsi.2017.03.037.
Leu, J.‐H., Tsai, C.‐H., Yang, C.‐H., Chou, H.‐Y., & Wang, H.‐C. (2021). Identification and characterization of l‐amino acid oxidase 2 gene in orange‐spotted grouper (Epinephelus coioides). Developmental & Comparative Immunology, 120, 104058. https://doi.org/10.1016/j.dci.2021.104058.
Li, F. L., & Lu, C. P. (2006). Purification and characterization of α2‐macroglobulin from grass carp Ctenopharyngodon idellus: Cloning a segment of the corresponding gene. Fish & Shellfish Immunology, 20(4), 474–481. https://doi.org/10.1016/j.fsi.2005.06.006.
Li, J., Bai, H., Yin, X., Wu, Z., Qiu, L., Wei, X., Zeng, Q., Mu, L., & Ye, J. (2022). Functional characterization of serum amyloid P component (SAP) in host defense against bacterial infection in a primary vertebrate. International Journal of Molecular Sciences, 23(16), 9468. https://doi.org/10.3390/ijms23169468.
Li, J., Cao, F., Yin, H., Huang, Z., Lin, Z., Mao, N., Sun, B., & Wang, G. (2020). Ferroptosis: Past, present and future. Cell Death & Disease, 11(2), 88. https://doi.org/10.1038/s41419‐020‐2298‐2.
Li, X., Liu, Y., Cheng, J., Xia, Y., Fan, K., Liu, Y., & Liu, P. (2022). Identification and expression analysis of a fibrinogen alpha chain‐like gene in Atlantic salmon (Salmo salar). Aquaculture Reports, 22, 100919. https://doi.org/10.1016/j.aqrep.2021.100919.
Lin, M. H., Wu, P. S., Wong, T. H., Lin, I. Y., Lin, J., Cox, J., & Yu, S. H. (2022). Benchmarking differential expression, imputation and quantification methods for proteomics data. Briefings in Bioinformatics, 23(3), bbac138. https://doi.org/10.1093/bib/bbac138.
Lopez‐Zavala, A. A., Carrasco‐Miranda, J. S., Ramirez‐Aguirre, C. D., López‐Hidalgo, M., Benitez‐Cardoza, C. G., Ochoa‐Leyva, A., Cardona‐Felix, C. S., Diaz‐Quezada, C., Rudiño‐Piñera, E., Sotelo‐Mundo, R. R., & Brieba, L. G. (2016). Structural insights from a novel invertebrate triosephosphate isomerase from Litopenaeus vannamei. Biochimica et Biophysica Acta, 1864(12), 1696–1706. https://doi.org/10.1016/j.bbapap.2016.09.002.
Low, C.‐F., Nor Shamsudin, M., Abdullah, M., Chee, H.‐Y., & Aliyu‐Paiko, M. (2015). Experimental infection of brown‐marbled grouper, Epinephelus fuscoguttatus (Forskal), with Vibrio parahaemolyticus identifies parvalbumin beta‐2 subunit I, alpha‐2‐macroglobulin, nattectin and immunoglobulin light chain, differentially expressed in resist. Journal of Fish Diseases, 38(1), 17–25. https://doi.org/10.1111/jfd.12195.
Lukasheva, E. V., Efremova, A. A., Treshalina, E. M., Arinbasarova, A. J., Medentzev, A. G., & Berezov, T. T. (2012). L‐amino acid oxidases: Properties and molecular mechanisms of action. Biomeditsinskaya Khimiya, 58(4), 372–384. https://doi.org/10.18097/pbmc20125804372.
Messina, M., Bulfon, C., Beraldo, P., Tibaldi, E., & Cardinaletti, G. (2019). Intestinal morpho‐physiology and innate immune status of European sea bass (Dicentrarchus labrax) in response to diets including a blend of two marine microalgae, Tisochrysis lutea and Tetraselmis suecica. Aquaculture, 500, 660–669. https://doi.org/10.1016/j.aquaculture.2018.09.054.
Mi, H., Ebert, D., Muruganujan, A., Mills, C., Albou, L.‐P., Mushayamaha, T., & Thomas, P. D. (2021). PANTHER version 16: A revised family classification, tree‐based classification tool, enhancer regions and extensive API. Nucleic Acids Research, 49(D1), D394–D403. https://doi.org/10.1093/nar/gkaa1106.
