Abstract
The genus Chirostoma (silversides) belongs to the family Atherinopsidae, which contains around 150 species, most of which are marine. However, Mexican silverside (Chirostoma estor) is one of the few representatives of freshwater atherinopsids and is only found in some lakes of the Mexican Central Plateau. However, studies have shown that C. estor has improved survival, growth, and development when cultured in water conditions with increased salinity. In addition, C. estor displays an unusual fatty acid composition for a freshwater fish with high docosahexaenoic acid (DHA)/ eicosapentaenoic acid (EPA) ratios. Freshwater and marine fish species display very different essential fatty acid metabolism and requirements, and so the present study investigated long-chain polyunsaturated fatty acid (LC-PUFA) biosynthesis to determine the capacity of C. estor for endogenous production of EPA and DHA, and the effect that salinity has on these pathways. Briefly, C. estor were maintained at three salinities (0, 5, and 15 ppt), and the metabolism of 14C-labeled 18:3n-3 was determined in isolated hepatocyte and enterocyte cells. The results showed that C. estor has the capacity for endogenous biosynthesis of LC-PUFA from 18-carbon fatty acid precursors, but that the pathway was essentially only active in saline conditions with virtually no activity in cells isolated from fish grown in freshwater. The activity of the LC-PUFA biosynthesis pathway was also higher in cells isolated from fish at 15 ppt compared with fish at 5 ppt. The activity was around fivefold higher in hepatocytes compared with enterocytes; although the majority of 18:3n-3 was converted to 18:4n-3 and 20:4n-3 in hepatocytes, the proportions of 18:3n-3 converted to EPA and DHA were higher in enterocytes. The data were consistent with the hypothesis that conversion of EPA to DHA could contribute, at least in part, to the generally high DHA/EPA ratios observed in the tissue lipids of C. estor.
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References
Ackman RG (1980) Fish lipids, part 1. In: Connell JJ (ed) Advances in fish science and technology. Fishing News Books, Farnham, pp 87–103
Barbour CD (1973) The systematics and evolution of the genus Chirostoma Swainson (Pisces: Atherinidae). Tulanne Stud Zool Bot 18:97–141
Bell JG, Tocher DR, Farndale BM, Cox DI, McKinney RW, Sargent JR (1997) The effect of dietary lipid on polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Lipids 32:515–525
Bendiksen EA, Arnesen AM, Jobling M (2003) Effects of dietary fatty acid profile and fat content on smolting and seawater performance in Atlantic salmon (Salmo salar L). Aquaculture 225:149–163
Bœuf G, Payan P (2001) How should salinity influences growth? Comp Biochem Physiol 130C:411–423
Borlongan IG, Benitez LV (1992) Lipid and fatty acid composition of milkfish (Chanos chanos) Forsskal grown in fresh water and seawater. Aquaculture 104:79–89
Christie WW (1993) Preparation of derivatives of fatty acids for chromatographic analysis. In: Christie WW (ed) Advances in lipid methodology—two. The Oily Press, Dundee, pp 69–111
Cordier M, Brichon G, Weber J-M, Zwingelstein G (2002) Changes in fatty acid composition of phospholipids in tissues of farmed sea bass (Dicentrarchus labrax) during an annual cycle. Roles of environmental temperature and salinity. Comp Biochem Physiol 133B:281–288
Daikoku T, Yano I, Masui M (1982) Lipid and fatty acid compositions and their changes in the different organs and tissues of guppy, Poecilia reticulate on sea water adaptation. Comp Biochem Physiol 73A:167–174
