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Dietary selenium supplementation alleviates low salinity stress in the Pacific white shrimp Litopenaeus vannamei: growth, antioxidative capacity and hepatopancreas transcriptomic responses

Published online by Cambridge University Press:  27 December 2022

Qiuran Yu
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China School of Life Sciences, East China Normal University, Shanghai, People’s Republic of China
Fenglu Han*
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
Artur Rombenso
Affiliation:
CSIRO, Agriculture and Food, Livestock & Aquaculture Program, Bribie Island Research Centre, Bribie Island, QLD, Australia
Jian G. Qin
Affiliation:
School of Biological Sciences, Flinders University, Adelaide, SA, Australia
Liqiao Chen
Affiliation:
School of Life Sciences, East China Normal University, Shanghai, People’s Republic of China
Erchao Li*
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
*
*Corresponding authors: Dr. Fenglu Han, email hanfenglu@163.com; Dr E. Li, email ecli@bio.ecnu.edu.cn
*Corresponding authors: Dr. Fenglu Han, email hanfenglu@163.com; Dr E. Li, email ecli@bio.ecnu.edu.cn

Abstract

Se is an essential trace element associated with animal growth and antioxidant and metabolic processes. However, whether Se, especially organic Se with higher bioavailability, can alleviate the adverse effects of low salinity stress on marine economic crustacean species has not been investigated. Accordingly, juvenile Pacific white shrimp (Litopenaeus vannamei) were reared in two culture conditions (low and standard salinity) fed diets supplemented with increasing levels of l-selenomethionine (0·41, 0·84 and 1·14 mg/kg Se) for 56 d, resulting in four treatments: 0·41 mg/kg under standard seawater (salinity 31) and 0·41, 0·84 and 1·14 mg/kg Se under low salinity (salinity 3). The diet containing 0·84 mg/kg Se significantly improved the survival and weight gain of shrimp under low salinity stress and enhanced the antioxidant capacity of the hepatopancreas. The increased numbers of B and R cells may be a passive change in hepatopancreas histology in the 1·14 mg/kg Se group. Transcriptomic analysis found that l-selenomethionine was involved in the regulatory pathways of energy metabolism, retinol metabolism and steroid hormones. In conclusion, dietary supplementation with 0·84 mg/kg Se (twice the recommended level) effectively alleviated the effects of low salinity stress on L. vannamei by regulating antioxidant capacity, hormone regulation and energy metabolism.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Romano, N & Zeng, C (2012) Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquaculture 334, 1223.CrossRefGoogle Scholar
Leonard, EM, Barcarolli, I, Silva, KR, et al. (2011) The effects of salinity on acute and chronic nickel toxicity and bioaccumulation in two euryhaline crustaceans: Litopenaeus vannamei and Excirolana armata . Comp Biochem Physiol Part C Toxicol Pharmacol 154, 409419.CrossRefGoogle ScholarPubMed
Laramore, S, Laramore, CR & Scarpa, J (2001) Effect of low salinity on growth and survival of postlarvae and juvenile Litopenaeus vannamei . J World Aquac Soc 32, 385392.CrossRefGoogle Scholar
Decamp, O, Cody, J, Conquest, L, et al. (2003) Effect of salinity on natural community and production of Litopenaeus vannamei (Boone), within experimental zero-water exchange culture systems. Aquac Res 34, 345355.CrossRefGoogle Scholar
Saoud, IP, Davis, DA & Rouse, DB (2003) Suitability studies of inland well waters for Litopenaeus vannamei culture. Aquaculture 217, 373383.CrossRefGoogle Scholar
Yan, B, Wang, X & Cao, M (2007) Effects of salinity and temperature on survival, growth, and energy budget of juvenile Litopenaeus vannamei. J Shellfish Res 26, 141146.CrossRefGoogle Scholar
