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Background: The broodstock diet, and in particular the lipid and fatty acid composition of the diet, is known to play a key role in reproductive efficiency and survival of the progeny in fish. A major problem when replacing both fish meal and fish oil by plant sources is the lack of n-3 long chain polyunsaturated fatty acids, such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). To address this problem, we studied the effect of the plant-based diet supplemented with Schizochytrium sp. microalgae, source of DHA, compared to a conventional commercial diet rich in fish meal and fish oil on reproductive performance and egg quality and the consequences on progeny, in female rainbow trout broodstock. Results: The results demonstrated that DHA-rich microalgae supplementation in a plant-based diet allowed for the maintenance of reproductive performance and egg quality comparable to a conventional commercial feed rich in fish meal and fish oil and led to an increased significant fry survival after resorption. Moreover, when females were fed a plant-based diet supplemented with micro-algae, the 4-month-old progenies showed a significant higher growth when they were challenged with a similar diet as broodstock during 1 month. We provide evidence for metabolic programming in which the maternal dietary induced significant protracted effects on lipid metabolism of progeny. Conclusions: The present study demonstrates that supplementation of a plant-based diet with DHA-rich microalgae can be an effective alternative to fish meal and fish oil in rainbow trout broodstock aquafeed. Keywords: Egg quality, Micro-algae, Nutritional programming, Plant diet, Rainbow trout, Reproduction * Correspondence: firstname.lastname@example.org INRAE, Univ. Pau & Pays Adour, E2S UPPA, NuMéA, F-64310, Saint Pée-sur-Nivelle, France INRAE, UR1037 Fish Physiology and Genomic laboratory, F-35000 Rennes, France Full list of author information is available at the end of the article © The Author(s). 2022 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 2 of 18 Introduction [15, 16]. One of the main challenges facing researchers Due to the increasing demand for fish and shellfish, today is to find a solution to this lack of essential fatty aquaculture is playing an increasingly important role in acids in the plant-based diet, particularly for broodstock. providing an important source of protein for people. In Microalgae (i.e. single-celled algae or phytoplankton) the last 30 years, the increase in aquaculture production are considered a promising alternative as replacements has forced a change in fish feed composition, whereby for FM and FO, and also help to ensure sustainability fishmeal (FM) and fish oil (FO) have been increasingly standards in aquaculture. Known as sources of protein, replaced by more available plant sources. Between 1990 lipid, vitamins, minerals or pigments, microalgae may and 2018, for example, FM and FO inclusion rates in the also be a source of n-3 LC-PUFAs . The marine diets of Atlantic salmon in Norway declined from 65% microalgae Schizochytrium sp., for example, contains be- to 13% and 24% to 10%, respectively . Despite the fact tween 18% and 22% DHA of their dry matter . Sup- that FM and FO inclusion rates in aquafeeds have shown plementation of aquafeed with this microalgae improved a clear downward trend over the last decades , their the levels of DHA and total n-3 LC-PUFAs in the fillet total replacement by plant sources is still not optimal as tissue in channel catfish  and in Nile Tilapia  but it leads to reduced feed efficiency, growth and repro- until now, this supplementation has yet to be investi- ductive performances [3, 4]. gated within rainbow trout broodstock. Carnivorous fish species, such as salmonids, are among Moreover, changes in the diet of the broodstock are the highest consumers of FO and FM . Among salmo- not without consequences for the offspring. Many au- nids, rainbow trout (Oncorhynchus mykiss) farming rep- thors have shown the importance of the maternal envir- resented a world production of 811 thousand tons in onment on the development of the offspring in 2017 . It is the main freshwater production in Europe vertebrates , including fish [13, 22]. The maternal (over 150,000 t produced by 14 countries in 2017) and environment, including nutrition, can influence embry- intense research efforts are currently focused on re- onic and fetal life and thus modify the trajectory of the placing marine ingredients (FM and FO) with more offspring’s development . In aquaculture, the readily available plant-based ingredients in their diets phenomenon of nutritional programming was previously [6–11]. tested to improve the acceptance of a plant-based diet in In the broodstock diet, especially for rainbow trout, rainbow trout [13, 14, 24]. Currently, research on nutri- the problem of FM and FO replacement is accentuated. tional programming is primarily focused on program- For successful reproduction, the protein and lipid re- ming juveniles through early nutritional stimuli, at first quirements for broodstock are important and highly spe- feeding [25–32], but research on the maternal role in cific. Several studies revealed that the replacement of FO progeny programming is still in its infancy [13, 14, 33]. and/or FM with plant products in broodstock diet alters Two studies on gilthead seabream [13, 14] demonstrated broodstock reproductive performances in rainbow trout that it is possible to nutritionally program offspring by [3, 12] and in other fish species [13, 14]. Two long-term replacing fish oil with vegetable oils in the broodstock studies (3 years) evaluated the effect of replacing only diet, resulting in an improvement in their ability to grow FM or both FO and FM with plant products on the re- fast when fed low fish meal and fish oil diets during the productive performance of female rainbow trout [3, 12]. grow-out phase. Lee et al.  investigated the long-term effects of re- In the present study, we compared the effects of a placement of FM by dietary cottonseed meal on growth plant-based diet supplemented with Schizochytrium sp. and reproductive performance of rainbow trout and micro-algae with those of a commercial diet, on repro- showed an important decrease in the survival of individ- ductive performances and egg quality of female rainbow uals at the eyed-stage. While Lazzarotto et al.  showed trout (Oncorhynchus mykiss). We also studied the conse- that, despite total replacement of FO and FM by plant quences of maternal nutritional history on offspring to products, rainbow trout can successfully produce ova in assess the implementation of nutritional programming. which neo-synthesized long chain polyunsaturated fatty acids (LC-PUFAs) accumulate, the reproductive per- Material and methods formance and egg quality remain negatively impacted by Ethical statements these total replacements notably by reducing egg size Broodstock experimentation was conducted in the and survival of the offspring. A major issue when re- Viviers de Rébénacq commercial fish farm (Rébénacq, placing both FM and FO by plant sources is the lack of France) and egg incubation and fingerling rearing were n-3 LC-PUFAs, such as eicosapentaenoic acid (EPA) and conducted in the Viviers de Sarrance commercial fish docosahexaenoic acid (DHA). These fatty acids are im- farm (Sarrance, France). All fish were reared and han- portant in the fish life-cycle, most notably for their roles dled in strict accordance with French and European pol- in reproduction, egg quality and offspring development icies and guidelines. Fish were monitored daily during Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 3 of 18 the experiment. If any clinical