Mijailovic, N., Richet, N., Villaume, S., Nesler, A., Perazzolli, M., Aït Barka, E., & Aziz, A. (2022). D‐tagatose‐based product triggers sweet immunity and resistance of grapevine to downy mildew, but not to gray mold disease. Plants, 11(3), 296. https://doi.org/10.3390/plants11030296.
Mohamad, N., Amal, M. N. A., Yasin, I. S. M., Zamri Saad, M., Nasruddin, N. S., Al‐saari, N., Mino, S., & Sawabe, T. (2019). Vibriosis in cultured marine fishes: A review. Aquaculture, 512, 734289. https://doi.org/10.1016/j.aquaculture.2019.734289.
Mohamed Alipiah, N., Ramli, N., Low, C., Shamsudin, M., & Yusoff, F. (2016). Protective effects of sea cucumber surface‐associated bacteria against Vibrio harveyi in brown‐marbled grouper fingerlings. Aquaculture Environment Interactions, 8, 147–155. https://doi.org/10.3354/aei00169.
Moreira, M., Schrama, D., Farinha, A. P., Cerqueira, M., Raposo de Magalhães, C., Carrilho, R., & Rodrigues, P. (2021). Fish pathology research and diagnosis in aquaculture of farmed Fish; a proteomics perspective. Animals, 11(1), 125. https://doi.org/10.3390/ani11010125.
Mutsuro, J., Nakao, M., Fujiki, K., & Yano, T. (2000). Multiple forms of α2‐macroglobulin from a bony fish, the common carp (Cyprinus carpio): Striking sequence diversity in functional sites. Immunogenetics, 51(10), 847–855. https://doi.org/10.1007/s002510000216.
Natnan, M. E., Low, C.‐F., Chong, C.‐M., Bunawan, H., & Baharum, S. N. (2021). Integration of omics tools for understanding the fish immune response due to microbial challenge. Frontiers in Marine Science, 8, 668771. https://doi.org/10.3389/fmars.2021.668771.
Nickerson, J. M., Frey, R. A., Ciavatta, V. T., & Stenkamp, D. L. (2006). Interphotoreceptor retinoid‐binding protein gene structure in tetrapods and teleost fish. Molecular Vision, 12, 1565–1585.
Ninawe, A. S., Hameed, A. S. S., & Selvin, J. (2017). Advancements in diagnosis and control measures of viral pathogens in aquaculture: An Indian perspective. Aquaculture International, 25(1), 251–264. https://doi.org/10.1007/s10499‐016‐0026‐9.
Ning, J., Liu, Y., Gao, F., Song, C., & Cui, Z. (2019). Two alpha‐2 macroglobulin from Portunus trituberculatus involved in the prophenoloxidase system, phagocytosis and regulation of antimicrobial peptides. Fish & Shellfish Immunology, 89, 574–585. https://doi.org/10.1016/j.fsi.2019.04.033.
Nurhikmah, N., Christianus, A., Wan Solahudin, W. M. S., Lau, B. Y. C., Ismail, I. S., & Fei, L. C. (2022). Skin mucus proteome analysis reveals disease‐resistant biomarker signatures in hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂) against Vibrio alginolyticus. Fishes, 7(5), 278. https://doi.org/10.3390/fishes7050278.
Parra, D., Reyes‐Lopez, F. E., & Tort, L. (2015). Mucosal immunity and B cells in teleosts: Effect of vaccination and stress. Frontiers in Immunology, 6, 354. https://doi.org/10.3389/fimmu.2015.00354.
Pauwels, A.‐M., Trost, M., Beyaert, R., & Hoffmann, E. (2017). Patterns, receptors, and signals: Regulation of phagosome maturation. Trends in Immunology, 38(6), 407–422. https://doi.org/10.1016/j.it.2017.03.006.
Rauta, P. R., Nayak, B., & Das, S. (2012). Immune system and immune responses in fish and their role in comparative immunity study: A model for higher organisms. Immunology Letters, 148(1), 23–33. https://doi.org/10.1016/j.imlet.2012.08.003.
