Skip to main content Accessibility help
×
Home
Hostname: page-component-59b7f5684b-n9lxd Total loading time: 0.552 Render date: 2022-10-01T15:47:01.301Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Vitamin D impacts on the intestinal health, immune status and metabolism in turbot (Scophthalmus maximus L.)

Published online by Cambridge University Press:  21 January 2022

Rui Shao
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Jiayu Liu
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Yawen Lan
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Xinmeng Liao
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Jinjin Zhang
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Weiqi Xu
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China
Kangsen Mai
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China Pilot National Laboratory of Marine Science and Technology, Qingdao266237, People’s Republic of China
Qinghui Ai
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China Pilot National Laboratory of Marine Science and Technology, Qingdao266237, People’s Republic of China
Min Wan*
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao266003, People’s Republic of China Pilot National Laboratory of Marine Science and Technology, Qingdao266237, People’s Republic of China
*
*Corresponding author: Min Wan, email wanmin@ouc.edu.cn

Abstract

Vitamin D (VD) plays a vital role in various physiological processes in addition to its classic functions on maintaining the balance of Ca and P metabolism. However, there still are gaps to understand in depth the issues on the precise requirement, metabolic processes and physiological functions of VD in fish. In this study, we investigated the effects of VD on the growth, intestinal health, host immunity and metabolism in turbot (Scophthalmus maximus L.), one important commercial carnivorous fish in aquaculture, through the supplementation of different doses of dietary VD3 (0, 200, 400, 800 and 1600 μg VD3/kg diet). According to our results, the optimal VD3 level in the feed for turbot growth was estimated to be around 400 μg/kg, whereas VD3 deficiency or overdose in diets induced the intestinal inflammation, lowered the diversity of gut microbiota and impaired the host resistance to bacterial infection in turbot. Moreover, the level of 1α,25(OH)2D3, the active metabolite of VD3, reached a peak value in the turbot serum in the 400 μg group, although the concentrations of Ca and phosphate in the turbot were stable in all groups. Finally, the deficiency of dietary VD3 disturbed the nutritional metabolism in turbot, especially the metabolism of lipids and glucose. In conclusion, this study evaluated the optimal dose of dietary VD3 for turbot and provided the evidence that VD has a significant impact on intestinal health, host immunity and nutritional metabolism in fish, which deepened our understanding on the physiological functions and metabolism of VD3 in fish.