symptoms (i.e. morpho- Table 1 Ingredients (only for MAB diet) and composition of female broodstock diets logical abnormalities, restlessness or uncoordinated movements) were observed, fish were sedated by Ingredients, % MAB CB immersion in MS-222 solution at a concentration of 50 Schizochytrium sp. microalgae biomass 6.9 mg/L and then euthanized by immersion in a MS-222 Corn gluten 19.7 solution at a concentration of 400 mg/L (anesthetic over- Soybean meal 14.5 dose) for 5 min. Pea protein concentrate (Lysamine) 15.0 Soy protein concentrate 9.6 Broodstock diet and challenge diet of progeny Bean protein concentrate 9.0 The broodstock experiment was conducted with two dif- Guar 70 PFR Roasted 9.0 ferent diets: a commercial broodstock diet (Neo repro, Alfalfa protein concentrate 5.0 Le Gouessant, Lamballe, Côte d’Armor, Brittany, France) Rapeseed oil 3.2 containing a mix of FM, FO and plant ingredients (CB), and a plant-based diet completely devoid of FM and FO Linseed oil 1.1 but supplemented with Schizochytrium sp. microalgae Choline chloride 60% 0.3 biomass (MAB). Soy lecithin 1.0 The plant-based diet supplemented with microalgae Minerals premix 1.6 biomass was formulated by INRAE to fulfill the nutri- Vitamin premix 1.5 tional requirements of rainbow trout . The two diets Dicalcium phosphate 1.2 were produced by the feed company “Le Gouessant” (Lamballe, Côte d’Armor, Brittany, France). Ingredients L-Lysine 0.8 of the MAB diet are presented in Table 1. L-Méthionine 0.5 The diet used to challenge the progeny was similar to Carophyll pink (astaxanthin) 0.04 the plant-based diet supplemented with Schizochytrium Proximate composition sp. microalgae used for broodstock (vegetable diet) but Dry Matter, % 91.7 92.6 modified to respond to the specific needs of juveniles Proteins, % DM 54.1 49.5 (MAO diet). Micro-algae biomass was replaced by micro-algae oil due to a supply problem concerning Lipids, % DM 12.1 15.2 micro-algae biomass during the production of the ex- Carbohydrate, % DM 11.5 15.3 perimental diet (Table 2). The ingredients list of the Ash, % DM 5.2 12.2 commercial diet (CO, Neo supra, Le Gouessant, Lam- Energy, kJ/g DM 23.3 22.2 balle, Côte d’Armor, Brittany, France) fed to progeny Cholesterol, mg/100 mg of DM 24.9 177.6 cannot be published because of the confidentiality agree- Phytosterol, mg/100 mg of DM 180.5 53.7 ment with the feed manufacturer but the proximate composition is available (Table 2). The fatty acid profile DM = dry matter. for the progeny diets is presented in Additional file 1: Table S1. The feeding rate used in the experimental design was established according to a conventional feeding table Broodstock breeding and experimental design provided by the feed manufacturer (Le Gouessant, Lam- Before any manipulation, fish were fasted for 24 h and balle, Côte d’Armor, Brittany, France). This table was anesthetized with MS-222 (50 mg/L). Female rainbow calculated according to fish weight and water trout from an autumn-spawning strain were held under temperature. natural photoperiod until their first reproduction (2 Two reproductive cycles were followed during this years) in the Viviers de Rebenacq fish farm. After the trial. For more fluidity, the cycle between the first and first spawning, each fish was individually weighed and the second reproduction period and between the second identified with a RFID Pit-tag (Biolog-id, Bernay, France). and the third reproduction period will be referred to as A total of 180 females, with a biomass of 25 kg/m (initial Cycle 2 (from week 0 to week 39) and Cycle 3 (from weight: 2227 ± 268 g), were then randomly transferred week 40 to week 80), respectively. It should be noted into 4 outdoor tanks with a volume ranging from that after the spawning period of Cycle 2, some fish were 3.5 to 4.5 m (n = 90 females per treatment). Each randomly eliminated to ensure that the second cycle diet was assigned to two tanks. Females were fed the started with an initial fish biomass of 25 kg/m . experimental diets after the first reproduction and During these two nine-month cycles, an artificial continued until the third reproduction. photoperiod regime was applied to trigger a second Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 4 of 18 Table 2 Ingredients (only for MAO diet) and composition of first ovulation was detected. Ovulating females were progeny diets weighed and manually stripped. The ovarian fluid and Ingredients, % MAO CO eggs produced by each female were weighed and eggs were sampled during the second and third reproduction Schizochytrium sp. microalgae oil 2.6 periods. Corn gluten 18.0 During Cycle 3, egg batches from 10 females by treat- Soybean meal 5.1 ment randomly selected at the peak of spawning were Pea protein concentrate 20.5 transferred to Viviers de Sarrance facilities. Approxi- Soy protein concentrate 23.6 mately 400 eggs from each batch were individually fertil- Bean protein concentrate 4.0 ized with a pool of sperm collected from neo-males from the fish farm that were fed a commercial diet ad Guar 70 PFR Roasted 2.0 libitum. Three microliters of a pool of semen obtained Alfalfa protein concentrate 5.0 from three neo-males presenting the highest sperm mo- Rapeseed oil 9.2 tility were pre-diluted in storFish solution (IMV tech- Linseed oil 2.0 nologies, L’Aigle, France) and added to each group of Choline chloride 60% 0.3 eggs. Fifteen mL of Actifish solution (sperm motility ac- Soy lecithin 2.5 tivating saline solution, IMV technologies, L’Aigle, France) were added to the eggs. Five min later, the Minerals premix 1.5 sperm motility activating solution was drained and egg Vitamin premix 1.2 batches were transferred into individual incubators in Dicalcium phosphate 1.2 recirculated water units. The temperature of the water L-Lysine 0.6 remained constant (9 °C) throughout the incubation L-Methionine 0.6 period. Dead eggs and embryos were periodically manu- Proximate composition ally counted and removed. Survival at completion of yolk-sac resorption were monitored and calculated as a Dry Matter, % 97.2 92.1 percentage of the initial number of eggs used for the Proteins, % DM 56.9 52.0 fertilization. The occurrence of noticeable morphological Lipids, % DM 23.3 17.3 malformations (spinal cord torsion, head or caudal fin Ash, % DM 6.0 10.4 malformations, etc.) at yolk-sac resorption was also Energy, kJ/g DM 25.7 19.2 recorded. Cholesterol, mg/100 mg of DM 38.6 301.1 Growth trial and nutritional challenge on progeny Phytosterol, mg/100 mg of DM 268.0 5.4 After resorption of the yolk vesicle, pools of fry were DM = dry matter. generated according to the maternal nutritional history. reproduction during summer, and a third reproduction Then, fingerlings were transferred in racks with well- during spring. The water renewal rate was 200% per aerated water at 16 ± 2 °C, under natural photoperiod. hour. Fish are reared in outdoor tank with a water turn- During this growth period, duplicate groups were manu- over of 200%. Temperature was checked twice a day to ally fed a commercial diet (Le Gouessant, neo supra, adjust feeding rate. During experiment, temperature Lamballe, Côte d’Armor, Brittany, France), fish were fed fluctuated with the season (from 8 °C to 13 °C). In order 4 times per day until first feed refusal (n = 2 racks per to monitor individual growth and to adjust the distribu- treatment). After 4 weeks of trial, groups were divided tion of feed, fish were individually weighed every 6 into two to decrease density and kept for the following weeks during Cycle 2 and at different stages of the re- trial (n = 4 ranks per treatment). The feed grain size was productive cycle during Cycle 3 (see paragraph Sampling adapted to the size of the fry. Biomass of each tank was for more details). During Cycle 3, at the