Rohlenová, K., Morand, S., Hyršl, P., Tolarová, S., Flajšhans, M., & Šimková, A. (2011). Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio). Parasites & Vectors, 4(1), 120. https://doi.org/10.1186/1756‐3305‐4‐120.
Salinas, I., Fernández‐Montero, Á., Ding, Y., & Sunyer, J. O. (2021). Mucosal immunoglobulins of teleost fish: A decade of advances. Developmental & Comparative Immunology, 121, 104079. https://doi.org/10.1016/j.dci.2021.104079.
Sheikh, H., John, A., Musa, N., Abdulrazzak, L. A., Alfatama, M., & Fadhlina, A. (2022). Vibrio spp. and their vibriocin as a vibriosis control measure in aquaculture. Applied Biochemistry and Biotechnology, 194(10), 4477–4491. https://doi.org/10.1007/s12010‐022‐03919‐3.
Shi, Y.‐H., Chen, K., Ma, W.‐J., & Chen, J. (2018). Ayu C‐reactive protein/serum amyloid P agglutinates bacteria and inhibits complement‐mediated opsonophagocytosis by monocytes/macrophages. Fish & Shellfish Immunology, 76, 58–67. https://doi.org/10.1016/j.fsi.2018.02.038.
Simonian, M., Nair, S. V., Nell, J. A., & Raftos, D. A. (2009). Proteomic clues to the identification of QX disease‐resistance biomarkers in selectively bred Sydney rock oysters, Saccostrea glomerata. Journal of Proteomics, 73(2), 209–217. https://doi.org/10.1016/j.jprot.2009.06.012.
Sumbria, D., Berber, E., Mathayan, M., & Rouse, B. T. (2021). Virus infections and host metabolism—Can we manage the interactions? Frontiers in Immunology, 11, 594963. https://doi.org/10.3389/fimmu.2020.594963.
Sun, B., van Dissel, D., Mo, I., Boysen, P., Haslene‐Hox, H., & Lund, H. (2022). Identification of novel biomarkers of inflammation in Atlantic salmon (Salmo salar L.) by a plasma proteomic approach. Developmental & Comparative Immunology, 127, 104268. https://doi.org/10.1016/j.dci.2021.104268.
Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta‐Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., Jensen, L. J., & von Mering, C. (2019). STRING v11: Protein‐protein association networks with increased coverage, supporting functional discovery in genome‐wide experimental datasets. Nucleic Acids Research, 47(D1), D607–D613. https://doi.org/10.1093/nar/gky1131.
Tang, D., Chen, X., Kang, R., & Kroemer, G. (2021). Ferroptosis: Molecular mechanisms and health implications. Cell Research, 31(2), 107–125. https://doi.org/10.1038/s41422‐020‐00441‐1.
Tavares‐Dias, M., & Oliveira, S. R. (2009). REVIEW: A review of the blood coagulation system of fish. Retrieved from http://www.ufrgs.br/seerbio/ojslindex.php/rbb/article/viewll144.
Tran, T. K. A., Yu, R. M. K., Islam, R., Nguyen, T. H. T., Bui, T. L. H., Kong, R. Y. C., O'Connor, W. A., Leusch, F. D. L., Andrew‐Priestley, M., & MacFarlane, G. R. (2019). The utility of vitellogenin as a biomarker of estrogenic endocrine disrupting chemicals in molluscs. Environmental Pollution, 248, 1067–1078. https://doi.org/10.1016/j.envpol.2019.02.056.
Umasuthan, N., Whang, I., Saranya Revathy, K., Oh, M.‐J., Jung, S.‐J., Choi, C. Y., Lee, J.‐H., Noh, J. K., & Lee, J. (2012). A teleostean angiotensinogen from Oplegnathus fasciatus responses to immune and injury challenges. Fish & Shellfish Immunology, 32(5), 922–928. https://doi.org/10.1016/j.fsi.2012.01.019.
Vandooren, J., & Itoh, Y. (2021). Alpha‐2‐macroglobulin in inflammation, immunity and infections. Frontiers in Immunology, 12, 803244. https://doi.org/10.3389/fimmu.2021.803244.
