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Dietary Saccharina japonica is a natural and effective tool to fortify marine teleost black sea bream fillets with iodine: effects on growth, flesh quality, and serum thyroid hormones

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Abstract

In the present study the effects of dietary Saccharina japonica on growth performance, flesh quality traits, and serum thyroid hormones (tetraiodothyronine (T4) and triiodothyronine (T3)) of juvenile black sea bream, Acanthopagrus schlegelii, were investigated. Seven diets containing graded levels of S. japonica (0, 0.1, 0.2, 1.2, 2.5, 5, and 10%) were formulated. Each diet was randomly assigned to sex replicate groups of 40 fish. After a 90-day feeding trial, the best growth performance was achieved in fish fed with the 2.5% S. japonica diet, with significantly higher weight gain rate (WGR) and lower feed coefficient (FC) than those fed with the other diets (P < 0.05). Meanwhile, S. japonica supplementation had no significant effects (P > 0.05) on proximate composition of the whole body and the muscle. However, the content of n-6PUFA, n-3PUFA, and LC-PUFA in the muscle was significantly increased with the increasing level of dietary S. japonica. No differences in the flesh texture, cooked meat rate and water holding capacity were found among fish fed with different diets. It was further demonstrated that dietary S. japonica significantly fortify fillets with iodine (from 0.11 to 1.05 mg kg−1DM) and increased serum T4 and T3 levels. These results showed that the inclusion of up to 2.5% of S. japonica meal in diets could be beneficial to aquaculture of juvenile black sea bream, while higher inclusion levels resulted in significantly smaller fish. Moreover, the content of flesh iodine content quintupled in fish fed 2.5% up to 2.5%, confirming S. japonica as a natural and effective tool to increase the nutritional value of juvenile black sea bream.

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References

  • Ambrosio R, De Stefano MA, Di Girolamob D, Salvatore D (2017) Thyroid hormone signaling and deiodinase actions in muscle stem/progenitor cells. Mol Cell Endocrinol 459:79–83

    CAS  PubMed  Google Scholar 

  • Andersen UB, Thomassen MS, Rørå AMB (1997) Texture properties of farmed rainbow trout (Oncorhynchus mykiss): effects of diet, muscle fat content and time of storage on ice. J Sci Food Agric 74:347–353

    CAS  Google Scholar 

  • AOAC (Association of Official Analytical Chemists) (2000) In: Cunniff PA (ed) Official methods of analysis of the AOAC international, 16th edn. USA, AOAC International, Arlington, VA

    Google Scholar 

  • Ayala MD, Abdel I, Santaella M, Martinez C, Periago MJ, Gil F, Blanco A, Albors OL (2010) Muscle tissue structural changes and texture development in sea bream, Sparus aurata L., during post-mortem storage. LWT-Food Sci Technol 43:465–475

    CAS  Google Scholar 

  • Bloise FF, Cordeiro A, Ortiga-Carvalho TM (2017) Role of thyroid hormone in skeletal muscle physiology. J Endocrinol 236:R57–R68

    PubMed  Google Scholar 

  • Brown CL, Doroshov SI, Nunez JM, Hadley C, Vaneenennaam J, Nishioka RS, Bern HA (1988) Maternal triiodothyronine injections cause increases in swimbladder inflation and survival rates in larval striped bass, Morone saxatilis. J Exp Zool 248:168–176

    CAS  Google Scholar 

  • Brown SB, Adams BA, Cyr DG, Eales JG (2004) Contaminant effects on the teleost fish thyroid. Environ Toxicol Chem 23:1680–1701

    CAS  PubMed  Google Scholar 

  • Buehrlen B, Canavari M, Breitschopf B (2005) Determinants of consumer preferences towards functional foods with seaweed ingredients. 97th EAAE seminar ‘The economics and policy of diet and Health’ Whiteknights Campus, University of Reading (UK), April 21st–22nd

  • Carbonell I, Duran L, Izquierdo L, Costell E (2003) Texture of cultured gilthead sea bream (Sparus aurata): instrumental and sensory measurement. J Texture Stud 34:203–217

    Google Scholar 

  • Cassar-Malek I, Marchal S, Rochard P, Casas F, Wrutniak C, Samarut J, Cabello G (1996) Induction of c-Erb A-AP-1 interactions and c-Erb A transcriptional activity in myoblasts by RXR. Consequences for muscle differentiation. J Biol Chem 271:11392–11399

