Immunochemical response and gene expression in juvenile shrimp (Litopenaeus vannamei) exposed to microorganisms isolated from marine sediment
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Abstract
The use of microorganisms isolated from the natural environment can improve the culture conditions in aquaculture systems and the immune and antioxidant response capacity of cultured organisms. In this study, the immunochemical response and gene expression of Litopenaeus vannamei juveniles were analyzed following exposure to microorganisms isolated from marine sediments after in vitro characterization of their probiotic properties. Two yeasts and one bacterium strain were used by immersion method (48 to 216 h) at a concentration of 1 × 106 CFU(mL)-1 with the following treatments: (1) Control, without probiotics; (2) Positive Control, commercial immunostimulant (Laminarin; β-1,3, glucan); (3) Candida maris, strain A1; (4) Geotrichum candidum, strain A3; and (5) Curtobacterium sp., strain S13. Shrimp treated with microorganisms and commercial immunostimulants showed a significant increase (P < 0.0500) in the soluble protein content in hemocytes compared with the control group. At 72 h post-exposures, G. candidum, Curtobacterium sp., and laminarin treatments showed a significant increase (P < 0.0500) in superoxide dismutase (SOD) activity compared with the control group. Superoxide dismutase enzyme gene expression showed a significant increase (P < 0.0500) in all shrimp treated with microorganisms from 48 post-exposures. The results obtained showed that the use of three microorganisms isolated from a marine environment can stimulate the protein content in circulating hemocytes, antioxidant activity, and gene expression in juvenile L. vannamei.
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References
FAO. The state of world fisheries and aquaculture 2022. Towards blue transformation. Rome; 2022. doi: 10.4060/cc0461en.
CONAPESCA. Anuario estadístico de pesca. CDMX, México: SAGARPA; 2021. https://nube.conapesca.gob.mx/sites/cona/dgppe/2021/ANUARIO_ESTADISTICO_D E_ACUACULTURA_Y_PESCA_2021.pdf
Arreguín-Sánchez F, Arcos-Huitrón E. Fishing in Mexico: state of exploitation and use of ecosystems. Hidrobiológica. 2011;21(3):431-462.
Pérez-Castañeda R, Sánchez-Martinez JG, Aguirre-Guzman G, Rabago-Castro JL, Vazquez-Sauceda (ML). Interaction of fisheries and aquaculture in the production of marine resources: advances and perspectives in Mexico. In: CW Finkl, C Makowski. editors. Switzerland: Environmental Management and Governance–Advances in Coastal and Marine Resources, Coastal Research Library 8, Springer International Publishing. 2014;111-140. doi: 10.1007/978-3-319-06305-8_5.
Morales-Cristóbal Y, Cortés-Jacinto E, Saucedo PE, Cadena-Roa M, Campa-Córdova AI. Dietary enrichment with crude protein content and feed additives (Bacillus spp. and yeast strains) improves growth performance, survival and circulating hemocytes in juvenile white shrimp, Litopenaeus vannamei. Revista de Biologia Marina y Oceanografia. 2022;57(1):45–56. doi: 10.22370/rbmo.2022.57.1.3361.
Burge E, Madigan DJ, Burnett LE, Burnett KG. Lysozyme gene expression by hemocytes of Pacific white shrimp, Litopenaeus vannamei, after injection with Vibrio. Fish & Shellfish Immunology. 2007;22(4):327-39. doi: 10.1016/j.fsi.2006.06.004.
Robalino J, Almeida JS, McKillen D, Colglazier J, Trent HF, Chen YA, Peck MET, Browdy CL, Chapman RW, Warr GW, Gross PS. Insights into the immune transcriptome of the shrimp Litopenaeus vannamei: tissue-specific expression profiles and transcriptomic responses to immune challenge. Physiology Genomics. 2007;29:44–56. doi: 10.1152/physiolgenomics.00165.2006.
Luna-González A, Moreno-Herrera JT, Campa-Córdova AI, González-Ocampo HA, Fierro-Coronado JA, Álvarez-Ruíz P, Bueno-Ibarra MA. Respuesta inmune y expresión de genes en el camarón blanco (Litopenaeus vannamei) inducida por inmunoestimulantes microbianos. Latin American Journal of Aquatic Research. 2013;41(5):898-907. doi: 103856/vol41-issue5-fulltext-10.