same time as weighed every 2 weeks to monitor growth. After 4 and 8 the fish were weighed, blood samplings were performed weeks of trial, fish were counted and weighed to calcu- after fish were sedated with MS-222 (50 mg/L). late percent survival (n = 2 at week 4; n = 4 at week 8). The experimental design is summarized in Fig. 1. After 8 weeks of trial, fish were weighed to calculate in- dividual body weights (n = 30). Reproduction, fertilization and incubation After 8 weeks of trial, all groups were adjusted to in- During the spawning season, females were anesthetized clude 150 fingerlings per rack. To determine the effect with MS-222 (50 mg/L) and checked for ovulation once of the maternal nutritional history on the ability of the a week by applying manual pressure on the abdomen of progeny to use a plant-based diet, half of the fish were the fish. Feeding was stopped for all animals when the challenged with the MAO diet for a period of 4 weeks Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 5 of 18 Fig. 1 Experimental design (W=Week of rearing) whereas the other half continued to be fed the commer- Progeny cial diet (CO). Fish were manually fed 4 times per day. At the end of the nutritional challenge (12 weeks), sam- At the end of nutritional challenge, all fish were counted pled fish were sedated by immersion in an iso-eugenol to calculate percent survival rate and 30 fish per condi- solution at a concentration of 20 mg/L and euthanized tion were weighed individually. by immersion in an iso-eugenol solution at a concentra- The goal of this study was to compare the maternal ef- tion of 100 mg/L (anesthetic overdose) for 3 min. Liver fect on progeny, and the effect of the diet supplied to (ten fish per condition) were dissected, immediately fro- the offspring will not be discussed here. zen in liquid nitrogen and stored at − 80 °C until further molecular analysis. Twenty fish were sampled for prox- Sampling imal composition and fatty acid profile analysis, and Female broodstock stored at − 20 °C until further analysis. During Cycle 3 of the experiment (week 40 to week 80), blood sampling was performed at different times (Fig. 1): Plasma cholesterol analysis at week 40 (just after the reproduction period of Cycle Cholesterol levels were measured from the plasma of fe- 2), 52 (before the change of photoperiod, i.e. early vitel- males whose eggs were used to produce fingerlings for logenesis), 58 (i.e. mid vitellogenesis), 68 (i.e. last step of the nutritional challenge (n = 10 per treatment) during vitellogenesis) and during spawning season (week 75). Cycle 3. Plasma cholesterol level was determined using Blood samples were collected from the caudal vein commercial kits adapted to a microplate format, accord- (approximatively 4 mL per fish) using EDTA-treated sy- ing to manufacturer recommendations (Sobioda, ringes (sodium EDTA, 10%). Blood samples were centri- Montbonnot-Saint-Martin, France). fuged (3500 × g, 15 min) and plasma was collected, frozen in liquid nitrogen and stored at − 80 °C until fur- Automatic egg size, number and integrity analysis ther analysis. Eggs (approximatively 30 g per fish) were Stripped unfertilized eggs (approximatively 400 eggs, sampled during spawning for each reproductive cycle about 25 to 30 g) were placed in 150 mL containers and and frozen at − 20 °C until further biochemical analysis. water was added to hydrate the eggs. After 24 h of Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 6 of 18 hydration, a picture of the sampled eggs was obtained comparing their retention times with a known standard mix- using the VisEGG shooting system consisting of a light ture (Sigma, St Louis, MO, USA) and peaks were integrated tablet and digital SLR camera (canon EOS 1000D, reso- using Varian Star Chromatography Software (Star Software, lution: 10.1 M pixels) equipment, as previously described version 5). The results for individual FA were expressed as . Pictures were analyzed with Visilog 7.3 software percentage of total identified FA methyl esters. (Thermo Scientific) allowing for automatic measurements to be made (number and size of the eggs and white egg Molecular analysis on progenies percentage). The total number of ovulated eggs per female RNA extractions were carried out on individual liver could be back calculated using the number of eggs mea- samples for 10 fry per condition. Livers were homoge- sured and the total weight of the egg batch analyzed. The nized in trizol reagent (Ambion) at a ratio of 1 mL for presence of white egg was interpreted as an indirect meas- 100 mg of tissue with precyllis®24 (Bertin Technologies) ure of egg integrity, the “whitening” being the result of and total RNA was extracted according to manufac- water entry into the egg and through the vitelline mem- turer’s instructions. The quantity and quality of RNA brane . These white eggs were considered non-viable were assessed by measuring their absorbance at 260 and due to their lack of physical integrity. 280 nm using a Nanodrop 1000 Spectrophotometer The total number of ovulated eggs per female correspond (Thermo Scientific) associated with ND-1000 V3 7.0 to the individual absolute fecundity. Individual fecundity software. Gene expression was assessed as follows: 1 μg was divided by the weight of the fish to give the value for of total RNA was subsequently reverse-transcribed to relative fecundity in number of eggs/kg of female. cDNA using the super script RNAse H-reverse tran- scriptase kit (Invitrogen) with random primers (Pro- Diet and fish proximate composition analysis mega, Charbonnières, France). Luciferase control RNA Proximate composition of the diets and biochemical com- (Promega) was added to each sample at the beginning of position of the progenies were determined according to reverse transcriptase. The levels of messenger RNAs the following procedures: dry matter after drying at 105 °C (mRNA) (including paralogs for some of them) were for 24 h, protein (N × 6.25) by the Kjeldahl method after measured in the liver of progenies at the end of the growth acid digestion, ash by incineration at 550 °C for 16 h and period (fed the C diet) and after the 4-week nutritional gross energy in an adiabatic bomb calorimeter. Total lipids challenge. Genes subjected to RT-PCR analysis were related were extracted using dichloromethane/methanol (2:1, v/ to lipogenesis (ATP cytrate lyase (ACLY)and fattyacidsyn- v), containing 0.01% butylated hydroxytoluene (BHT) as thase (FAS)), β-oxidation of long-chain fatty acids (carnitine an antioxidant, according to Folch et al. . palmitoyl transferase 1 (CPT1a), hydroxyacylcoA dehydro- Dietary levels of cholesterol and phytosterol were de- genase (HADH) and acylcoA oxidase (ACOX)), long-chain termined by gas chromatography according to the norm fatty acid biosynthesis (acyl-CoA desaturase - delta-9 desa- NF EN ISO 12228-1 . turase (SCDB), elongation of very long chain fatty acids proteins 2 (ELOVL2b)and 5(ELOVL5a, ELOVL5c) and Lipid and fatty acid analysis fatty acid desaturase 2 (FADS2a, FADS2b and FADS2c)) Diets and eggs (10 eggs batches per treatment) from and cholesterol metabolism (3-hydroxy-3-methylglutaryl- each cycle of reproduction were analyzed for lipids and CoA synthase 1 (HMGCS), 3-hydroxy-3-methylglutaryl- fatty acid composition. Egg samples were of the same CoA reductase (HMGCRa, HMGCRb),cholesterol 7alpha origin as the eggs used for monitoring fertilization and incu- hydroxylase a (CYP7a) lanosterol 14-alpha demethylase bation. Total lipids were extracted by dichloromethane/ (CYP51a, CYP51b), ATP-binding cassette sub-family A methanol (2:1, v/v), containing 0.01% of butylated hydroxy- member 1-like (ABCA1), ATP binding cassette subfamily G toluene (BHT) as antioxidant, according to Folch et al. . member 5 and 8 (ABCG5, ABCG8) and 7- Fatty acid methyl esters (FAME) were prepared by acid- dehydrocholesterol reductase (DHCR7a and DHCR7b). catalyzed transmethylation, using boron trifluoride according Quantitative RT-PCR analyses were performed with to Shantha et al. . Fatty acid methyl esters were analyzed the Roche Lightcycler 480 system (Roche Diagnostics, with a Varian 3900 gas chromatograph equipped with a Neuilly-sur-Seine, France). The reaction mix was 6 μL fused silica DB Wax capillary column (30 m × 0.25 mm in- per sample, including 2 μL of diluted cDNA template (1: ternal diameter, film thickness 0.25 μm; JW Alltech, France). 