    CAS  PubMed  Google Scholar 

  • Dantagnan P, Hernandez A, Borquez A, Mansilla A (2009) Inclusion of macroalgae meal (Macrocystis pyrifera) as feed ingredient for rainbow trout (Oncorhynchus mykiss): effect on flesh fatty acid composition. Aquac Res 41:87–94

    CAS  Google Scholar 

  • De la Vieja A, Santisteban P (2018) Role of iodide metabolism in physiology and cancer. Endocr Relat Cancer 25:R225–R245

    PubMed  Google Scholar 

  • Dickson-Spillmann M, Siegrist M, Keller C (2011) Attitudes toward chemicals are associated with preference for natural food. Food Qual Prefer 22:149–156

    Google Scholar 

  • Do JR, Kim EM, Koo JG, Jo KS (1997) Dietary fiber contents of marine algae and extraction condition of the fiber. J Korean Fish Soc 30:291–296

    Google Scholar 

  • EFSA (2005) Opinion of the scientific panel on additives and products or substances used in animal feed on the request from the commission on the use of iodine in feeding stuffs. EFSA J 168:1–42

    Google Scholar 

  • EFSA (2014) Scientific opinion on health benefits of seafood (fish and shellfish) consumption in relation to health risks associated with exposure to methylmercury. EFSA J 12:3761

    Google Scholar 

  • FAO (2015) Food outlook: biannual report on global food markets. May 2015. FAO Trade and Markets Division, Rome (136 pp)

    Google Scholar 

  • Furuya VRB, Furaya WM, Hayshi C, Soares CM (2000) Niveles de inclusión de harina de girasol en la alimentación de la tilapia del Nilo (Oreochromis niloticus) en etapa juvenil. Zootec Trop 18:1–10

    Google Scholar 

  • Gao J, Lin LZ, Sun BG, Zhao MM (2017) A comparison study on polysaccharides extracted from Saccharina japonica using different methods: structural characterization and bile acid-binding capacity. Food Funct 8:3043–3052

    CAS  PubMed  Google Scholar 

  • Gensic M, Wissing PJ, Keefe TR, Mustafa A (2004) Effects of iodized feed on stress modulation in steelhead trout, Oncorhynchus mykiss (Walbaum). Aquac Res 35:1117–1121

    CAS  Google Scholar 

  • Glencross B (2009) The influence of soluble and insoluble lupin non-starch polysaccharides on the digestibility of diets fed to rainbow trout (Oncorhynchus mykiss). Aquaculture 294:256–261

    CAS  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    CAS  Google Scholar 

  • Hou X, Chai C, Qian Q, Yan X, Fan X (1997) Determination of chemical species of iodine in some seaweeds (I). Sci Total Environ 204:215–221

    Google Scholar 

  • Julshamn K, Maage A, Waagbo R, Lundebye AK (2006) A preliminary study on tailoring of fillet iodine concentrations in adult Atlantic salmon (Salmo salar L.) through dietary supplementation. Aquac Nutr 12:45–51

    CAS  Google Scholar 

  • Kim J-Y, Kwon YM, Kim I-S, Kim J-A, Yu D-Y, Adhikari B, Lee S-S, Choi I-S, Cho K-K (2018) Effects of the brown seaweed Saccharina japonica supplementation on serum concentrations of IgG, triglycerides, and cholesterol, and intestinal microbiota composition in rats. Front Nutr 5:23

    PubMed  PubMed Central  Google Scholar 

  • Konno N, Yuri K, Taguchi H, Miura K, Taguchi S, Hagiwara K, Murakami S (1993) Screening for thyroid diseases in an iodine sufficient area with sensitive thyrotrophin assays, and serum thyroid autoantibody and urinary iodide determinations. Clin Endocrinol 38:273–281

    CAS  Google Scholar 

  • Kraan S, Mair C (2010) Seaweeds as ingredients in aquatic feeds. Turk J Fish Aquat Sci 13:10–14

    Google Scholar 

  • Kumar CS, Ganesan P, Suresh PV, Bhaskar N (2008) Seaweeds as a source of nutritionally beneficial compounds - a review. J Food Sci Tech Mysore 45:1–13

    CAS  Google Scholar 

  • Kupper FC, Carrano CJ (2019) Key aspects of the iodine metabolism in brown algae: a brief critical review. Metallomics 11:756–764