Li, E, Chen, L, Zeng, C, et al. (2007) Growth, body composition, respiration and ambient ammonia nitrogen tolerance of the juvenile white shrimp, Litopenaeus vannamei, at different salinities. Aquaculture 265, 385390.CrossRefGoogle Scholar
Davis, DA, Saoud, IP, McGraw, WJ, et al. (2002) Considerations for Litopenaeus vannamei Reared in Inland Low Salinity Waters. Cancún, QI: Avances en Nutrición Acuícola VI.Google Scholar
Li, E, Chen, L, Zeng, C, et al. (2008) Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture 274, 8086.Google Scholar
Xu, C, Li, E, Liu, Y, et al. (2017) Comparative proteome analysis of the hepatopancreas from the Pacific white shrimp Litopenaeus vannamei under long-term low salinity stress. J Proteomics 162, 110.Google ScholarPubMed
Zhang, M, Sun, Y, Liu, Y, et al. (2016) Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture 454, 7280.CrossRefGoogle Scholar
Rotruck, JT, Pope, AL, Ganther, HE, et al. (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179, 588590.CrossRefGoogle ScholarPubMed
Dröge, W (2002) Aging-related changes in the thiol/disulfide redox state: implications for the use of thiol antioxidants. Exp Gerontol 37, 13331345.CrossRefGoogle ScholarPubMed
Lin, Y-H & Shiau, S-Y (2005) Dietary selenium requirements of juvenile grouper, Epinephelus malabaricus. Aquaculture 250, 356363.Google Scholar
Mansour, AT-E, Goda, AA, Omar, EA, et al. (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, Argyrosomus regius, juveniles. Fish Shellfish Immunol 68, 516524.Google ScholarPubMed
Hamilton, SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326, 131.CrossRefGoogle ScholarPubMed
Wang, W, Wang, A & Zhang, Y (2006) Effect of dietary higher level of selenium and nitrite concentration on the cellular defense response of Penaeus vannamei. Aquaculture 256, 558563.CrossRefGoogle Scholar
Yu, Q, Fu, Z, Huang, M, et al. (2021) Growth, physiological, biochemical, and molecular responses of Pacific white shrimp Litopenaeus vannamei fed different levels of dietary selenium. Aquaculture 535, 736393.CrossRefGoogle Scholar
Han, D, Xie, S, Liu, M, et al. (2011) The effects of dietary selenium on growth performances, oxidative stress and tissue selenium concentration of Gibel carp (Carassius auratus gibelio). Aquac Nutr 17, e741e749.Google Scholar
Liu, K, Wang, XJ, Ai, Q, et al. (2010) Dietary selenium requirement for juvenile cobia, Rachycentron canadum L. Aquac Res 41, e594e601.Google Scholar
Atencio, L, Moreno, I, Jos, Á, et al. (2009) Effects of dietary selenium on the oxidative stress and pathological changes in tilapia (Oreochromis niloticus) exposed to a microcystin-producing cyanobacterial water bloom. Toxicon 53, 269282.Google ScholarPubMed
Yu, Q, Xia, C, Han, F, et al. (2022) Effect of different dietary selenium sources on growth performance, antioxidant capacity, gut microbiota, and molecular responses in pacific white shrimp Litopenaeus vannamei . Aquac Nutr 2022, 5738008.CrossRefGoogle Scholar
Bu, X, Wang, X, Lin, Z, et al. (2022) Myo-inositol improves growth performance and regulates lipid metabolism of juvenile Chinese mitten crab (Eriocheir sinensis) fed different percentage of lipid. Br J Nutr 127, 666678.CrossRefGoogle ScholarPubMed
Horwitz, W (2010) Official Methods of Analysis of AOAC International. Volume I, agricultural Chemicals, Contaminants, Drugs. Gaithersburg, MD: AOAC International.Google Scholar
Cline, MS, Smoot, M, Cerami, E, et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2, 23662382.Google ScholarPubMed
Szklarczyk, D, Franceschini, A, Wyder, S, et al. (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43, D447D452.CrossRefGoogle ScholarPubMed
Zhang, P, Zhang, X, Li, J, et al. (2009) Effect of salinity on survival, growth, oxygen consumption and ammonia-N excretion of juvenile whiteleg shrimp, Litopenaeus vannamei . Aquac Res 40, 14191427.CrossRefGoogle Scholar