25), 0.12 μL of each primer (10 μmol/L), 3 μL of Light Injection volume was 1 μL, using helium as carrier gas (1 Cycler 480 SYBR® Green I Master mix and 0.76 μLof mL/min). The temperatures of the injector and the flame DNAse/RNAse-free water (5 Prime GmbH, Hamburg, ionization detector were 260 °C and 250 °C, respectively. The Germany). The qPCR protocol was initiated at 95 °C for thermal gradient was as follows: 100–180 °C at 8 °C/min, 10 min for the initial denaturation of the cDNA and hot- 180–220 °C at 4 °C/min and a constant temperature of start Taq-polymerase activation, followed by 40 cycles of 220 °C for 20 min. The fatty acids (FAs) were identified by a two-step amplification program (15 s at 95 °C; 10 s at Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 7 of 18 60 °C). Melting curves were monitored systematically (from W68). MAB-fed females presented significant (temperature gradient 0.11 °C/s from 65 to 97 °C) at the lower body weights (− 5.4%) at the end of the trial. end of the last amplification cycle to confirm the specifi- city of the amplification reaction. Each qPCR assay in- Plasma cholesterol analysis cluded replicate samples and negative controls (reverse The evolution of cholesterol level in plasma during re- transcriptase- and cDNA template-free samples). Data productive Cycle 3 (W40 to W68) and spawning period were subsequently normalized to the exogenous lucifer- (W75) are presented in Fig. 3. Cholesterol concentration ase transcript abundance. Sequences of primers are pre- was significantly affected during the week of rearing, i.e. sented in Additional file 2: Table S2. by the stage of vitellogenesis (n= 10 females per treat- ment; P < 0.001). The level was relatively high after Statistical analysis spawning during Cycle 2, then gradually decreased to Results are expressed as means and standard deviations. W58 and increased again until spawning during Cycle 3. A statistical analysis of the data was carried out using R Cholesterol levels are significantly higher in the plasma studio software (version 4.0). A two-way ANOVA was of CB-fed females throughout the reproductive cycle performed to assess the effect of dietary treatment and than in MAB-fed females (P < 0.001). cycle of reproduction for reproductive performance pa- rameters, egg quality as well as for molecular and bio- Reproductive performance in females, and egg and progeny chemical results on eggs and progeny. A one-way qualities ANOVA was performed to assess the maternal origin Data on reproductive performances as well as egg and and diet on progeny individual weight. A Kruskal-Wallis fingerlings qualities are reported in Table 3. test was carried out to assess the effect of maternal nu- At each reproductive cycle, the absolute and relative tritional origin on survival percent of broodstock and on fecundity as well as the spawn egg weight were similar survival percent, evolution of weight means during rear- between the two dietary conditions. In terms of egg ing and proximate composition of progeny. quality, a significant interaction between the diet and the The adequacy of the final ANOVA results was reproductive cycle was observed on a percentage of non- assessed by making residual plots to check the normal- viable eggs (i.e. white eggs) and the egg diameter. There- ity. This analysis did not reveal abnormalities, and thus fore, during the reproduction of Cycle 3, MAB diet led the analysis was validated. When an interaction was to smaller eggs (4.64 mm vs. 4.90 mm, respectively for found to be significant, the means for all treatments eggs from MAB-fed females or CB-fed females) but re- were compared using a Tukey’s post hoc analysis. sulted in fewer non-viable eggs (i.e. higher egg integrity; Growth monitoring analyses of broodstock and plasma 2.9% vs. 8.9% respectively for eggs from MAB-fed female cholesterol analyses were performed on the same ani- sand CB-fed females). Diet had no impact on egg size mals during different sample times and analyses can be variability. considered as dependent. Thus, in this case, the data Fry survival after resorption was significantly higher followed a normal distribution and a linear mixed model for eggs originating from MAB-fed females compared to was applied (package LME4 with R studio software). The those from CB-fed females (70.3% vs. 47.6% for fry from adequacy of the final linear model was assessed by mak- females fed the MAB diet compared to the CB diet; n= ing residual plots to check the normality. This analysis 10 eggs batches per treatment P = 0.02). No maternal ef- did not reveal abnormalities, and thus the analysis was fect was observed on the malformation rate and fry validated. As no significant rearing tank effect was ob- weight at yolk-sac resorption. served, we were thus able to only consider feeding pro- cedure as variable factor. Lipid composition and fatty acid (FA) profile of broodstock diet and eggs Results The proximal composition and the FA profiles of the di- Female ets are presented in Table 1 and Table 4, respectively. Biometric parameters of females The CB diet presented a higher level of lipids, including No difference in percent survival was detected between seven times more cholesterol, and a higher level of treatments for female broodstock (i.e. percent survival starch. Inversely, the MAB diet presented a higher level was above 90% for both Cycle 2 and Cycle 3) (see Table of phytosterols (3.4 more than the CB diet). Dietary FA 1). The evolution of female weights is presented in Fig. 2. profiles showed differences between the two diets. One Compared to the CB diet, the MAB diet significantly re- of the largest differences, was attributed to monounsatu- duced the growth of females (n= 90 females per treat- rated fatty acid (MUFA), specifically the 16:1 fatty acid, ment; P < 0.0001). Tukey’s post hoc analysis revealed that was present in very small quantities in the MAB that the differences are significant at the end of Cycle 3 diet (0.44%) while its proportion reached 9.21% of total Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 8 of 18 Fig. 2 Evolution of female weight according the diet treatment. The red arrows represent the spawning periods. The measurements were carried out on the same females at different times; data can be considered as dependent. Linear mixed model was applied, the best model was then selected using the Akaike Information Criterion (AIC). Replicates correspond to different individual females (n = 90 per treatment). “n.s”: not significant; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001 FA in the CB diet. Inversely, the 18:1 fatty acid repre- 1 and EPA were observed in eggs from MAB-fed females sented 24.4% of total FA in the MAB diet whereas it compared to eggs from CB-fed females. accounted for only 14.5% of the total fatty acids in the Interestingly, although the proportion of EPA and DHA CB diet. The MAB diet also presented 2.5 times more n- followed the same trend as in the diet (significantly more 6 PUFA. The difference was essentially due to the higher DHA and less EPA in eggs from MAB-fed females than in proportion of linoleic acid (18:2 