Dantagnan H, Borquez AS, Valdebenito IN, Salgado IA, Serrano EA, Izquierdo MS (2007) Lipid and fatty acid composition during embryo and larval development of puye Galaxias maculatus Jenyns, 1842, obtained from estuarine, freshwater and cultured populations. J Fish Biol 70:770–781
Fonseca-Madrigal J, Karalazos PJ, Campbell PJ, Bell JG, Tocher DR (2005) Influence of dietary palm oil on growth, tissue fatty acid compositions, and fatty acid metabolism in liver and intestine in rainbow trout (Oncorhynchus mykiss). Aquac Nutr 11:241–250
Fonseca-Madrigal J, Bell JG, Tocher DR (2006) Nutritional and environmental regulation of the synthesis of highly unsaturated fatty acids and fatty-acid oxidation in Atlantic salmon (Salmo salar L.) enterocytes and hepatocytes. Fish Physiol Biochem 32:317–328
Ghioni C, Tocher DR, Sargent JR (1997) The effect of culture on morphology, lipid and fatty acid composition, and polyunsaturated fatty acid metabolism of rainbow trout (Oncorhynchus mykiss) skin cells. Fish Physiol Biochem 16:499–513
Grum DE, Drackley JK, Clark JH (2002) Fatty acid metabolism in liver of dairy cows fed supplemental fat and nicotinic acid during an entire lactation. J Dairy Sci 85:3026–3034
Haliloglu HI, Bayir A, Sirkecioglu AN, Aras NM, Atamanalp M (2004) Comparison of fatty acid composition in some tissues of rainbow trout (Oncorhynchus mykiss) living in seawater and freshwater. Food Chem 86:55–59
Hastings N, Agaba M, Tocher DR, Leaver MJ, Dick JR, Sargent JR, Teale AJ (2001) A vertebrate fatty acid desaturase with Δ6 and Δ5 activities. Proc Natl Acad Sci USA 98:14304–14309
Henderson RJ (1996) Fatty acid metabolism in freshwater fish with particular reference to polyunsaturated fatty acids. Arch Anim Nutr 49:5–22
Hunt AO, Oxkan FE, Engin K, Tekelioglu N (2011) The effects of freshwater rearing on the whole body and muscle tissue fatty acid profile of the European sea bass (Dicentrarchus labrax). Aquacult Int 19:51–61
Kheriji S, El Cafsi M, Masmoudi W, Castell JD, Romdhane MS (2003) Salinity and temperature effects on the lipid composition of mullet sea fry (Mugil cephalus, Linne, 1758). Aquacult Int 11:571–582
Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Río MP, Míguez JM, Soengas JL, Mancera JM (2004) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27:179–188
Leaver MJ, Bautista JM, Björnsson T, Jönsson E, Krey G, Tocher DR, Torstensen BE (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fisheries Sci 16(S1):71–92
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 151B:183–190
Li Y, Monroig Ó, Zhang L, Wang S, Zheng X, Dick JR, You C, Tocher DR (2010) Vertebrate fatty acyl desaturase with Δ4 activity. Proc Natl Acad Sci USA 107:16840–16845
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Martinez-Alvarez RM, Sanz A, Gracia-Gallego M, Domezain A, Domezain J, Carmona R, de ValleOstos-Garrido M, Morales AE (2005) Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to saltwater. Comp Biochem Physiol 141A:183–190
Martínez-Palacios CA, Barriga-Tovar E, Taylor JF, Ríos-Duran MG, Ross LG (2002) Effect of temperature on growth and survival of Chirostoma estor estor, Jordan 1879, monitored using a simple video technique for remote measurement of length and mass of larval and juvenile fishes. Aquaculture 209:369–377
Martínez-Palacios CA, Ríos-Duran MG, Campos-Mendoza A, Toledo-Cuevas M, Aguilar-Valdez MA, Ross LG (2003) Desarrollo tecnológico alcanzado en el cultivo del pez blanco de Pátzcuaro. In: Historia y avances del cultivo del pescado blanco, Instituto Nacional de la Pesca. Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. México