Ceseña CE, Vega-Villasante F, Aguirre-Guzman G, Luna-González A, Campa-Córdova AI. Update on the use of yeast in shrimp aquaculture: a minireview. International Aquatic research. 2021b;13:1-16. doi: 10.22034/IAR.2021.1904524.1066.
Méndez-Martínez Y, Torres-Navarrete YG, Cortés-Jacinto E, García-Guerrero MU, Hernández-Hernández LH, Verdecía DM. Biological, nutritional, and hematoimmune response in juvenile Cherax quadricarinatus (Decapoda:Parastacidae) fed with probiotic mixture. Revista MVZ Córdoba. 2022;27(3). doi: 10.21897/rmvz.2578.
Kumar S, Verma AK, Singh SP, Awasthi A. Immunostimulants for shrimp aquaculture: paving pathway towards shrimp sustainability. Environmental Science and Pollution Research. 2022(Jan);13. doi: 10.1007/s11356-021-18433-y.
Türker M. Yeast biotechnology: diversity and applications. Advances in science and industrial productions of baker’s yeast. 27th VH Yeast Conference, April 14th–15th. Istanbul, Turkey: 2014; 1-26.
Campa-Córdova AI, Hernández-Saavedra NY, Aguirre-Guzmán G, Ascencio F. Immunomodulatory response of superoxide dismutase in juvenile American white shrimp (Litopenaeus vannamei) exposed to immunostimulants. Ciencias Marinas. 2005;31(4):661-669. doi: 10.7773/cm.v31i4.32.
Samuel P, Prince L, Prabakaran P. Antibacterial activity of marine derived fungi collected from South East Coast of Tamilnadu, India. Journal of Microbiology and Biotechnology Research. 2011;1(4):86-94.
Fell JW. Yeast in marine environments. In: EB Gareth, KL Pang, editors. Marine fungi and fungal-like organisms. De Gruyter: University of Malaya; 2012. pp: 92-103.
Campa-Córdova AI, Valenzuela-Chávez JA, García-Armenta J, Medina D, Licona-Jain AB, Angulo-Valadez CE, Aguirre-Guzmán G, Mejía-Ruíz CH. Uso profiláctico de aditivos inmunoestimulantes en el cultivo del camarón blanco, Litopenaeus vannamei. In: LE Cruz Suárez, D Ricque D, M Tapia M, MG Nieto, DA Villarreal, J Gamboa, L Mercedes L, MA Galaviz editors. Nuevo León, México: Universidad Autónoma de San Nicolás de los Garza, Nuevo León, México: 2017. pp. 541-559.
Ochoa N. Evaluación de factores de virulencia de hongos infecciosos en camarón blanco (Litopenaeus vannamei) [tesis de maestría]. La Paz, Baja California Sur, México: Instituto Politécnico Nacional, Centro Interdisciplinario en Ciencias Marinas; 2004.
Ochoa JL, Ochoa-Alvarez N, Guzmán-Murillo MA, Hernandez S, Ascencio F. Isolation and risk assessment of Geotrichum spp. in the white shrimp (Litopenaeus vannamei Boone, 1931) from culture ponds. Latin American Journal of Aquatic Research. 2015;43(4):755-765. doi: 10.3856/vol43-issue4-fulltext-14.
Ibrar M, Zuberi A, Amir I, Imran M, Noor Z. Effect of probiotic Geotrichum candidum on early rearing of Labeo rohita (Hamilton, 1822). Turkish Journal of Fisheries and Aquatic Sciences. 2017;17:1263-1270. doi: 10.4194/1303-2712-v17_6_19.
Amir I, Zuberi A, Kamran M, Imran M, Ul M, Murtaz H. Evaluation of commercial application of dietary encapsulated probiotic (Geotrichum candidum QAUGC01): effect on growth and immunological indices of rohu (Labeo rohita, Hamilton 1822) in semi-intensive culture system. Fish & Shellfish Immunology. 2019;95:464-472. doi: 10.1016/j.fsi.2019.11.011.
Ibarra-Serrano, AC. Evaluación de microorganismos aislados de sistema de mangle con capacidades biorremediadoras e inmunoestimulantes en el cultivo de camarón blanco del Pacífico Litopenaeus vannamei (Boone, 1931) [tesis de maestría]. La Paz, Baja California Sur, México: Centro de Investigaciones Biológicas del Noroeste; 2018. pp. 62.