    CAS  PubMed  Google Scholar 

  • Larsen R, Eilertsen K-E, Elvevoll EO (2011) Health benefits of marine foods and ingredients. Biotechnol Adv 29:508–518

    CAS  PubMed  Google Scholar 

  • Leung AM, Braverman LE (2014) Consequences of excess iodine. Nat Rev Endocrinol 10:136–142

    CAS  Google Scholar 

  • Li Y, Hu C, Zheng Y, Xia X, Xu W, Wang S, Chen W, Sun Z, Huang J (2008) The effects of dietary fatty acids on liver fatty acid composition and delta 6-desaturase expression differ with ambient salinities in Siganus canaliculatus. Comp Biochem Physiol B 151:183–190

    PubMed  Google Scholar 

  • Li Y, Monroig O, Zhang L, Wang S, Zheng X, Dick JR, You C, Tocher DR (2010) Vertebrate fatty acyl desaturase with D4 activity. Proc Natl Acad Sci U S A 107:16840–16845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li MH, Oberle DF, Lucas PM (2012a) Effects of dietary fiber concentrations supplied by corn bran on feed intake, growth, and feed efficiency of channel catfish. N Am J Aquac 74:148–153

    Google Scholar 

  • Li QM, Mair C, Schedle K, Hammerl S, Schodl K, Windisch W (2012b) Effect of iodine source and dose on growth and iodine content in tissue and plasma thyroid hormones in fattening pigs. Eur J Nutr 51:685–691

    CAS  PubMed  Google Scholar 

  • Li M, Zhang M, Ma Y, Ye R, Wang M, Chen H, Xie D, Dong Y, Ning L, You C, Wang S, Li Y (2019) Dietary supplementation with n-3 high unsaturated fatty acids decreases serum lipid levels and improves flesh quality in the marine teleost golden pompano Trachinotus ovatus. Aquaculture 734632

  • Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Physiol B 129:207–219

    CAS  PubMed  Google Scholar 

  • Mørkøre T, Hansen AÅ, Unander E, Einen O (2002) Composition, liquid leakage, and mechanical properties of farmed rainbow trout: variation between fillet sections and the impact of ice and frozen storage. J Food Sci 67:1933–1938

    Google Scholar 

  • Morshedi V, Nafisi Bahabadi M, Sotoudeh E, Azodi M, Hafezieh M (2018) Nutritional evaluation of Gracilaria pulvinata as partial substitute with fish meal in practical diets of barramundi (Lates calcarifer). J Appl Phycol 30:619–628

    CAS  Google Scholar 

  • Moutinho S, Linares F, Rodríguez JL, Sousa V, Valente LMP (2018) Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). J Appl Phycol 30:3589–3601

    CAS  Google Scholar 

  • Nakagawa HSM, Gatlin DM III (2007) Dietary supplements for the health and quality of cultured fish. CABI, Wallingford, pp 133–167 168–177

    Google Scholar 

  • Ng WK, Bahurmiz OM (2009) The impact of dietary oil source and frozen storage on the physical, chemical and sensorial quality of fillets from market size red hybrid tilapia, Oreochromis sp. Food Chem 113:1041–1048

    CAS  Google Scholar 

  • Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, Beard A, Turchini GM (2015) Algae in fish feed: performances and fatty acid metabolism in juvenile Atlantic salmon. PLoS One 10:e0124042

    PubMed  PubMed Central  Google Scholar 

  • Qin F, Zhu X, Zhang W, Zhou J, Zhang S, Jia Z (2011) Effects of dietary iodine and selenium on nutrient digestibility, serum thyroid hormones, and antioxidant status of Liaoning cashmere goats. Biol Trace Elem Res 143:1480–1488

    CAS  PubMed  Google Scholar 

  • Ragaza JA, Koshio S, Mamauag RE, Ishikawa M, Yokoyama S, Villamor SS (2013) Dietary supplemental effects of red seaweed Eucheuma denticulatum on growth performance, carcass composition and blood chemistry of juvenile Japanese flounder, Paralichthys olivaceus. Aquac Res 46:647–657

    Google Scholar 

  • Reid SNS, Ryu JK, Kim Y, Jeon BH (2018) The effects of fermented Laminaria japonica on short-term working memory and physical fitness in the elderly. Evid Based Complement Alternat Med 2018:1–12

