Article

Lipid and Fatty Acid Status of the Liver and Gonads of the Three-Spined Stickleback Gasterosteus aculeatus (Gastrosteidae) from Different Spawning Grounds in the White Sea

Authors:
  • Institute of Biology of the Karelian Research Cenre of the Russian Acaemy of Sciences
  • Institut of Biology of Karelian Research Centre of the Russian Academy of Sciences
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Abstract

The content of the total lipids, including structural and storage, and fatty acids (FAs) was evaluated in the liver and gonads of females of the three-spined stickleback Gasterosteus aculeatus from different spawning grounds of the White Sea: in Sel’dyanaya Inlet and Kolyushkovaya Lagoon (Kandalaksha Bay), and in Konyukhov Bay (Onega Bay). The content of total lipids in the gonads was high (from 14.25 to 20.05% of dry weight); while significant differences in their content, as well as in the quantitative profile of the main lipid classes, may indicate differences in the spawning peculiarities. In the gonads, the amount of the structural phospholipids was different, but the most pronounced variations were registered in the content of the reserve triacylglycerols and their components, in particular, two essential polyunsaturated FAs (22:6n-3, docosahexaenoic, and 20:5n-3, eicosapentaenoic), and a monounsaturated FA (16:1n-7, palmitoleic). In the gonads of the fish sampled in Konyukhov Inlet, the highest level of reserve triacylglycerols and palmitoleic acid was registered; this can positively affect the body weight and viability of the coming embryos. The increased content of physiologically significant n-3 polyenic FA (22:6n-3 and 20:5n-3) in the gonads of the stickleback females at this stage of the reproductive cycle may be associated with increased need for these acids by the coming embryos.

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... The three-spined stickleback, Gasterosteus aculeatus, is widely distributed throughout the mid-latitude Northern Hemisphere. Various aspects of the evolution, ecology, and behavior of this fish are discussed in numerous articles [9,13,15,17,36], reviews [11,24,26,27], and books [45,46]. G. aculeatus forms both marine [17,27] and freshwater populations [1,25,30]. ...
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... Studies of the threespine stickleback inhabiting the White Sea, on the one hand, evidenced a significant heterogeneity in the content of various lipids and fatty acids in fish from different habitats at different stages of the spawning period, which might indicate significant physiological differences between different specimens due to the fact that they were in different phases of the spawning cycle (Murzina et al., 2017(Murzina et al., , 2018(Murzina et al., , 2019a(Murzina et al., , 2019b of n-3 families) was reported for the threespine stickleback in comparison with most of the other fish species. ...
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Lipid reserves in teleost eggs are stored in lipoprotein yolk and, in some species, a discrete oil globule. Lipoprotein yolk lipids are primarily polar lipids, especially phosphatidylcholine and phosphatidylethanolamine (PE), and are rich in (n-3) polyunsaturated fatty acids, especially 22:6(n-3) (docosahexaenoic acid, DHA). Oil consists of neutral lipids and is rich in monounsaturated fatty acids (MUFA). Egg lipids are derived from dietary fatty acid, fatty acid mobilized from reserves and possibly fatty acid synthesized de novo. There is selective incorporation of essential fatty acids, particularly DHA, into yolk lipids and discrimination against incorporation of 22:1(n-11). Lipid is delivered to the oocyte by vitellogenin, which is rich in polar lipids, and likely also by other lipoproteins, especially very low density lipoprotein, which is rich in triacylglycerol (TAG). All classes of lipid may be used as fuel during embryonic and larval development and MUFA are preferred fatty acids for catabolism by embryos. Catabolism of oil globules is frequently delayed until latter stages of development. In some species, DHA derived from hydrolysis of phospholipid may be conserved by transfer to the neutral lipid. Recent work has expanded knowledge of the role of DHA in membrane structure, especially in neural tissue, and molecular species analysis has indicated that PE containing sn-1 oleic acid is a prime contributor to membrane fluidity. The results of this type of study provide an explanation for the selection pressures that influence yolk lipid composition. Future work ought to expand knowledge of specific roles of individual fatty acids in embryos along with knowledge of the ecological physiology of ovarian recrudescence, environmental influences on vitellogenin and yolk lipid composition, and the control of yolk lipid accumulation and utilization.
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Effects of two weaning diets that differed in phospholipid (PL) classes on growth, survival and deformities of cod larvae and early juveniles were evaluated. Cod larvae were fed rotifers until 21 days post hatch (dph) and then weaning onto dry diet started. One group of larvae were fed a control diet with low levels of phosphatidylcholine (PC), PE and phosphatidylinositol (PI) and the other group of larvae were fed with an experimental diet containing higher levels of PC, PE and PI. Larvae fed with the control diet were significantly smaller than larvae fed with the experimental diet at the end of the experiment. Swim bladder abnormalities were significantly higher in larvae fed with control diet at 35 dph than the larvae fed with experimental diet; however, no significant difference was evident at 42 dph. Vertebral deformities were significantly higher in larvae fed with control diet and scoliosis was significantly different between the treatments. Survival was also significantly higher in the experimental group. Our results indicate that dietary levels of PL, PC and PI may affect the cod larval growth, survival and deformities. More detail studies are needed to find out the optimal levels of these important PL classes in larval cod diets.