n-6; LA) and docosapen- eggs from CB-fed females), the difference observed in the taenoic acid (22:5 n-6; DPA) (2.5 × and 33.9 × higher than eggs was notably less important than in the diets. Eggs from CB diet, respectively). In contrast, arachidonic acid (20:4 MAB-fed females were enriched with EPA although the n-6; ARA) was higher in CB than in the MA diet (4.3 × amount of EPA in the diet was very low. Eggs from CB-fed higher) although its proportion remained lower than 1% females, on the other hand, presented a higher proportion of of the total FA. The proportion of n-3 PUFA was 3.3 times DHA compared to that measured in the diet. Moreover, lower in the MAB diet than in the CB diet. This difference ARA, present in higher quantities in the CB diet compared was mainly explained by the lower proportion of eicosa- to the MAB diet, was found, conversely, in higher quantities pentaenoic acid (20:5 n-3; EPA) since it was 41.9 less con- in eggs from MAB-fed females than those from CB-fed fe- centrated in the MAB diet than in the CB diet. However, males. It should be noted that only a few differences were de- higher proportions of α-linolenic acid (18:3 n-3; ALA) and tected in the FA profile of eggs between Cycle 2 and Cycle 3. docosahexaenoic acid (22:6 n-3; DHA) (8.2 and 2.8-fold, respectively) were present in the MAB diet. Progeny FA egg profiles were very different between the diets (n = Impact of the origin of the maternal diet on progeny 10 eggs batches per treatment) (Table 5). Eggs from MAB- performance fed females presented a higher proportion of n-6 PUFA (2.3 During the growing period where fry were fed a com- to 2.8 × more) but a lower proportion of n-3 PUFA (1.3 × mercial diet (CO; Fig. 4A), maternal origin did not more) than eggs from CB-fed females. A higher proportion affect the percent survival and the individual body of 18:1, LA, DPA, ALA, DHA and a lower proportion of 16: weight of the fingerlings (n = 30 fingerlings per Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 9 of 18 Fig. 3 Evolution of plasma cholesterol concentrations over the vitellogenesis during Cycle 3. Plasma sampling was performed at different times during the reproductive Cycle 3: just after the second reproduction period (week 40, W40), before the change of photoperiod, i.e. early vitellogenesis (week 52, W52), at mid vitellogenesis (week 58, W58), at the last step of vitellogenesis (week 68, W68) and during spawning season (week 75, W75). . The measurements were carried out on the same animals (females were individually identified with a RFID Pit-tag) at different times; data can be considered as dependent. Linear mixed model was applied; the best model was then selected using the Akaike Information Criterion (AIC). Replicates correspond to different individual females (n = 10 per treatment). “n.s”: not significant; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001. Different letters indicate significant differences between maternal origin, which were investigated with a Tukey post hoc test treatment) after 4 or 8 weeks of rearing (14.29 ± 3.15 g Impact of the origin of the maternal diet on the lipid for progeny from CB-fed females versus 14.02 ± 2.55 g metabolism of the progeny for progeny from MAB-fed females at the end of Maternal nutrition affected lipid metabolism of the pro- growth trial). The different measures of the mean geny that were fed the CO diet or challenged with the weight carried out throughout the rearing period MAO diet (n = 10 livers from individual fingerlings per (once every 2 weeks) did not reveal any significant treatment) (Fig. 5). The FA β-oxidation pathway of pro- difference between the two maternal origins (n =2 geny seems to be affected by maternal nutrition origin. racks per treatment from week 0 to week 4 and n =4 The expression of the hepatic CPT1a gene was up- racks from week 5 to week 8). regulated in progeny from MAB-fed females (Fig. 5A), After the nutritional challenge (i.e. progeny fed the regardless of the diet of the offspring. Further, the CO MAO diet for 4 weeks), although no difference was ob- diet magnified the impact of the maternal nutritional served on percent survival (90% for both maternal ori- history on the hepatic expression of CPT1a. gins), the final individual weights of the fish (n = 30 fish Similarly, feeding female broodstock the MAB diet led per treatment) were significantly higher (P = 0.02) for to an up-regulation of some genes involved in LC-PUFA progeny from MAB-fed females (12.98 ± 2.99 g vs. biosynthesis in the progeny. Thus, offspring exhibited an 11.65 ± 2.25 g) (Fig. 4B). up-regulation of hepatic SCDB, ELOVL2b, FADS2a and A biochemical analysis of the whole-body compos- FADS2b when female broodstock were fed the MAB diet ition of the fingerlings (n = 4 pools of fingerlings per (Fig. 5B). The nutritional challenge with MAO diet ac- treatment) indicated no significant difference linked centuated the difference of FADS2a gene expression be- to the maternal diet in terms of lipids and proteins tween the progeny from MAB-fed females and those (Table 6). from CB-fed females. Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 10 of 18 Table 3 Reproductive performances of females, egg quality and fingerling biometric parameters according to diet treatment during reproductive Cycle 2 and Cycle 3 Cycle 1 Cycle 2 Statistical results Diets CB MAB CB MAB Diet Cycle Diet × Cycle Female biometric parameters and reproductive performances Survival, % 90.32 ± 2.38 91.81 ± 0.71 94.10 ± 3.78 90.00 ± 14.14 n.s n.s n.s Weight female at spawning time, g 3770.39 ± 349.83 3799.18 ± 310.41 5285.21 ± 623.48 5016.32 ± 510.36 n.s *** ** Egg spawn weight, g 551.91 ± 123.11 542.98 ± 119.53 682.56 ± 135.11 675.02 ± 133.11 n.s *** n.s Absolute fecundity, eggs per female 7887.09 ± 2008.14 8086.81 ± 2046.72 9175.20 ± 2005.94 9988.04 ± 2173.13 n.s *** n.s Relative fecundity, eggs/kg of female 2108.84 ± 543.57 2134.54 ± 534.79 1764.04 ± 450.98 2007.70 ± 451.19 n.s *** n.s Egg quality Egg diameter, mm 5.20 ± 1.11 5.15 ± 0.19 4.90 ± 0.48 4.64 ± 0.63 ** *** * Coefficient of variation of egg diameter 3.29 ± 1.11 3.15 ± 0.88 3.07 ± 0.51 3.03 ± 0.43 n.s n.s n.s White eggs, % 6.41 ± 8.58 6.66 ± 9.98 8.89 ± 16.72 2.88 ± 5.13 n.s n.s * Embryo development Fry survival after resorption, % _ _ 47.58 ± 33.65 70.29 ± 17.55 * _ _ Fry weigth, mg _ _ 12.99 ± 1.48 12.53 ± 1.52 n.s _ _ Malformation rate of fry, % _ _ 3.87 ± 5.55 4.30 ± 6.63 n.s _ _ No resorption rate of fry, % _ _ 0.40 ± 0.82 0.41 ± 0.35 n.s _ _ Values are means ± s.d. Two-way analysis of variance was carried out in order to assess effects of diet and cycle of reproduction. Replicates to asses statistical effect on reproductive performances of females and egg quality correspond to different individual females (n = 90 females per treatment). Replicates to asses statistical effect on fingerling biometric parameters correspond to different individual egg batches (n = 10 egg batches per treatment). “n.s”: not significant; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001 Finally, the maternal nutritional history also affected Schizochytrium sp. supplementation in plant diet on cholesterol biosynthesis in the liver. Higher relative ex- lipid metabolism due to the high DHA content of this pression of CYP51a and b, and DHCR7 were recorded in micro-algae and of the important role of this fatty acid the progenies of MAB-fed females, whether fed with a in the trout reproduction but it was not possible to re- CO diet or challenged with a MAO diet. A different ex- ject completely any effect on the effect on reproductive pression pattern was observed for HMGCRb which was performance and progeny of other factors such as diet- up-regulated in fry from MAB-fed females but only ary protein content, amino acid