Abstract
The common use of antimicrobials in food-animal production can lead to drug residues in edible tissues for consumers. However, immunomodulators enhance immune responses and vaccine effectiveness. A new perspective explores bacterial extracellular bioactive molecules (EBMs) in food-animal production to modulate host immune responses, potentially transforming pathogen management and antimicrobial use. This study investigates the immunogenic potential of Aeromonas hydrophila-derived EBMs (Antigens) to enhance the immune system. Four Antigens were administered intraperitoneally to Oreochromis niloticus (Nile Tilapia). Antigens 2 and Antigens 3 boosted fish immune competence within 21 days. Remarkably, Antigens 3 induced robust immunity against A. hydrophila with a single dose, notably enhancing antibody-based immune responses. The increased antibody activity suggests Antigens 3 could be a vaccine candidate, promising further research and potential application in food-animal production to improve disease control. This study highlights immunomodulators' potential in reshaping disease management in the food-animal industry, emphasizing the benefits of focusing on bacterial EBMs to reduce reliance on antimicrobials and achieve sustainable disease prevention.
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The datasets generated during and/or analyzed in this study are available from the corresponding author upon reasonable request.
References
Food and Agriculture Organization of the United Nations (2020) The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations
Rocha CP, Cabral HN, Marques JC, Goncalves AM (2022) A global overview of Aquaculture Food production with a focus on the activity’s development in transitional systems—the case study of a South European country (Portugal). J Mar Sci Eng 10:417. https://doi.org/10.3390/jmse10030417
Zhang H, Liu P, Feng Y, Yang F (2013) Fate of antibiotics during wastewater treatment and antibiotic distribution in the effluent receiving waters of the Yellow Sea, northern China. Mar Pollut Bull 73:282–290. https://doi.org/10.1016/j.marpolbul.2013.05.007
Olga H (2017) Major bacterial diseases affecting aquaculture. Food and Agriculture Organization of the United Nations. Aquatic AMR Workshop, vol 1, pp 10–11
Dar GH, Kamili AN, Chishti MZ, Dar SA, Tantry TA, Ahmad F (2016) Characterization of Aeromonas sobria isolated from fish Rohu (Labeo rohita) collected from polluted pond. J Bacteriol Parasitol. https://doi.org/10.4172/2155-9597.1000273
Yu JH, Koo BH, Kim DH, Kim DW, Park SW (2015) Aeromonas sorbia infection in farmed mud loach (Misgurnus mizolepis) in Korea, a bacteriological survey. Iran J Vet Res 16:194–201
Hossain MJ, Sun D, McGarey DJ, Wrenn S, Alexander LM, Martino ME, Xing Y, Terhune JS, Liles MR (2014) An Asian origin of virulent Aeromonas hydrophila responsible for disease epidemics in United States-farmed catfish. MBio 5:e00848-e814. https://doi.org/10.1128/mBio.00848-14
Stratev D, Daskalov H, Vashin I (2015) Characterization and determination of antimicrobial resistance of β-haemolytic Aeromonas spp isolated from common carp (Cyprinus carpio L.). Revue Méd Vét 166:54–61
Mulyani Y, Aryantha NP, Suhandono S, Pancoro A (2018) Intestinal bacteria common carp (Carpinus carpio L) as a biological control agent for Aeromonas. J Pure Appl Microbiol 12:601–610
Firdaus-Nawi M, Zamri-Saad M (2016) Major components of fish immunity: a review. Pertanika J Trop Agric Sci 39:393–420
United Nations Environment Programme (UNEP) (2023) Bracing for Superbugs: Strengthening environmental action in the One Health response to antimicrobial resistance. United Nations Environment Programme. ISBN: 978-92-807-4006-6. Job number: DTI/2504/GE
Chuah L, Effarizah ME, Goni AM, Rusul G (2016) Antibiotic application and emergence of multiple antibiotic resistance (MAR) in global catfish aquaculture. Curr Environ Health Rep 3:118–127
Årdal C, Baraldi E, Beyer P, Lacotte Y, Larsson DJ, Ploy M-C, Rottingen J-A, Smith I (2021) Supply chain transparency and the availability of essential medicines. Bull World Health Organ 99:319–320. https://doi.org/10.2471/blt.20.267724
Fatsi PSK, Hashem S, Kodama A, Appiah EK, Saito H, Kawai K (2020) Population genetics and taxonomic signatures of wild Tilapia in Japan based on mitochondrial DNA control region analysis. Hydrobiologia 847:1491–1504. https://doi.org/10.1007/s10750-020-04203-3
Fatsi PSK, Hashem S, Appiah EK, Mensah ET-D, Setufe SB, Saito H, Kawai K (2021) Morphological divergence within the largest genetically consistent group of wild Tilapia. Environ Biol Fishes 104:597–613. https://doi.org/10.1007/s10641-021-01098-4
Marcos-Lopez M, Ruiz CE, Rodger HD, O’Connor I, MacCarthy E, Estaban MA (2017) Local and systemic humoral immune response in farmed Atlantic salmon (Salmo salar L) under a natural amoebic gill disease outbreak. Fish Shellfish Immunol 66:207–216. https://doi.org/10.1016/j.fsi.2017.05.029
Dhasarathan P, Pugazhenthi M, Valivittan K (2014) Experimental immunology Analysis of humoral immune response of animals exposed to bacterial antigens. Central Eur J Immunol 3:323–326. https://doi.org/10.5114/ceji.2014.45942
Guardiola FA, Cuesta A, Abellán E, Meseguer J, Esteban MA (2014) Comparative analysis of the humoral immunity of skin mucus from several marine teleost fish. Fish Shellfish Immunol 40:24–31. https://doi.org/10.1016/j.fsi.2014.06.018
Agbowuro AA, Huston WM, Gamble AB, Tyndall JDA (2017) Proteases and protease inhibitors in infectious diseases. Med Res Rev 38:1295–1331
Chebaani N, Guardiola FA, Sihem M, Nabil A, Oumouna M, Meseguer J, Estaban MA, Cuesta A (2014) Innate humoral immune parameters in Tilapia zillii under acute stress by low temperature and crowding. Fish Physiol Biochem 40:797–804. https://doi.org/10.1007/s10695-013-9886-3
Gonzalez-Silvera D, Herrera M, Giráldez I, Esteban M (2018) Effects of the dietary tryptophan and aspartate on the immune response of meagre (Argyrosomus regius) after stress. Fishes 3:6
Acknowledgements
We extend our gratitude to the Japanese Government, through the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) and the Graduate School of Integrated Sciences for Life (under the Sustainable Food Production program; S.F.P.P), Hiroshima University, Japan, for financially supporting this study. We are equally grateful to Hiroshima University’s Oceanography Cruise (Toyoshio-Maru) Team for their valuable support during field sampling.
Funding
This study was funded by the Japanese Government, through the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) and the Graduate School of Integrated Sciences for Life, Hiroshima University, Japan; under the Sustainable Food Production program (S.F.P.). Funding was provided by Japan Student Services Organization.
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All efforts made to minimize the suffering of experimental animals were under animal care 111, and experimental procedures were conducted according to the Ethical practices approved in 112 Animal Experimentation at Hiroshima University (Permit Number: G13-3), even though such recommendations are not strictly enforced for teleost research.
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Fatsi, P.S.K., Kawai, K., Asmah, R. et al. Immunomodulation and Humoral Immune Response in Teleost Immunized with Aeromonas-Derived Antigenic Extracellular Bioactive Molecules. Indian J Microbiol (2024). https://doi.org/10.1007/s12088-024-01254-1
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DOI: https://doi.org/10.1007/s12088-024-01254-1