    Google Scholar 

  • Ribeiro ARA, Ribeiro L, Saele O, Dinis MT, Moren M (2012) Iodine and selenium supplementation increased survival and changed thyroid hormone status in Senegalese sole (Solea senegalensis) larvae reared in a recirculation system. Fish Physiol Biochem 38:725–734

    CAS  PubMed  Google Scholar 

  • Ribeiro AR, Goncalves A, Colen R, Nunes ML, Dinis MT, Dias J (2015) Dietary macroalgae is a natural and effective tool to fortify gilthead seabream fillets with iodine: effects on growth, sensory quality and nutritional value. Aquaculture 437:51–59

    Google Scholar 

  • Ribeiro AR, Goncalves A, Bandarra N, Nunes ML, Dinis MT, Dias J, Rema P (2017) Natural fortification fortification of trout with dietary macroalgae and selenised-yeast increases the nutritional contribution in iodine and selenium. Food Res Int 99:1103–1109

    Google Scholar 

  • Sargent JR, Tocher DR, Bell JG (2003) Fish nutrition. Academic Press, New York

    Google Scholar 

  • Schmid S, Ranz D, He ML, Burkard S, Lukowicz MV, Reiter R, Arnold R, Le Deit H, David M, Rambeck WA (2003) Marine algae as natural source of iodine in the feeding of freshwater fish - a new possibility to improve iodine supply of man. Rev Med Vet-Toulouse 154:645–648

    CAS  Google Scholar 

  • Shi QC, Rong H, Hao ML, Zhu DS, Aweya JJ, Li SK, Wen XB (2019) Effects of dietary Sargassum horneri on growth performance, serum biochemical parameters, hepatic antioxidant status, and immune responses of juvenile black sea bream Acanthopagrus schlegelii. J Appl Phycol 31:2103–2113

    CAS  Google Scholar 

  • Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquac Res 41:717–732

    CAS  Google Scholar 

  • Valente LMP, Rema P, Ferraro V, Pintado M, Sousa-Pinto I, Cunha LM, Oliveira MB, Araujo M (2015) Iodine enrichment of rainbow trout flesh by dietary supplementation with the red seaweed Gracilaria vermiculophylla. Aquaculture 446:132–139

    CAS  Google Scholar 

  • Wang XT, Wang LL, Che J, Li Z, Zhang JC, Li XY, Hu WQ, Xu YP (2015) Improving the quality of Saccharina japonica-based diet for Apostichopus japonicus through degradation of its algin content with Bacillus amyloliquefaciens WB1. Appl Microbiol Biotechnol 99:5843–5853

    CAS  PubMed  Google Scholar 

  • Wang C, Hu W, Wang L, Qiao H, Wu H, Xu Z (2019) Effects of dietary supplementation with Sargassum horneri meal on growth performance, body composition, and immune response of juvenile turbot. J Appl Phycol 31:771–778

    CAS  Google Scholar 

  • Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151:185–207

    CAS  Google Scholar 

  • Weng HX, Liu HP, Li DW, Ye ML, Pan LH, Xia TH (2014) An innovative approach for iodine supplementation using iodine-rich phytogenic food. Environ Geochem Health 36:815–828

    CAS  PubMed  Google Scholar 

  • WHO (2008) WHO expert consultation on salt as a vehicle for fortification. WHO, Geneva

    Google Scholar 

  • WHO UNICEF, ICCIDD (2007) Assessment of iodine deficiency disorders and monitoring their elimination: a guide for programme managers, 3rd edn. WHO, Geneva

    Google Scholar 

  • Witt EM, Laidley CW, Liu KKM, Hirano T, Grau EG (2009) Correlation between environmental iodide concentrations and larval growth, survival, and whole body concentrations of thyroid hormones and cortisol in Pacific threadfin (Polydactylus sexfilis). Aquaculture 289:357–364

    CAS  Google Scholar 

  • Zimmermann MB (2009) Iodine deficiency. Endocr Rev 30:376–408

    CAS  PubMed  Google Scholar 

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This work was supported by grant No. 31972806 from the National Natural Science Foundation of China.

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Correspondence to Xiaobo Wen.

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Yu, C., Liu, G., Yu, J. et al. Dietary Saccharina japonica is a natural and effective tool to fortify marine teleost black sea bream fillets with iodine: effects on growth, flesh quality, and serum thyroid hormones. J Appl Phycol 32, 3447–3456 (2020). https://doi.org/10.1007/s10811-020-02131-2

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