Cowan ST, Steel LJ. Manual for the identification of medical bacteria. Cambridge, UK: University of Cambridge; 1993.
Abasolo-Pacheco F, Campa- Córdova AI, Mazón-Suástegui JM, Tovar-Ramírez D, Araya R, Saucedo PE. Enhancing growth and resistance to Vibrio alginolyticus disease in catarina scallop (Argopecten ventricosus) with Bacillus and Lactobacillus probiotic strains during early development. Aquaculture Research. 2017;48:4597-4607. doi: 10.1111/are.13283.
Campa-Córdova AI, Hernández-Saavedra NY, de Philippis R, Ascencio F. Generation of superoxide anion and SOD activity in haemocytes and muscle of American white shrimp (Litopenaeus vannamei) as a response to β-glucan and sulphated polysaccharide. Fish and Shellfish Immunology. 2002;12:353-366. doi: 10.1006/fsim.2001.0377.
Pacheco M, Campa A, Aguirre G, Luna A, Guzmán M, Ascencio F. Effect of Debaryomyces hansenii on the antioxidant response of juvenile white shrimp Litopenaeus vannamei. Revista MVZ. Córdoba. 2012;17(1):2820-2826.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976;72:248-54.
Wang Z, Zhu F. MicroARN-100 is involved in shrimp immune response to white spot syndrome virus (WSSV) and Vibrio alginolyticus infection. Scientific Reports. 2017;7:42334. doi: 10.1038/srep42334.
Suzuki K. Measurements of Mn-SOD and Cu, Zn-SOD. In: N Taniguchi and J Gutteridge, editors. Experimental protocols for reactive oxygen and nitrogen species. Oxford, UK: Oxford University Press. 2000;91-95.
Gutiérrez-Dagnino A, Luna-González A, Fierro-Coronado JA, Álvarez-Ruíz P, Flores-Miranda MC, Miranda-Saucedo S, Medina-Beltrán V, Escamilla-Montes R. Efecto de la inulina y del ácido fúlvico en la supervivencia, crecimiento, sistema inmune y prevalencia de WSSV en Litopenaeus vannamei. Latin American Journal of Aquatic Research. 2015;43(5):912-921. doi: 10.3856/vol43-issue5-fulltext-11.
Fernandes TJR, Costa J, Oliveira MBPP, Mafra I. COI barcode-HRM as a novel approach for the discrimination of hake species. Fisheries Research. 2018;197:50-59. doi: 10.1016/j.fishres.2017.09.014.
Ceseña CE, Cortés-Jacinto E, Luna-González A, Vega-Villasante F, Ochoa-Álvarez NA, Morelos-Castro RI, Escamilla-Montes R, Tovar-Ramírez D, Sánchez-Ortiz AC, Campa-Córdova AI. Dietary supplementation of Debaryomyces hansenii enhanced survival, antioxidant and immune response in juvenile shrimp Penaeus vannamei challenged with Vibrio parahaemolyticus. Tropical and Subtropical Agroecosystems. 2021;24(2):1-13. doi: 10.56369/tsaes.3616.
Ventura-Lopez C, Gomez-Anduro G, Arcos FG, Llera-Herrera R, Racotta IS, Ibarra AM. A novel CHH gene from the Pacific white shrimp Litopenaeus vannamei was characterized and found highly expressed in gut and less in eyestalk and other extra- eyestalk tissue. Gene. 2016;582(2):148-60. doi: 10.1016/j.gene.2016.02.011.
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology. 2007;8(2):R19.
Zhang Z, Aweya JJ, Yao D, Zheng Z, Tran NT, Li S, Zhang T. Ubiquitination as an important host-immune response strategy in penaeid shrimp: inferences from other species. Frontiers in Immunology. 2021;12:697397. doi: 10.3389/fimmu.2021.697397.
Licona-Jain A, Racotta I, Angulo C, Luna-González A, Escamilla-Montes R, Cortés-Jacinto E, Morelos-Castro RM, Campa-Córdova AI. Combined administration routes of marine yeasts enhanced immune-related genes and protection of white shrimp (Penaeus vannamei) against Vibrio parahaemolyticus. Fish & Shellfish Immunology. 2022;124:192-200. doi: 10.1016/j.fsi.2022.04.004.