profile additives, etc. when fed the CO diet (Fig. 5C). Genes involved in the elimination of cholesterol were Validation of DHA-rich microalgae as supplementation in only affected by maternal nutritional history when pro- a plant-based diet for female broodstock geny were fed the CO diet as illustrated by the up- The present study indicates that for rainbow trout fe- regulation of ABCG5 and LXRα gene expression in the male broodstock, a plant-based diet containing Schizo- fry from MAB-fed females (Fig. 5D). chytrium sp. micro-algae as an alternative source of DHA could be as efficient as the current commercial Discussion diet, during the reproductive cycle. Despite a signifi- FM and FO replacement in aquaculture diet is the key cantly lower growth rate for females fed the plant-based issue for maintaining sustainable aquaculture produc- diet containing Schizochytrium sp. micro-algae, the re- tion. Although research on this topic for growing trout productive performances, namely egg weight, absolute is well advanced, there is little research on the impact of fecundity and relative fecundity, were similar to brood- this replacement on broodstock and their offspring. The stock females fed a commercial diet containing fishmeal first objective of the present study was to determine if and fish oil. Moreover, during the second reproductive microalgae could be an efficient alternative source of cycle, even if egg diameter was lower, eggs produced by DHA in a plant-based diet dedicated to female brood- females fed the plant-based diet supplemented with stock. The second objective was to investigate the pos- microalgae exhibited a greater integrity illustrated by sible implementation of a nutritional programming in fewer white eggs after 24 h of hydration, which indicates the offspring, related to maternal nutritional history. a better overall egg quality. The presence of white eggs However, we would advise that in the present study, can be interpreted as an indirect measure of vitelline we have chosen to highlight the impact of the membrane integrity. Therefore, when eggs are of good Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 11 of 18 Table 4 Main fatty acids (% of total FA) of broodstock diets (C reproductive performances and egg quality by reducing the and MA) egg size and the survival of the offspring. As reproductive Broodstock diet performance was not impaired in the present study, it can be assumed that the addition of DHA-rich microalgae can limit Saturated fatty acids (SFA) CB MAB the negative effects of plant-based diets on reproduction. 14:0 6.30 ± 0.06 0.47 ± 0.04 16:0 18.81 ± 0.12 17.54 ± 0.37 Possible improvement of egg quality through a fatty acid 18:0 3.14 ± 0.38 2.39 ± 0.02 profile that appears more suitable with a DHA-rich Total saturated FA (SFA) 29.27 ± 0.81 21.46 ± 0.11 microalgae plant diet Monounsatured fatty acids (MUFA) The vitellus reserves are intended to feed the embryo endo- 16:1 9.21 ± 2.65 0.44 ± 0.10 trophically until the complete resorption of the yolk sac and the transition to exotrophic feeding . In the present 18:1 14.49 ± 0.47 24.08 ± 0.30 study, the difference in FA profile of the eggs could explain 20:1 2.14 ± 0.21 0.63 ± 0.07 the higher quality of eggs produced by females fed the plant- 22:1 1.62 ± 0.05 0.37 ± 0.00 based diet. The FA composition of egg reserves is a good Total monosatured FA 27.59 ± 3.39 25.73 ± 0.04 proxy for the female broodstock diet, further supporting re- Polyunsatured fatty acid (PUFA) sults reported in previous studies on rainbow trout or 16:2 n-4 1.34 ± 0.13 0.01 ± 0.01 other fish species [13, 40]. However, although the diets used in this study contained very distinct levels of DHA, the dif- 16:3 n-4 1.37 ± 0.03 0.08 ± 0.00 ferences observed in the eggs were considerably less signifi- 16:4 n-1 2.40 ± 0.33 0.04 ± 0.00 cant than in the diets. This result confirms that DHA is PUFA n-6 selectively accumulated in eggs regardless of its level in the 18:2 n-6 5.74 ± 0.46 20.27 ± 0.96 diet [40, 41]. A significant proportion of EPA was found in 20:4 n-6 0.78 ± 0.20 0.18 ± 0.16 the eggs of females fed the commercial diet (10% to 12%), 22:5 n-6 0.14 ± 0.05 4.89 ± 0.15 reflecting the high EPA content of the commercial diet. Fur- ther, despite the near absence of EPA in the plant-based diet, Total PUFA n-6 9.80 ± 4.20 25.97 ± 0.75 EPA was also detected in eggs from females fed the plant- PUFA n-3 based diet, in non-negligible proportions (between 3.9% and 18:3 n-3 0.95 ± 0.06 8.76 ± 0.19 5.1%). Two hypotheses can be proposed to explain this 18:4 n-3 1.74 ± 0.09 0.11 ± 0.01 phenomenon. As during the first breeding eggs are of poor 20:5 n-3 15.50 ± 0.02 0.37 ± 0.15 quality and barely used for fry production, the experiment 22:5 n-3 1.72 ± 0.24 0.08 ± 0.01 started with broodstock females, just after their first reproduction. During this period, fish were fed the standard 22:6 n-3 5.63 ± 1.02 15.50 ± 0.46 commercial diet. It is known that the n-3 PUFAs are stored Total PUFA n-3 24.29 ± 0.74 16.27 ± 0.60 in the female’s tissue reserves for further use during develop- Ratio ment and then selectively mobilized and incorporated into SFA/PUFA 0.73 ± 0.01 0.42 ± 0.01 the eggs during vitellogenesis . It is thus possible that the n3 / n6 3.67 ± 0.31 0.97 ± 0.02 EPA present in the eggs of females fed the experimental Index Insat 198.83 ± 0.39 216.74 ± 4.61 plant-based diet, which was almost devoid of EPA, comes from the tissue reserves accumulated by the female before EPA/DHA 2.80 ± 0.50 0.02 ± 0.01 the first reproduction and then mobilized for the benefit of ARA/EPA 0.05 ± 0.01 0.42 ± 0.26 the eggs during the second and third reproductive periods. ARA/DHA 0.14 ± 0.01 0.01 ± 0.01 However, EPA could have also been biosynthesized from its precursor, the ALA, present in large quantities in the plant- quality, the vitelline membrane is highly impermeable to based diet [43, 44]. The two phenomena, the mobilization of water and electrolytes which reduces the risk of rupture of reserves or biosynthesis, can proceed at the same time. the membrane . Inversely, when eggs are of bad quality, Finally, the concentrations of ARA were also of inter- the vitelline membrane is weakened and the water pressure est. In the eggs produced by the females fed the plant- is enough to break it. In this case, eggs turns white during based diet supplemented with microalgae, the propor- hydration . The higher fry percent survival after resorp- tion of ARA was significantly higher than in females fed tion also confirmed higher egg quality from females fed the the control diet, though it was much less abundant in plant-based diet. In a previous study, Lazzarotto et al.  the plant-based diet (0.2% vs. 0.8%). This demonstrates a showed that a plant-based diet completely devoid of long selective incorporation of ARA into the eggs of females chain PUFAs had negative consequences on rainbow trout fed the plant-based diet. Thus, ARA was probably Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 12 of 18 Table 5 Fatty acid profiles (% of total FA) of eggs from females fed C or MA diet sampled during Cycle 2 and Cycle 3 of the experimentation Cycle 2 Cycle 3 Statistical results Saturated fatty acids (SFA) CB MAB CB MAB Diet Cycle Diet x Cycle 12:0 _____ _ _ 14:0 2.27 ± 0.14 0.49 ± 0.03 2.62 ± 0.14 0.45 ± 0.04 *** *** n.s 15:0 0.25 ± 0.01 0.13 ± 0.01 0.26 ± 0.02 0.14 ± 0.01 *** *** * 16:0 15.47 ± 0.50 14.10 ± 0.69 16.14 ± 0.77 15.04 ± 0.40 *** *** n.s 17:0 0.29 ± 0.02 0.17 ± 0.01 0.28 ± 0.03 0.18 ± 0.02 *** n.s n.s 18:0 5.70 ± 0.38 4.71 ± 0.36 5.91 ± 0.25 5.50 ± 0.35 *** *** ** 20:0 0.04 ± 0.01 0.05 ± 0.01 0.05 ± 0.00 0.05 ± 0.01 *** ** n.s 22:0 n.d n.d n.d n.d _ _ _ Total saturated FA (SFA) 24.03 ± 0.39 19.65 ± 0.99 25.26 ± 0.99 21.35 ± 0.69 *** *** n.s Monounsatured