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

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Christakos, S, Dhawan, P, Verstuyf, A, et al. (2016) Vitamin D: metabolism, molecular mechanism of action, and pleiotropic effects. Physiol Rev 96, 365408.CrossRefGoogle ScholarPubMed
Jones, G, Prosser, DE & Kaufmann, M (2014) Cytochrome P450-mediated metabolism of vitamin D. J Lipid Res 55, 1331.CrossRefGoogle ScholarPubMed
Pike, JW, Meyer, MB, Lee, SM, et al. (2017) The vitamin D receptor: contemporary genomic approaches reveal new basic and translational insights. J Clin Invest 127, 11461154.CrossRefGoogle ScholarPubMed
Hanel, A & Carlberg, C (2020) Vitamin D and evolution: pharmacologic implications. Biochem Pharmacol 173, 113595.CrossRefGoogle ScholarPubMed
Sunita Rao, D & Raghuramulu, N (1996) Food chain as origin of vitamin D in fish. Comp Biochem Physiol Part A: Mol Integr Physiol 114, 1519.CrossRefGoogle Scholar
Howarth, DL, Law, SH, Barnes, B, et al. (2008) Paralogous vitamin D receptors in teleosts: transition of nuclear receptor function. Endocrinol 149, 24112422.CrossRefGoogle ScholarPubMed
Craig, TA, Sommer, S, Sussman, CR, et al. (2008) Expression and regulation of the vitamin D receptor in the zebrafish, Danio rerio. J Bone Miner Res 23, 14861496.CrossRefGoogle ScholarPubMed
Lock, EJ, Waagbø, R, Bonga, SW, et al. (2010) The significance of vitamin D for fish: a review. Aquacult Nutr 16, 100116.CrossRefGoogle Scholar
Cerezuela, R, Cuesta, A, Meseguer, J, et al. (2009) Effects of dietary vitamin D3 administration on innate immune parameters of seabream (Sparus aurata L.). Fish Shellfish Immunol 26, 243248.CrossRefGoogle Scholar
Fenwick, J (2011) Effect of vitamin D3 (cholecalciferol) on plasma calcium and intestinal 45calcium absorption in goldfish, Carassius auratus L. Can J Zool 62, 3436.CrossRefGoogle Scholar
National Research Council (2011) Nutrient Requirements of Fish and Shrimp. Washington, DC: National Academies Press.Google Scholar
Miao, LH, Ge, XP, Xie, J, et al. (2015) Dietary vitamin D3 requirement of Wuchang bream (Megalobrama amblycephala). Aquaculture 436, 104109.Google Scholar
He, S, Ding, M, Watson Ray, G, et al. (2021) Effect of dietary vitamin D levels on growth, serum biochemical parameters, lipid metabolism enzyme activities, fatty acid synthase and hepatic lipase mRNA expression for orange-spotted grouper (Epinephelus coioides) in growth mid-stage. Aquacult Nutr 27, 655665.CrossRefGoogle Scholar
Zhang, L, Li, J, Mai, K, et al. (2016) Effects of different dietary vitamin D contents on growth performance, calcium and phosphorus metabolism of juvenile Japanese Seabass (Lateolabrax japonicus). Chinese J Anim Nutr 28, 14021411.Google Scholar
Hodar, A, Vasava, R, Mahavadiya, D, et al. (2020) Fish meal and fish oil replacement for aqua feed formulation by using alternative sources: a review. J Exp Zool India 23, 1321.Google Scholar
Additives EPanel FEEDAP, Rychen, G, Aquilina, G, et al. (2017) Safety of vitamin D3 addition to feedingstuffs for fish. EFSA J 15, e04713.Google ScholarPubMed
Sassi, F, Tamone, C & D’Amelio, P (2018) Vitamin D: nutrient, hormone, and immunomodulator. Nutrients 10, 1656.CrossRefGoogle ScholarPubMed
Kongsbak, M, von Essen, MR, Boding, L, et al. (2014) Vitamin D up-regulates the vitamin D receptor by protecting it from proteasomal degradation in human CD4+ T Cells. PLOS ONE 9, e96695.CrossRefGoogle ScholarPubMed
Ooi, JH, McDaniel, KL, Weaver, V, et al. (2014) Murine CD8+ T cells but not macrophages express the vitamin D 1α-hydroxylase. J Nutr Biochem 25, 5865.CrossRefGoogle Scholar
Liu, PT, Stenger, S, Li, H, et al. (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 17701773.CrossRefGoogle ScholarPubMed
Gombart, AF, Borregaard, N & Koeffler, HP (2005) Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J 19, 10671077.CrossRefGoogle ScholarPubMed
Martineau, AR, Jolliffe, DA, Hooper, RL, et al. (2017) Vitamin D supplementation to prevent acute respiratory tract infections: systematic review and meta-analysis of individual participant data. Br Med J 356, i6583.CrossRefGoogle ScholarPubMed
Wan, M, Tang, X, Rekha, RS, et al. (2018) Prostaglandin E2 suppresses hCAP18/LL-37 expression in human macrophages via EP2/EP4: implications for treatment of Mycobacterium tuberculosis infection. FASEB J 32, 28272840.CrossRefGoogle ScholarPubMed
Cheng, K, Tang, Q, Guo, X, et al. (2020) High dose of dietary vitamin D(3) modulated the yellow catfish (Pelteobagrus fulvidraco) splenic innate immune response after Edwardsiella ictaluri infection. Fish Shellfish Immunol 100, 4148.CrossRefGoogle ScholarPubMed