Article
In female sea bream Sparus aurata fed a control diet (C), ovarian levels of neutral lipids (NL) and polar lipids (PL) remained constant between November and March, while a decrease in NL content was observed in liver and muscle. In the same period, liver PL content increased, while no changes were observed in muscle. Between March and June ovarian NL and PL showed a strong decrease, while NL remained constant in liver and muscle. When fish were fed a diet lacking in n-3 highly unsaturated fatty acids, n-3 HUFA (D), the pattern observed was similar to that found in the fish fed diet C, with the exception of liver NL, which increased between March and June. In general, the changes in fatty acid content, in both groups of fish, were highly influenced by the diet given to the broodstock, although these effects were greater on ovarian NL and PL than on liver and muscle lipids. Despite the fact that gilthead seabream females continue feeding during the spawning season, they probably make use of their liver and muscle reserves during the gonadal maturation process. Furthermore, the fatty acid composition of the broodstock diet was reflected in the body composition, especially in the ovaries.
Article
Polyunsaturated fatty acids (PUFAs), especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), are currently in demand in the pure form and actively being studied to understand their potential roles in human health. Arachidonic acid, 20:4 (n-6), and DHA, 22:6 (n-3), are important in normal neurodevelopment and visual function. Infants fed formula often have low blood lipid 20:4 (n-6) and 22:6 (n-3). Consumption of fish oils may increase the 20:5 (n-3) (EPA) and 22:6 (n-3) (DHA) in human blood. Some marine fish oils contain higher amounts of arachidonic acid, EPA, and DHA. PUFA contents in different marine fishes and methods for their extraction and fractionation, in terms of fatty acid constituents in the form of methyl esters, are covered in this review. Emphasis is given to the fractionations of EPA and DHA by means of supercritical fluid extractions (SFE). The advantages of SFE compared to conventional methods are discussed in this review. PUFAs are usually extracted at about 10 to 30 MPa and at 40 to 80 °C. SFE is a promising and currently the best technique to extract PUFAs, especially EPA and DHA, from marine and freshwater fish.
Article
Fatty acid (FA) compositions and C/N ratios of 28 marine microalgae from nine taxonomic classes were examined. A combination of several criteria was selected to discriminate taxonomic classes: 16:4 (n-1), 20:5 (n-3), 22:6(n-3), C18 polyunsaturated FA (PUFA), C20)PUFA, C22PUFA, 16:1(n-7)/I6:0, C16FA/C18FA, C16PUFA/ C18PUFA, 18:5(n-3)/18:3(n-3). Results expressed in terms of relative abundance (per cent of total fatty acids) and absolute abundance (ng FA mg C−1 and pg FA cell−1) led to different interpretations concerning the nutritional value of the different species as food for organisms in culture or in the natural environment.
Article
In order to study the biological activity of a micro-algae extract rich in fatty acids, the purification and structural identification of two hexadecadienoic methyl esters (16 : 2) and one hexadecatrienoic methyl ester (16 : 3) were performed. The purification of these molecules was carried out by liquid chromatography using a porous graphitic carbon phase. Determination of the chain length, degree and position of unsaturations was achieved by gas chromatography/electron impact mass spectrometer on dimethyloxazoline derivatives. With regard to the double bonds cis or trans isomery was determined by Fourier transform infrared spectroscopy. Structures were confirmed by 1H and 13C nuclear magnetic resonance.
Article
Oocyte growth and development is an important issue in fish and fisheries biology. This paper reviews the information available on oocyte growth patterns and the rates and dynamics of oocyte growth in teleosts. In synchronous spawners, the weight of the gonad may represent as much as 40% of the overall body weight of the fish. In asynchronous spawners, the weight of the mature ovary is considerably less than in synchronous ovulators, but the ovary shows a more regular periodicity and may grow repeatedly many times during the breeding season. There is a huge variability in egg size in teleosts, with the largest known measuring up to 8 cm in diameter. Within the limits of variance set by genetic constraints, egg size may vary between populations of the same species. Oocytes in all teleosts undergo the same basic pattern of growth: oogenesis, primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation and ovulation. The mechanisms that control oocyte growth are addressed in this review, albeit that the available information, as in all other vertebrates, is very limited. The main hormones that have been shown to affect ovarian growth are gonadotrophin, thyroid hormones, growth hormone, insulin and insulin-like growth factors. An overview of the determinants of fecundity, with particular reference to oocyte recruitment and atresia, is the focus of the second part of the paper. Genetics and nutrition have major effects on fecundity, and studies so far suggest that the determinants of fecundity usually operate during the early part of gametogenesis. The role of atresia in determining fecundity is less clear. The final part of this review highlights some areas of study that are priorities for research on ovarian development in fish.