Martínez-Palacios CA, Comas Morte J, Tello-Ballinas JA, Toledo-Cuevas M, Ross LG (2004) The effects of saline environments on survival and growth of eggs and larvae of Chirostoma estor estor Jordan 1879 (Pisces: Atherinidae). Aquaculture 238:509–522
Martínez-Palacios CA, Racotta IS, Ríos-Duran MG, Palacios E, Toledo-Cuevas M, Ross LG (2006) Advances in applied research for the culture of Mexican silversides (Chirostoma, Atherinopsidae). Biocell 30:137–148
Martínez-Palacios CA, Ambriz-Cervantes L, Ríos-Duran MG, Jauncey KJ, Ross LG (2007) Dietary protein requirement of juvenile Mexican Silverside (Chirostoma estor estor Jordan 1879), a stomachless zooplanktophagous fish. Aquacult Nutr 13304–310
Martínez-Palacios CA, Ríos-Duran MG, Fonseca-Madrigal J, Toledo-Cuevas M, Sotelo Lopez A, Ross LG (2008) Developments in the nutrition of Menidia estor Jordan 1880. Aquacult Res 39:738–747
Monroig Ó, Zheng X, Morais S, Leaver MJ, Taggart JB, Tocher DR (2010) Multiple fatty acyl desaturase (FAD) genes in Atlantic salmon: cloning and functional expression of cDNAs confirm presence of three Δ6 FADs. Biochim Biophys Acta 1801:1072–1081
Morais S, Monroig O, Zheng X, Leaver MJ, Tocher DR (2009) Highly unsaturated fatty acid synthesis in Atlantic salmon: isolation of genes of fatty acyl elongases and characterisation of ELOVL5- and ELOVL2-like elongase cDNAs. Mar Biotechnol 11:627–639
Morgan JD (1997) Energetic aspects of osmoregulation in fish. Doctoral thesis. The University of British Columbia, Canada
National Research Council (2011) Nutrient requirements of fish and shrimp. National Academic Press, Washington
Navarro JC, Perez MJ, Acosta NG, Viciano E, Varo I, Urena R, Torreblanca A, Rodriguez C (2009) The fatty acid profiles of polar and neutral lipids from enterocytes and hepatocytes of gilthead seabream (Sparus aurata) cultured at two salinities: a chemometric approach. Comp Biochem Physiol 154A:S20
Nelson JS (2006) Fishes of the World, 4th edn. Wiley, New York
Olsen RE, Ringø E (1997) Lipid digestibility in fish: a review. Rec Res Dev Lipids Res 1:199–265
Palacios E, Racotta IS, Apaicio B, Arjona O, Martínez-Palacios CA (2007) Lipid classes and fatty acids during embryogenesis of captive and wild silverside (Chirostoma estor estor) from Pátzcuaro Lake. Fish Physiol Biochem 33:81–91
Peng J, Larondelle Y, Pham D, Ackman RG, Rollin X (2003) Polyunsaturated fatty acid profiles of whole body phospholipids and triacylglycerols in anadromous and landlocked Atlantic salmon (Salmo salar L.) fry. Comp Biochem Physiol 134B:335–348
Ross LG, Sánchez-Blanco J, Martínez-Palacios CA, Racotta IS, Toledo-Cuevas M (2007) Anesthesia, sedation and transportation of juvenile Menidia estor (Jordan) using benzocaine and hypothermia. Aquacult Res 38:909–917
Sargent JR, Henderson RJ, Tocher DR (1989) The lipids. In: Halver JE (ed) Fish nutrition, 2nd edn. Academic Press, San Diego, pp 154–219
Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995a) Requirement criteria for essential fatty acids. J Appl Ichthyol 11:183–198
Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995b) Dietary origins and functions of long-chain (n-3) polyunsaturated fatty acids in marine fish. J Mar Biotechnol 3:26–28
Sargent JR, Bell JG, McEvoy L, Tocher DR, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199
Sarkar MA, Yamamoto YH, YutakaSarker MSA, Miwa M, Yoshizaki G, Satoh S (2011) Influences of low salinity and dietary fatty acids on fatty acid composition and fatty acid desaturase and elongase expression in red sea bream Pagrus major. Fisheries Sci 77:385–396
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fisheries Sci 11:107–184
Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquacult Res 41:717–732
Tocher DR, Harvie DG (1988) Fatty acid compositions of the major phosphoglycerides from fish neural tissues; (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri) and cod (Gadus morhua) brains and retinas. Fish Physiol Biochem 5:229–239
Tocher DR, Castell JD, Dick JR, Sargent JR (1994) Effects of salinity on the growth and lipid composition of Atlantic salmon (Salmo salar) and turbot (Scophthalmus maximus) cells in culture. Fish Physiol Biochem 13:451–461
Tocher DR, Castell JD, Dick JR, Sargent JR (1995) Effects of salinity on the fatty acid compositions of total lipid and individual glycerophospholipid classes of Atlantic salmon (Salmo salar) and turbot (Scophthalmus maximus) cells in culture. Fish Physiol Biochem 14:125–137
Tocher DR, Bell JG, Dick JR, Sargent JR (1997) Fatty acyl desaturation in isolated hepatocytes from Atlantic salmon (Salmo salar): simulation by dietary borage oil containing γ-linolenic acid. Lipids 32:1237–1247
Tocher DR, Bell JG, Henderson RJ, McGhee F, Mitchell D, Morris PC (2000) Polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation and the effects of dietary linseed and rapeseed oils. Fish Physiol Biochem 23:59–73
Tocher DR, Fonseca-Madrigal J, Bell JG, Dick JR, Henderson RJ, Sargent JR (2002) Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol Biochem 26:157–170
Tocher DR, Zheng X, Schlechtriem C, Hastings N, Dick JR, Teale AJ (2006) Highly unsaturated fatty acid synthesis in marine fish: cloning, functional characterization, and nutritional regulation of fatty acyl Δ6 desaturase of Atlantic cod (Gadus morhua L.). Lipids 41:1003–1016
Vagner M, Santigosa E (2011) Characterization and modulation of gene expression and enzymatic activity of Δ-6 desaturase in teleosts: a review. Aquaculture 315:131–143
Wilson R, Sargent JR (1992) High resolution separation of polyunsaturated fatty acids by argentation thin-layer chromatography. J Chromatogr 623:403–407
Xu J, Yan B, Teng Y, Lou G, Lu Z (2010) Analysis of nutrient composition and fatty acid profiles of Japanese sea bass Lateolabrax japonicus (Cuvier) reared in seawater and freshwater. J Food Comps Anal 23:401–405
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hal, Upper Saddle River
Zheng X, Seiliez I, Hastings N, Tocher DR, Panserat S, Dickson CA, Bergot P, Teale AJ (2004) Characterization and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species. Comp Biochem Physiol 139B:269–279
Zheng X, Torstensen BE, Tocher DR, Dick JR, Henderson RJ, Bell JG (2005) Environmental and dietary influences on highly unsaturated fatty acid biosynthesis and expression of fatty acyl desaturase and elongase genes in liver of Atlantic salmon (Salmo salar). Biochim Biophys Acta 1734:13–24
Zheng X, Ding Z, Xu Y, Monroig O, Morais S, Tocher DR (2009) Physiological roles of fatty acyl desaturase and elongase in marine fish: characterisation of cDNAs of fatty acyl Δ6 desaturase and Elovl5 elongase of cobia (Rachycentron canadum). Aquaculture 290:122–131
Acknowledgments
Dr. Jorge Fonseca-Madrigal was supported by CONACyT, Mexico, with the research grant #61117. Dr. Rodríguez was supported by project CTM2006-14279-C02-02-MAR from Spanish MEC.
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Fonseca-Madrigal, J., Pineda-Delgado, D., Martínez-Palacios, C. et al. Effect of salinity on the biosynthesis of n-3 long-chain polyunsaturated fatty acids in silverside Chirostoma estor . Fish Physiol Biochem 38, 1047–1057 (2012). https://doi.org/10.1007/s10695-011-9589-6
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DOI: https://doi.org/10.1007/s10695-011-9589-6