Neves CA, Santos EA, Bainy ACD. Reduced superoxide dismutase activity in Palaemonetes argentinus (Decapoda, Paleminedae), infected by Probopyrus ringueleti (Isopoda, Bopyridae). Diseases of Aquatic Organisms. 2000;39:155-158.
Aguirre-Guzmán G, Sánchez-Martínez JG, Campa-Córdova AI, Luna-González A, Ascencio F. Penaeid shrimp immune system: a minireview. Thai Journal of Veterinary Medicine. 2009;39(3):205-215.
Ji PF, Yao CL, Wang ZY. Immune response and gene expression in shrimp (Litopenaeus vannamei) hemocytes and hepatopancreas against some pathogen-associated molecular patterns. Fish & Shellfish Immunology. 2009;27:563-570. doi: 10.1016/j.fsi.2009.08.001.
Lin YC, Chen JH, Man SNC, Morni WZW, Suhaili ASNA, Cheng SY, Hsu CH. Modulation of innate immunity and gene expressions in white shrimp Litopenaeus vannamei following long-term starvation and re-feeding. Results in Immunology. 2012;2:148-156. doi: 10.1016/j.rinim.2012.07.001.
Apines-Amar MJS, Amar EC. Use of immunostimulants in shrimp culture: an update. In: CMA Caipang, MBI Bacano-Maningas, FF Fagutao, editors. Biotechnological Advances in Shrimp Health Management in the Philippines, Research Signepost. 2015;45-71.
Lin YC, Tayag CM, Huang CL, Tsui WC, Chen JC. White shrimp Litopenaeus vannamei that had received the hot-water extract of Spirulina platensis showed earlier recovery in immunity and up-regulation of gene expressions after pH stress. Fish & Shellfish Immunology. 2010;29:1092-1098.
Jennissen HP. Ubiquitin and the enigma of intracellular protein degradation. European Journal of Biochemistry. 1995;231:1-30.
Dugger D. Bio-modulation of the non-specific immune response in marine shrimp with beta-glucan. Aquaculture Magazine. 1999;1:81-89.
Karunasagar I, Otta SK, Devaraj TN, Shubha G, Iddya K. Immunostimulation of Penaeus monodon through the oral route. In: Workshop: Shrimp Immunity and Disease Control. Thailand; 1999. http://www.ifremer.fr/incode/htm
Hien TTT, Tao CT, Hoa TTT, Huynh TG, Tu TLC, Hai TN, Nguyen DH, Kim SH, Song JW, Nhan HT, Duc PM. Effects of dietary supplementation with Pro-A on growth performance, feed utilization, immune responses, and intestinal microbiota of whiteleg shrimp (Litopenaeus vannamei). Aquaculture Reports. 2022;24:101125. doi: 10.1016/j.aqrep.2022.101125.
Zhang Q, Li F, Wang B, Zhang J, Liu Y, Zhou Q, Xiang J. The mitochondrial manganese superoxide dismutase gene in Chinese shrimp Fenneropenaeus chinensis: Cloning, distribution and expression. Developmental and Comparative Immunology. 2007;31:429-440. doi: 10.1016/j.dci.2006.08.005.
García-Triana A, Zenteno-Savín T, Peregrino-Uriarte AB, Yepiz-Plascencia G. Hypoxia, reoxygenation and cytosolic manganese superoxide dismutase (cMnSOD) silencing in Litopenaeus vannamei: Effects on cMnSOD transcripts, superoxide dismutase activity and superoxide anion production capacity. Developmental and Comparative Immunology. 2010;34:1230–1235. doi: 10.1016/j.dci.2010.06.018.
Le Moullac G, Soyez C, Saulnier D, Ansquer D, Avarre JC, Levy P. Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish & Shellfish Immunology. 1998;8:621-629.
Downs C, Fauth JE, Woodley CM. Assessing the health of grass shrimp (Palaemonetes pugio) exposed to natural and anthropogenic stressors: a molecular biomarker system. Marine Biotechnology. 2001;3:380-397.
Truscott R, White KN. The influence of metal and temperature stress on the immune system of crabs. Functional Ecology. 1990;4:455-461.
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