Article
Lipid reserves in teleost eggs are stored in lipoprotein yolk and, in some species, a discrete oil globule. Lipoprotein yolk lipids are primarily polar lipids, especially phosphatidylcholine and phosphatidylethanolamine (PE), and are rich in (n–3) polyunsaturated fatty acids, especially 22:6(n–3) (docosahexaenoic acid, DHA). Oil consists of neutral lipids and is rich in monounsaturated fatty acids (MUFA). Egg lipids are derived from dietary fatty acid, fatty acid mobilized from reserves and possibly fatty acid synthesized de novo. There is selective incorporation of essential fatty acids, particularly DHA, into yolk lipids and discrimination against incorporation of 22:1(n–11). Lipid is delivered to the oocyte by vitellogenin, which is rich in polar lipids, and likely also by other lipoproteins, especially very low density lipoprotein, which is rich in triacylglycerol (TAG). All classes of lipid may be used as fuel during embryonic and larval development and MUFA are preferred fatty acids for catabolism by embryos. Catabolism of oil globules is frequently delayed until latter stages of development. In some species, DHA derived from hydrolysis of phospholipid may be conserved by transfer to the neutral lipid. Recent work has expanded knowledge of the role of DHA in membrane structure, especially in neural tissue, and molecular species analysis has indicated that PE containing sn-1 oleic acid is a prime contributor to membrane fluidity. The results of this type of study provide an explanation for the selection pressures that influence yolk lipid composition. Future work ought to expand knowledge of specific roles of individual fatty acids in embryos along with knowledge of the ecological physiology of ovarian recrudescence, environmental influences on vitellogenin and yolk lipid composition, and the control of yolk lipid accumulation and utilization.
Article
In juveniles of Atlantic salmon Salmo salar of two age groups (0+ and 1+) living in the mainstream and in the tributary of the subarctic Varzuga River, the activity of some enzymes was determined (cytochrome c oxidase, malate dehydrogenase, lactate dehydrogenase, glucose-6-phosphate dehydrogenase, and 1-glycerophosphate dehydrogenase), reflecting the intensity of the direction of principal pathways of carbohydrate metabolism and of synthesis of ATP. The effect of environmental conditions on growth and development of different age groups is different. Underyearlings (0+) living in the tributary are characterized by an advanced locomotor performance and growth rate. They possess a higher level of aerobic and anaerobic energy metabolism and assimilation of carbohydrates for synthesis of structural and stock compounds in comparison with yearlings living in the mainstream. No significant differences are found between two-summer-old fish (1+) from different habitats in parameters of energy metabolism. This demonstrates that the living conditions for them in the tributary are not so favorable as from underyearlings. The food items in the tributary are small and numerous, i.e., are more available for salmon underyearlings. Parrs 1+ feed on large invertebrates and feeding in the mainstream is preferable. The differences in parameters of energy metabolism of juvenile salmon manifesting themselves in the first year of life make the basis for the fact that the subsequent smoltification of parrs and migration for feeding occur at different ages—2+, 3+, or 4+. This contributes to the formation of the complex age structure of the Varzuga stock of salmon.
Article
The present work reviews the significance of lipids at different early stages of marine fish larvae. Lipids in broodstock nutrition are considered to be important for the quality of the larvae. Lipids affect the spawning and the egg quality of many fish species and a deficiency in (n−3) highly unsaturated fatty acids (HUFA) in broodstock negatively affects fecundity, fertilization rate and hatching rate of the species studied. Lipids as a source of energy at the embryonic and larval stage (before first-feeding) are evaluated in relation to other sources of energy such as protein and carbohydrates. After hatching and prior to first-feeding, some marine species show a preference in catabolizing phosphatidylcholine, whereas phosphatidylethanolamine tends to be synthesized. The effect of long-term (LT) and short-term (ST) enrichment techniques on the lipid composition of rotifers has been documented using various marine oils/emulsions. The quantitative and qualitative lipid class and fatty acid composition of diets influenced the lipid and fatty acid composition of both LT- or ST-enriched rotifers. The nutritional improvement of Artemia is also important and may follow the general methods used for rotifers. The functions of docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) during early stages of marine fish larvae are apparently different. High amounts of EPA in relation to DHA may create an imbalance in the structural composition of the phospholipids, which could affect the normal growth and the quality of the larvae. Turbot larvae tended to exhibit lower pigmentation success with lower DHA:EPA ratio in the total lipid fraction of the larvae, especially when the absolute amounts of EPA were high compared to those of DHA (in the total lipid and phospholipid fraction of the larvae). Considerable research is necessary to clarify many aspects regarding the function of these fatty acids, especially how their content at the egg stage can affect further requirements for normal growth and survival.