Rider, SA, Davies, SJ, Jha, AN, et al. (2009) Supra-nutritional dietary intake of selenite and selenium yeast in normal and stressed rainbow trout (Oncorhynchus mykiss): implications on selenium status and health responses. Aquaculture 295, 282291.CrossRefGoogle Scholar
Dawood, MAO, Basuini, MF, El Yilmaz, S, et al. (2021) Selenium nanoparticles as a natural antioxidant and metabolic regulator in aquaculture: a review. Antioxidants 10, 1364.Google ScholarPubMed
Jovanovic, A, Grubor-Lajsic, G, Djukic, N, et al. (1997) The effect of selenium on antioxidant system in erythrocytes and liver of the carp (Cyprinus carpio L.). Crit Rev Food Sci Nutr 37, 443448.Google ScholarPubMed
Liu, Z, Huang, J, Nie, Y, et al. (2019) Selenium treatment enhanced clearance of salmonella in chicken macrophages (HD11). Antioxidants 8, 532.CrossRefGoogle ScholarPubMed
Chen, K, Li, E, Li, T, et al. (2015) Transcriptome and molecular pathway analysis of the hepatopancreas in the Pacific white shrimp Litopenaeus vannamei under chronic low-salinity stress. PLoS ONE 10, e0131503.Google ScholarPubMed
Labunskyy, VM, Lee, BC, Handy, DE, et al. (2011) Both maximal expression of selenoproteins and selenoprotein deficiency can promote development of type 2 diabetes-like phenotype in mice. Antioxid Redox Signal 14, 23272336.CrossRefGoogle ScholarPubMed
Seale, LA, Hashimoto, AC, Kurokawa, S, et al. (2012) Disruption of the selenocysteine lyase-mediated selenium recycling pathway leads to metabolic syndrome in mice. Mol Cell Biol 32, 41414154.Google ScholarPubMed
Phillips, D, Covian, R, Aponte, AM, et al. (2012) Regulation of oxidative phosphorylation complex activity: effects of tissue-specific metabolic stress within an allometric series and acute changes in workload. Am J Physiol Integr Comp Physiol 302, R1034R1048.CrossRefGoogle ScholarPubMed
Li, E, Wang, S, Li, C, et al. (2014) Transcriptome sequencing revealed the genes and pathways involved in salinity stress of Chinese mitten crab, Eriocheir sinensis . Physiol Genomics 46, 177190.Google ScholarPubMed
Jacquemin, G, Margiotta, D, Kasahara, A, et al. (2015) Granzyme B-induced mitochondrial ROS are required for apoptosis. Cell Death Differ 22, 862874.Google ScholarPubMed
Wang, M, Wang, D, Lin, L, et al. (2010) Protein profiles in zebrafish (Danio rerio) brains exposed to chronic microcystin-LR. Chemosphere 81, 716724.Google ScholarPubMed
Brown, KH (2008) Fish mitochondrial genomics: sequence, inheritance and functional variation. J Fish Biol 72, 355374.CrossRefGoogle Scholar
Chen, L, Hu, Y, He, J, et al. (2017) Responses of the proteome and metabolome in livers of Zebrafish exposed chronically to environmentally relevant concentrations of microcystin-LR. Environ Sci Technol 51, 596607.CrossRefGoogle ScholarPubMed
Du, X, Shi, Q, Zhao, Y, et al. (2021) Se-methylselenocysteine (smc) improves cognitive deficits by attenuating synaptic and metabolic abnormalities in Alzheimer’s mice model: a proteomic study. ACS Chem Neurosci 12, 11121132.Google Scholar
Frye, CA (2009) Steroids, reproductive endocrine function, and affect. A review. Minerva Ginecol 61, 541562.Google ScholarPubMed
Funder, JW, Krozowski, Z, Myles, K, et al. (1997) Mineralocorticoid receptors, salt, and hypertension. Recent Prog Horm Res 52, 247260.Google ScholarPubMed
Gupta, BBP & Lalchhandama, K (2002) Molecular mechanisms of glucocorticoid action. Curr Sci 83, 11031111.Google Scholar
Shao, C, Song, J, Zhao, S, et al. (2018) Therapeutic effect and metabolic mechanism of a selenium-polysaccharide from Ziyang green tea on chronic fatigue syndrome. Polymers 10, 1269.Google ScholarPubMed
Birukawa, N, Ando, H, Goto, M, et al. (2005) Plasma and urine levels of electrolytes, urea and steroid hormones involved in osmoregulation of cetaceans. Zoolog Sci 22, 12451257.Google ScholarPubMed