fatty acids (MUFA) 16:1 5.56 ± 0.23 2.90 ± 0.26 6.12 ± 0.29 2.75 ± 0.32 *** n.s *** 17:1 0.00 ± 0.00 0.00 ± 0.00 0.08 ± 0.01 0.00 ± 0.00 *** *** *** 18:1 19.92 ± 0.92 23.91 ± 1.30 17.48 ± 0.69 20.79 ± 0.77 *** *** n.s 20:1 1.50 ± 0.12 1.38 ± 0.25 1.64 ± 0.18 1.63 ± 0.21 * *** n.s 22:1 0.04 ± 0.05 0.00 ± 0.00 0.03 ± 0.03 0.00 ± 0.00 *** n.s n.s Total monosatured FA 27.04 ± 0.95 28.18 ± 1.07 25.38 ± 1.02 25.17 ± 0.99 n.s *** n.s Polyunsatured fatty acid (PUFA) 16:2 n-4 0.27 ± 0.05 0.00 ± 0.00 0.35 ± 0.03 0.14 ± 0.02 *** *** n.s 16:3 n-4 0.28 ± 0.02 0.10 ± 0.02 0.30 ± 0.02 0.02 ± 0.02 *** *** *** 16:4 n-1 0.12 ± 0.02 0.00 ± 0.00 0.14 ± 0.02 0.05 ± 0.02 *** *** n.s 18:2 n-4 0.39 ± 0.02 0.06 ± 0.01 0.41 ± 0.02 0.00 ± 0.00 ** n.s *** 18:3 n-4 0.51 ± 0.02 0.06 ± 0.02 0.52 ± 0.04 0.03 ± 0.03 *** * n.s 18:4 n-1 0.65 ± 0.04 0.09 ± 0.02 0.68 ± 0.08 0.00 ± 0.00 *** * *** PUFA n-6 18:2 n-6 5.14 ± 0.41 10.94 ± 1.27 4.09 ± 0.34 11.20 ± 0.71 *** ** *** 18:2 n-4 0.39 ± 0.02 0.06 ± 0.01 0.41 ± 0.02 0.00 ± 0.00 ** n.s *** 18:3 n-6 0.16 ± 0.03 0.29 ± 0.06 0.06 ± 0.01 0.28 ± 0.06 *** n.s *** 20:2 n-6 1.04 ± 0.08 1.93 ± 0.24 0.95 ± 0.09 2.40 ± 0.32 *** ** *** 20:3 n-6 0.60 ± 0.08 1.02 ± 0.07 0.55 ± 0.06 1.21 ± 0.17 *** ** *** 20:4 n-6 1.80 ± 0.08 3.29 ± 0.20 1.74 ± 0.06 3.91 ± 0.22 *** *** * 22:2 n-6 0.08 ± 0.03 0.08 ± 0.04 0.15 ± 0.08 0.15 ± 0.04 *** *** * 22:4 n-6 0.10 ± 0.01 0.22 ± 0.04 0.12 ± 0.02 0.30 ± 0.05 *** *** *** 22:5 n-6 0.15 ± 0.03 2.26 ± 0.22 0.15 ± 0.01 2.56 ± 0.19 *** *** *** Total PUFA n-6 11.29 ± 0.52 20.35 ± 1.05 10.23 ± 0.48 22.26 ± 0.85 *** n.s *** PUFA n-3 16:4 n-3 0.05 ± 0.02 0.00 ± 0.00 0.04 ± 0.02 0.07 ± 0.01 *** *** n.s 18:3 n-3 1.00 ± 0.09 3.03 ± 0.39 0.61 ± 0.09 2.90 ± 0.20 *** *** * 18:4 n-3 0.39 ± 0.06 0.39 ± 0.09 0.32 ± 0.04 0.35 ± 0.08 ** * n.s 20:3 n-3 0.21 ± 0.05 0.40 ± 0.07 0.14 ± 0.02 0.40 ± 0.06 *** * * 20:4 n-3 0.79 ± 0.10 0.54 ± 0.05 0.72 ± 0.11 0.41 ± 0.06 *** *** n.s 20:5 n-3 10.91 ± 0.54 5.07 ± 0.32 10.60 ± 0.71 3.58 ± 0.45 *** *** *** 21:5 n-3 0.40 ± 0.01 0.07 ± 0.01 0.48 ± 0.04 0.00 ± 0.00 *** n.s *** Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 13 of 18 Table 5 Fatty acid profiles (% of total FA) of eggs from females fed C or MA diet sampled during Cycle 2 and Cycle 3 of the experimentation (Continued) Cycle 2 Cycle 3 Statistical results Saturated fatty acids (SFA) CB MAB CB MAB Diet Cycle Diet x Cycle 22:5 n-3 4.33 ± 0.33 1.77 ± 0.15 4.99 ± 0.62 1.25 ± 0.13 *** n.s *** 22:6 n-3 18.95 ± 1.45 20.09 ± 1.46 19.70 ± 1.36 21.40 ± 0.94 *** *** n.s Total PUFA n-3 35.57 ± 1.38 27.94 ± 1.42 36.64 ± 0.89 27.04 ± 0.64 *** *** *** Ratio SFA/PUFA 0.50 ± 0.02 0.38 ± 0.03 0.53 ± 0.02 0.41 ± 0.02 *** *** n.s n3 / n6 4.09 ± 0.31 1.57 ± 0.12 4.83 ± 0.25 1.38 ± 0.05 *** *** *** Index Insat 257.33 ± 6.52 253.43 ± 6.21 258.24 ± 3.97 253.14 ± 4.22 * *** n.s EPA/DHA 0.58 ± 0.06 0.25 ± 0.03 0.54 ± 0.07 0.17 ± 0.03 *** *** n.s ARA/EPA 0.16 ± 0.01 0.65 ± 0.05 0.16 ± 0.01 1.11 ± 0.13 *** *** *** ARA/DHA 0.10 ± 0.01 0.16 ± 0.01 0.09 ± 0.01 0.18 ± 0.02 *** *** *** Values are means ± s.d. Two-way analysis of variance was carried out in order to assess effects of diet and cycle of reproduction. Replicates correspondto different individual egg batches (n = 10 per treatment). “n.s”: not significant; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001 biosynthesized from linoleic acid (LA) and stored in the reproduction [45–47] and egg quality [40, 48, 49]. In eggs of the females fed the plant-based diet enriched both mammals and fish, ARA and EPA are considered with DHA. This increased proportion of ARA and the as the precursors of eicosanoids, namely prostaglandin higher ARA/EPA ratio in the eggs of females fed the (Pg), thromboxane (Tx) and leukotriene (Lt) but ARA is plant-based diet might explain the higher fry survival considered the most active eicosanoid precursor in fish after resorption. In fish, ARA plays a major role in . The competitive relationship between ARA and Fig. 4 Effect of maternal nutrition on fry performances (A) during classic growth trial where fry were fed a CO diet for 12 weeks (evolution of mean body weight (g) during the 12 week-trial, individual weight (g) and survival percent (%) after 8 and 12 weeks) and (B) after 4 weeks of nutritional challenge where fry were fed the MAO diet (individual weight (g) and survival percent (%)). One-way analysis of variance was carried out in order to assess effects of maternal nutritional origin on individual final weight; replicates correspond to different individual fingerlings(n = 30 fingerlings per treatment). Kruskal-Wallis test was carried out to assess the effect of maternal nutritional origin on survival rate (n = 4 racks at week 8 and n = 2 racks at week 12) and the weight mean during rearing (n = 2 racks per treatment from week 0 to week 4 and n = 4 racks from week 5 to week 8). “n.s”: not significant; “*”: P < 0.05 Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 14 of 18 Table 6 Proximate composition of progeny according to maternal nutritional origin and diet of progeny (fed a commercial diet or challenged with a MA diet) Progeny diet CO MAO Statistical results Maternal origin CB MAB CB MAB Maternal origin Progeny diet Dry Matter, % 22.8 ± 0.3 21.9 ± 0.00 23.6 ± 0.3 23.9 ± 0.1 n.s *** Protein, % WM 14.3 ± 0.5 13.81 ± 0.1 13.9 ± 0.2 13.8 ± 0.1 n.s *** Lipids, % WM 7.1 ± 0.2 7.2 ± 0.2 9.1 ± 0.1 9.3 ± 0.2 n.s *** Ash, % WM 2.0 ± 0.1 1.9 ± 0.1 1.7 ± 0.1 1.7 ± 0.1 n.s *** Energy, kJ/g WM 5.8 ± 0.1 5.5 ± 0.3 6.4 ± 0.1 6.5 ± 0.1 n.s ** Kruskal-Wallis test was carried out to assess the effects of diet and cycle of reproduction on proximate composition. Replicates correspond to different pools of fingerlings (n = 4 per treatment). Values are means ± s.d. “n.s”: not significate; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001. WM = wet matter. EPA in the production of eicosanoids has drawn at- diet had a more suitable profile of PUFAs which tention to the importance of the EPA/ARA ratio in could result in better egg quality. Results from this addition to the individual levels of these PUFAs . studyconfirm theimportanceofthe balancebetween Furthermore, EPA and ARA compete for the same PUFAs and highlight a specific requirement for ARA metabolic and enzymatic pathways  which could in female rainbow trout broodstock. Further studies explain the difference in egg quality observed in this are necessary to determine the specifics of the re- study. Thus, the present study suggests that the MAB quirement in rainbow trout. Fig. 5 Relative expression of genes involved in hepatic lipid metabolism of the progeny according maternal origin (MO) and progeny diet (PD: fed a C diet or challenged with a MA diet). Only genes where a significant effect of maternal origin are represented. Other results are presented in Additional file 3: Table S3. Different pathways of pentose phosphate (A), of β-oxidation FA (B), of biosynthesis of PUFA (C), of cholesterol synthesis (D) and of cholesterol elimination (E) are represented in different boxes. Two-way analysis of variance was carried out in order to assess effects of maternal nutritional origin and diet of progeny. Replicates correspond to liver from different individual fingerlings (n = 10 per treatment). “n.s”: not significate; “*”: P < 0.05; “**”: P < 0.01; “***”: P < 0.001. a.u = arbitrary unit. Different letters indicate significant differences between groups, which were investigated with a Tukey post hoc test Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 15 of 18 Confirmation of nutritional programming through controlling the mitochondrial uptake of long-chain acyl- maternal nutrition CoAs. Expression of CPT1 in the liver of rainbow trout The vitellus reserves of the egg are known to affect pro- is strongly, directly and differently regulated by