Article
When cholesterol, dissolved in acetic acid, is mixed with premixed ferric chloride reagent and heated at 50°C for 15 min, a bright pink colour forms which is stable for 1 hr. The reagent contains acetic acid, sulphuric acid, ferric chloride and phosphoric acid, and is stable for years. Sterols extracted from saponified serum by petroleum ether produce an absorbance directly proportional to the cholesterol present. When whole serum is dissolved in acetic acid and treated with the reagent, the absorbance of the solution is equal to the sum of the absorbance due to cholesterol plus an amount due to other serum components which is constant in healthy persons. By using two reference sera to set up the linear standard curve of absorbance versus cholesterol concentration, a rapid precise method for serum cholesterol is obtained, applicable to healthy persons. The results of this direct method were well in agreement with those from established methods.
Article
Linoleic and alpha-linolenic acid are essential for normal cellular function, and act as precursors for the synthesis of longer chained polyunsaturated fatty acids (PUFAs) such as arachidonic (AA), eicosapentaenoic (EPA) and docosahexaenoic acids (DHA), which have been shown to partake in numerous cellular functions affecting membrane fluidity, membrane enzyme activities and eicosanoid synthesis. The brain is particularly rich in PUFAs such as DHA, and changes in tissue membrane composition of these PUFAs reflect that of the dietary source. The decline in structural and functional integrity of this tissue appears to correlate with loss in membrane DHA concentrations. Arachidonic acid, also predominant in this tissue, is a major precursor for the synthesis of eicosanoids, that serve as intracellular or extracellular signals. With aging comes a likely increase in reactive oxygen species and hence a concomitant decline in membrane PUFA concentrations, and with it, cognitive impairment. Neurodegenerative disorders such as Parkinson's and Alzheimer's disease also appear to exhibit membrane loss of PUFAs. Thus it may be that an optimal diet with a balance of n-6 and n-3 fatty acids may help to delay their onset or reduce the insult to brain functions which these diseases elicit.
Article
A method for detailed quantitative analysis of barley and malt lipids was developed. Extractable lipids were fractionated into four broad classes of compounds: phospholipids, mono- and diglycerides, triglycerids and hydrocarbons. The hydroxamic acid colorimetric test for ester groups was modified to quantitatively measure lipids that contained ester groups and the dichromic acid test for organic compounds was modified to quantitatively measure lipids, such as hydrocarbons, which contained no ester group. Standard curves were prepared for the four lipid fractions by the use of a thick-layer preparative procedure. Each lipid fraction can be analyzed for fatty acid composition by a thin-layer chromatographic method which separates fatty acids in the form of saturated fatty acid methyl esters and mercuric acetate adducts of unsaturated fatty acid methyl ester. The method gave quantitative results for both fatty acid analysis and lipid fraction analysis.
Article
The relation between n-3 polyunsaturated fatty acid (PUFA) and nonfatal myocardial infarction is still controversial. A multicenter case-control pilot study on n-3 PUFA as a negative risk factor for myocardial infarction was performed in Niigata prefecture. Seventy-three patients with acute myocardial infarction (AMI) and age and gender matched controls (n = 84) were recruited. Serum leptin levels were significantly higher in patients with AMI than the controls (8.1 +/- 6.7 ng/mL versus 5.8 +/- 3.7 ng/mL, P < 0.01), and serum high-density lipoprotein cholesterol (HDLc) levels were significantly lower in patients with AMI than the controls (46 +/- 10.5 mg/dL versus 60 +/- 15 mg/dL, P < 0.00001). Statistically significant differences were preserved in leptin and HDLc when the data were analyzed separately by gender. Serum levels (%weight) of linolenic acid (C18:3:n3), eicosapentaenoic acid (C20:5:n3), docosapentaenoic acid (C22:5:n3), and total n-3 PUFA were significantly lower in patients with AMI than the control group (P < 0.000001, < 0.05, < 0.05, < 0.05, respectively). The serum n-3 PUFA/saturated fatty acid (SF) ratio and n-3 PUFA/n-9 monounsaturated fatty acid (MUFA) ratio were significantly lower in patients with AMI than the controls (P < 0.05 and < 0.01, respectively). When the subjects were separated into two categories according to an n-3/n-6 PUFA ratio below 0.3 or above 0.3, patients with AMI were more frequently in the former while the controls were more frequently in the latter (P < 0.05). N-3 PUFA may be a negative risk factor for AMI. The results suggest leptin is a risk factor for AMI irrespective of ethnicity and gender.
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