Cheng, K, Tang, Q, Huang, Y, et al. (2020) Effect of vitamin D(3) on the immunomodulation of head kidney after Edwardsiella ictaluri challenge in yellow catfish (Pelteobagrus fulvidraco). Fish Shellfish Immunol 99, 353361.CrossRefGoogle Scholar
Soto-Davila, M, Valderrama, K, Inkpen, SM, et al. (2019) Effects of vitamin D2 (Ergocalciferol) and D3 (Cholecalciferol) on atlantic salmon (Salmo salar) primary macrophage immune response to aeromonas salmonicida subsp. salmonicida Infection. Front Immunol 10, 3011.CrossRefGoogle ScholarPubMed
Cheng, K, Ma, C, Guo, X, et al. (2020) Vitamin D(3) modulates yellow catfish (Pelteobagrus fulvidraco) immune function in vivo and in vitro and this involves the vitamin D(3)/VDR-type I interferon axis. Dev Comp Immunol 107, 103644.CrossRefGoogle ScholarPubMed
Polakof, S & Panserat, S (2016) How Tom Moon’s research highlighted the question of glucose tolerance in carnivorous fish. Comp Biochem Physiol B: Biochem Mol Biol 199, 4349.CrossRefGoogle ScholarPubMed
Peng, X, Shang, G, Wang, W, et al. (2017) Fatty acid oxidation in zebrafish adipose tissue is promoted by 1α,25(OH)(2)D(3). Cell Rep 19, 14441455.CrossRefGoogle Scholar
Sittipo, P, Lobionda, S, Lee, YK, et al. (2018) Intestinal microbiota and the immune system in metabolic diseases. J Microbiol 56, 154162.CrossRefGoogle ScholarPubMed
Wang, J, Thingholm, LB, Skieceviciene, J, et al. (2016) Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat Genet 48, 13961406.CrossRefGoogle ScholarPubMed
Bora, SA, Kennett, MJ, Smith, PB, et al. (2018) The gut microbiota regulates endocrine vitamin d metabolism through fibroblast growth factor 23. Front Immunol 9, 408.CrossRefGoogle ScholarPubMed
Pereiro, P, Figueras, A & Novoa, B (2016) Turbot (Scophthalmus maximus) v. VHSV (Viral Hemorrhagic Septicemia Virus): a review. Front Aquat Physiol 7, 192.Google Scholar
Kaushik, SJ (1998) Whole body amino acid composition of European seabass (Dicentrarchus labrax), gilthead seabream (Sparus aurata) and turbot (Psetta maxima) with an estimation of their IAA requirement profiles. Aquat Living Resour 11, 355358.CrossRefGoogle Scholar
Horvli, O & Lie, Ø (1994) Determination of vitamin D3 in fish meals by HPLC. Fisk Dir Skr Ser Ern 6, 163175.Google Scholar
Cunniff, P (1995) Official methods of analysis of the Association of Official Analytical Chemists (AOAC). 16th ed. Arlington: AOAC International.Google Scholar
Edgar, RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Meth 10, 996998.CrossRefGoogle ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acid Res 41, D590596.CrossRefGoogle ScholarPubMed
Barnett, BJ, Cho, CY & Slinger, SJ (1979) The essentiality of cholecalciferol in the diets of rainbow trout (Salmo gairdneri). Comp Biochem Physiol Part A: Mol Integr Physiol 63, 291297.CrossRefGoogle Scholar
Baker, DH (1986) Problems and pitfalls in animal experiments designed to establish dietary requirements for essential nutrients. J Nutr 116, 23392349.CrossRefGoogle ScholarPubMed
Wu, C, Lu, B, Wang, Y, et al. (2020) Effects of dietary vitamin D(3) on growth performance, antioxidant capacities and innate immune responses in juvenile black carp Mylopharyngodon piceus. Fish Physiol Biochem 46, 22432256.CrossRefGoogle ScholarPubMed
Shiau, S-Y & Hwang, J-Y (1993) Vitamin D requirements of juvenile hybrid tilapia (Oreochromis niloticus×O. aureus). Nippon Suisan Gakkaishi 59, 553558.CrossRefGoogle Scholar
Ashok, A, Rao, DS & Raghuramulu, N (1998) Vitamin D is not an essential nutrient for Rora (Labeo rohita) as a representative of freshwater fish. J Nutr Sci Vitaminol 44, 195205.CrossRefGoogle Scholar
Prabhu, PAJ, Lock, E-J, Hemre, G-I, et al. (2019) Recommendations for dietary level of micro-minerals and vitamin D3 to Atlantic salmon (Salmo salar) parr and post-smolt when fed low fish meal diets. PeerJ 7, e6996.CrossRefGoogle Scholar
Dominguez, D, Montero, D, Zamorano, MJ, et al. (2021) Effects of vitamin D3 supplementation in gilthead seabream (Sparus aurata) juveniles fed diets high in plant based feedstuffs. Aquaculture 543, 736991.CrossRefGoogle Scholar
Graff, IE, Hoie, SM, Totland, GK, et al. (2002) Three different levels of dietary vitamin D3 fed to firs” feeding fry of Atlantic salmon (Salmo salar L.): effect on growth, mortality, calcium content and bone formation. Aquacult Nutr 8, 103111.CrossRefGoogle Scholar