Wang, D., Gou, M., Hou, J., Pang, Y., & Li, Q. (2019). The role of serpin protein on the natural immune defense against pathogen infection in Lampetra japonica. Fish & Shellfish Immunology, 92, 196–208. https://doi.org/10.1016/j.fsi.2019.05.062.
Wang, T., & Sun, L. (2016). CsSAP, a teleost serum amyloid P component, interacts with bacteria, promotes phagocytosis, and enhances host resistance against bacterial and viral infection. Developmental & Comparative Immunology, 55, 12–20. https://doi.org/10.1016/j.dci.2015.10.002.
Wei, Y., Ding, J., Li, J., Cai, S., Liu, S., Hong, L., Yin, T., Zhang, Y., & Diao, L. (2021). Metabolic reprogramming of immune cells at the maternal‐fetal Interface and the development of techniques for immunometabolism. Frontiers in Immunology, 12, 717014. https://doi.org/10.3389/fimmu.2021.717014.
Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C.‐Y., & Wei, L. (2011). KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research, 39(Web Server issue), W316–W322. https://doi.org/10.1093/nar/gkr483.
Xu, Z., Parra, D., Gómez, D., Salinas, I., Zhang, Y.‐A., von Gersdorff Jørgensen, L., Heinecke, R. D., Buchmann, K., LaPatra, S., & Sunyer, J. O. (2013). Teleost skin, an ancient mucosal surface that elicits gut‐like immune responses. Proceedings of the National Academy of Sciences of the United States of America, 110(32), 13097–13102. https://doi.org/10.1073/pnas.1304319110.
Yang, W., Lv, X., Leng, J., Li, Y., Sun, J., Yang, C., Wang, L., & Song, L. (2021). A fibrinogen‐related protein mediates the recognition of various bacteria and haemocyte phagocytosis in oyster Crassostrea gigas. Fish & Shellfish Immunology, 114, 161–170. https://doi.org/10.1016/j.fsi.2021.04.022.
Yanuhar, U., Nurcahyo, H., Widiyanti, L., Junirahma, N. S., Caesar, N. R., & Sukoso, S. (2022). In vivo test of Vibrio alginolyticus and Vibrio harveyi infection in the humpback grouper (Cromileptes altivelis) from East Java Indonesia. Veterinary World, 15(5), 1269–1282. https://doi.org/10.14202/vetworld.2022.1269‐1282.
Yu, Y., Wang, Q., Huang, Z., Ding, L., & Xu, Z. (2020). Immunoglobulins, mucosal immunity and vaccination in teleost fish. Frontiers in Immunology, 11, 567941. https://doi.org/10.3389/fimmu.2020.567941.
Zhang, D., Liu, C., Nakatsukasa, H., & Chen, W. (2022). Editorial: Hexose uptake and metabolism in immune homeostasis and inflammation. Frontiers in Immunology, 12, 832293. https://doi.org/10.3389/fimmu.2021.832293.
Zhang, W., Dan, Z., Zhuang, Y., Zheng, J., Gong, Y., Liu, Y., Mai, K., & Ai, Q. (2022). Effects of dietary lipid levels on growth, digestive enzyme activities, antioxidant capacity, and lipid metabolism in turbot (Scophthalmus maximus L.) at three different stages. Aquaculture Nutrition, 2022, 1–18. https://doi.org/10.1155/2022/1042263.
Zhu, J., Yu, K., Ao, Q., Tan, Y., Fu, Q., & Jiang, H. (2021). Comparative splenic proteomic analysis of susceptible and resistant GIFT tilapia following challenge with Streptococcus agalactiae. Aquaculture International, 29(3), 1141–1159. https://doi.org/10.1007/s10499‐021‐00683‐9.

TRGS/1/2020/UPM/02/1/3 Ministry of Higher Education, Malaysia

Keywords: Vibrio alginolyticus; disease‐resistant phenotype; hybrid grouper; serum proteome; vibriosis

0 (Proteome)
0 (Biomarkers)
0 (Fish Proteins)

Date Created: 20240325 Date Completed: 20240607 Latest Revision: 20240607

20240608

10.1111/jfd.13940

38523352