individ- geny survival and development and are at the origin of ual FAs. EPA down-regulates CPT1 expression in rain- early nutritional programming of phenotypes in fish bow trout while DHA has the opposite effect . The . Nutritional programming is emerging as a potential different contents of EPA and DHA between the com- strategy to modulate some metabolic pathways and to mercial diet and the DHA enriched plant-based diet improve the ability of fish to grow despite being fed a given to fingerlings did not lead to a differential expres- challenging diet. This study supports this assumption. sion of CPT1 in the progeny. However, the MAB diet Indeed, the present results demonstrate that the seems to be responsible for a higher expression of CPT1 utilization of plant-based diets in rainbow trout could be in the progeny. This highlights the occurrence of an- improved by maternal nutrition. Feeding females a other maternal nutritional programming process, which plant-based diet supplemented with micro-algae im- could be linked to the FA profile of the maternal diet. proves growth in 4-month-old progeny challenged with Maternal nutrition also induced changes in LC-PUFA a plant-based diet also supplemented with microalgae. biogenesis. Progeny of females fed the plant-based diet This is in accordance with previous results on gilthead supplemented with microalgae exhibited higher expres- sea bream which showed that replacement of FO with sion of genes involved in elongation and desaturation of linseed oil in broodstock diets improved growth in 4- n-3 and n-6 FAs. Such changes are consistent with pre- month-old progeny challenged with low FO and FM di- vious results showing that feeding gilthead sea bream ets for a period of 1 month . broodstock different FA profiles affects the LC-PUFA Nevertheless, the effect of programming was revealed biosynthesis pathway of the progeny [13, 53]. Long- regardless of the diet fed to the progeny. At the molecu- chain PUFA can be synthesized from ALA and LA in lar level, whether the progeny is fed a commercial diet vertebrates through a series of desaturation and elong- or challenged with a plant-based diet supplemented with ation reactions . Therefore, the higher expression of DHA, lipid and cholesterol metabolisms were affected by SCBE, FADS2a, FADS2b and ELOVL2b could be an the maternal nutrition. The capacity of endogenous bio- adaptation to the very high proportion of ALA and LA synthesis of cholesterol and LC-PUFAs were enhanced supplied by the MAB broodstock diet . in the progeny of females fed the plant-based diet, at the messenger RNA level. Conclusion The higher expression of genes involved in cholesterol To conclude, the present study demonstrates that sup- synthesis (HMGCRb, CYP51a, CYP51b, DHCR7b) could plementation of a plant-based diet with DHA-rich be a consequence of the near absence of cholesterol in microalgae yields reproductive performance and egg the maternal diet. This maternal cholesterol deficiency, quality comparable to those observed with a conven- which induces a significant decrease in the plasma chol- tional commercial feed containing FM and FO. More- esterol level in female broodstock, could be at the origin over, we show that feeding a plant-based diet enriched of a parental nutritional programming of the offspring in DHA to rainbow trout broodstock females could in- leading to an increased capacity of the progeny to bio- duce metabolic programming processes in the progeny synthesize cholesterol in anticipation of a possible ab- that may be related to the lipid profile of the maternal sence of cholesterol in the diet. Maternal diet. In order to better understand these programming cholesterolemia is known to affect the hepatic choles- events, the underlying molecular mechanisms will need terol metabolism in mouse offspring . This kind of to be characterized. Particular attention should be paid nutritional programming through maternal nutrition to epigenetic mechanisms known to orchestrate pro- thus seems to trigger a “predictive adaptive response” to gramming by maternal nutrition . quote the words of Gluckman et al. . Increased ex- pression of genes involved in the cholesterol elimination Abbreviations FM: Fishmeal; FO: Fish oil; SFA: Saturated fatty acid; MUFA: Monounsaturated pathway (ABCG5 and LXR) in progeny from females fed fatty acid; LC-PUFA: Long chain polyunsaturated fatty acid; a plant-based diet is only observed when the progeny EPA: Eicosapentaenoic acid (20:5 n-3); DHA: Docosahexaenoic acid (22:6 n-3); was fed the commercial diet. The neosynthesized choles- LA: Linoleic acid (18:2 n-6); ALA: Linolenic acid (18:3 n-3); DPA: Docosapentaenoic acid (22:5 n-6); ARA: Arachidonic Acid (20:4 n-6); terol added to the cholesterol supplied by the commer- ACLY: ATP cytrate lyase; FAS: Fatty acid synthase; CPT1a: Carnitine palmitoyl cial diet likely led to a high accumulation of cholesterol, transferase 1; HADH: HydroxyacylcoA dehydrogenase; ACOX: AcylcoA hence an increase of its elimination only when the pro- oxidase; SCDB: Acyl-CoA desaturase - delta-9 desaturase; ELOVL2: Elongation of very long chain fatty acids protein 2; ELOVL5: Elongation of very long geny was fed with a diet rich in cholesterol. chain fatty acids protein 5; FADS2: Fatty acid desaturase 2; HMGCS: 3- Carnitine palmitoyltransferase-1 is considered as a hydroxy-3-methylglutaryl-CoA synthase 1; HMGCR: 3-hydroxy-3- rate-limiting step of the mitochondrial β-oxidation by methylglutaryl-CoA reductase; CYP7a: Cholesterol 7 alpha hydroxylase a; Cardona et al. Journal of Animal Science and Biotechnology (2022) 13:33 Page 16 of 18 CYP51: Lanosterol 14-alpha demethylase; ABCA1: ATP-binding cassette sub- laboratory, F-35000 Rennes, France. Viviers de Sarrance, F-64490, Sarrance, family A member 1-like; ABCG5: ATP binding cassette subfamily G member 5; France. Viviers de Rébénacq, F-64260, Rébénacq, France. ABCG8: ATP binding cassette subfamily G member 8; DHCR7: 7- dehydrocholesterol reductase Received: 27 September 2021 Accepted: 13 January 2022 Supplementary Information The online version contains supplementary material available at https://doi. References org/10.1186/s40104-022-00680-9. 1. Mowi company. Salmon Farming Industry Handbook 2019. 2019. Available from URL: https://ml.globenewswire.com/Resource/Download/1766f220-c83 Additional file 1: Table S1. Main fatty acid (% of total FA) of progeny b-499a-a46e-3941577e038b. diets (C and MA). 2. Food and Agriculture Organisation (FAO). 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We thank Chloé Barrier-Loiseau, Laura Vas- 020-0078-x. seur, Floriane Colon, Patrick Maunas, Nicolas Turronet and the Viviers de Sar- rance staff for their help during experimentation. We thank Yann Marchand 6. Sanz A, Morales AE, de la Higuera M, Cardenete G. Sunflower meal for its help in diet manufacturing and for its expertise. We thank all of the compared with soybean meals as partial substitutes for fish meal in rainbow people of NuMeA for the help that they provided during the sampling and trout (Oncorhynchus mykiss) diets: protein and energy utilization. reproductive seasons. We thank Therese Callet, Nathan Favalier and Lucie Aquaculture. 1994;128(3-4):287–300. https://doi.org/10.1016/0044-8486(94 Marandel who designed the primers for different paralogues of genes in- )90318-2. volved in lipid metabolism. In addition, we thank in particular Therese Callet 7. Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconneau B, Laroche M. 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Journal of Animal Science and Biotechnology – Springer Journals
Published: Mar 10, 2022
Keywords: Egg quality; Micro-algae; Nutritional programming; Plant diet; Rainbow trout; Reproduction
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