Jiang, J, Shi, D, Zhou, X-Q, et al. (2015) Vitamin D inhibits lipopolysaccharide-induced inflammatory response potentially through the Toll-like receptor 4 signalling pathway in the intestine and enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Br J Nutr 114, 15601568.CrossRefGoogle Scholar
Zhao, H, Zhang, H, Wu, H, et al. (2012) Protective role of 1,25(OH)2 vitamin D3 in the mucosal injury and epithelial barrier disruption in DSS-induced acute colitis in mice. BMC Gastroenterol 12, 57.CrossRefGoogle ScholarPubMed
Dioguardi, M, Guardiola, FA, Vazzana, M, et al. (2017) Vitamin D(3) affects innate immune status of European sea bass (Dicentrarchus labrax L.). Fish Physiol Biochem 43, 11611174.CrossRefGoogle Scholar
Liu, J, Shao, R, Lan, Y, et al. (2021) Vitamin D(3) protects turbot (Scophthalmus maximus L.) from bacterial infection. Fish Shellfish Immunol 118, 2533.CrossRefGoogle Scholar
Cantorna, MT, Rogers, CJ & Arora, J (2019) Aligning the paradoxical role of vitamin D in gastrointestinal immunity. Trends Endocrinol Metab 30, 459466.CrossRefGoogle ScholarPubMed
Estévez, RA, Mostazo, MGC, Rodriguez, E, et al. (2018) Inducers of salmon innate immunity: an in vitro and in vivo approach. Fish Shellfish Immunol 72, 247258.CrossRefGoogle Scholar
Zuk, A, Fitzpatrick, T & Rosella, LC (2016) Effect of vitamin D3 supplementation on inflammatory markers and glycemic measures among overweight or obese adults: a systematic review of randomized controlled trials. PLOS ONE 11, e0154215.CrossRefGoogle ScholarPubMed
Craig, TA, Zhang, Y, McNulty, MS, et al. (2012) Research resource: whole transcriptome RNA sequencing detects multiple 1α,25-dihydroxyvitamin D(3)-sensitive metabolic pathways in developing zebrafish. Mol Endocrinol 26, 16301642.CrossRefGoogle ScholarPubMed
Round, JL, Mazmanian, SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9, 313323.CrossRefGoogle ScholarPubMed
Jin, D, Wu, S, Zhang, YG, et al. (2015) Lack of vitamin D receptor causes dysbiosis and changes the functions of the murine intestinal microbiome. Clin Ther 37, 9961009.e1007.CrossRefGoogle ScholarPubMed
Garcia, PM, Moore, J, Kahan, D, et al. (2020) Effects of vitamin D supplementation on inflammation, colonic cell kinetics, and microbiota in colitis: a review. Molecules 25, 2300.CrossRefGoogle ScholarPubMed
Chatterjee, I, Lu, R, Zhang, Y, et al. (2020) Vitamin D receptor promotes healthy microbial metabolites and microbiome. Sci Rep 10, 7340.CrossRefGoogle ScholarPubMed
Takeuchi, A, Okano, T & Kobayashi, T (1991) The existence of 25-hydroxyvitamin D3–1α-hydroxylase in the liver of carp and bastard halibut. Life Sci 48, 275282.CrossRefGoogle Scholar
Sunita Rao, D & Raghuramulu, N (1998) Vitamin D metabolism in tilapia (Oreochromis mossambicus). Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 120, 145149.Google Scholar
Fraser, DR (2018) Chapter 2 – evolutionary biology: mysteries of vitamin D in fish. In Vitamin D, Volume 1: Biochemistry, Physiology and Diagnostics, 4th ed., pp. 13–27 [D Feldman, editor]. Cambridge, MA: Academic Press.Google Scholar
Henry, HL (2011) Regulation of vitamin D metabolism. Best Pract Res Clin Endocrinol Metab 25, 531541.CrossRefGoogle ScholarPubMed
Bikle, DD, Murphy, EW & Rasmussen, H (1975) The ionic control of 1,25-dihydroxyvitamin D3 synthesis in isolated chick renal mitochondria. The role of calcium as influenced by inorganic phosphate and hydrogen-ion. J Clin Invest 55, 299304.CrossRefGoogle ScholarPubMed
McCollum, EV, Simmonds, N, Becker, JE, et al. (1925) The effect of additions of fluorine to the diet of the rat on the quality of the teeth. J Biol Chem 63, 553562.CrossRefGoogle Scholar
Sunita Rao, D & Raghuramulu, N (1996) Lack of vitamin D3 synthesis in Tilapia mossambica from cholesterol and acetate. Comp Biochem Physiol Part A: Mol Integr Physiol 114, 2125.CrossRefGoogle Scholar
Darias, MJ, Mazurais, D, Koumoundouros, G, et al. (2010) Dietary vitamin D3 affects digestive system ontogenesis and ossification in European sea bass (Dicentrarchus labrax, Linnaeus, 1758). Aquaculture 298, 300307.CrossRefGoogle Scholar

Linked content

Please note a has been issued for this article.

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Vitamin D impacts on the intestinal health, immune status and metabolism in turbot (Scophthalmus maximus L.)
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Vitamin D impacts on the intestinal health, immune status and metabolism in turbot (Scophthalmus maximus L.)
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Vitamin D impacts on the intestinal health, immune status and metabolism in turbot (Scophthalmus maximus L.)
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *