Source: TEXAS A&M UNIVERSITY submitted to NRP
BIOSYNTHESIS AND NUTRITIONAL ROLES OF GLYCINE IN HYBRID STRIPED BASS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1027856
Grant No.
2022-67015-36200
Cumulative Award Amt.
$650,000.00
Proposal No.
2021-07147
Multistate No.
(N/A)
Project Start Date
Feb 1, 2022
Project End Date
Jan 31, 2026
Grant Year
2022
Program Code
[A1231]- Animal Health and Production and Animal Products: Improved Nutritional Performance, Growth, and Lactation of Animals
Recipient Organization
TEXAS A&M UNIVERSITY
750 AGRONOMY RD STE 2701
COLLEGE STATION,TX 77843-0001
Performing Department
Animal Science
Non Technical Summary
Non-Technical Project SummaryThe United States is the top producer of hybrid striped bass (HSB) in the world. Fishmeal has traditionally been used as the major protein feedstuff in HSB diets, but this approach is not sustainable in aquaculture due to the increasingly limited sources and high costs of fishmeal. Thus, there has been growing interest in using plant proteins (mainly soybean meal) to replace fishmeal in aquafoods, but success has been variable. We found that glycine (the most abundant amino acid in the body of fish and fishmeal) is relatively low in plant proteins. Based on results of our preliminary study, we hypothesize that dietary glycine plays an important role in HSB growth by maximizing protein synthesis, anti-oxidative capacity, and creatine (muscle builder) production in their tissues. We will test this hypothesis by pursuing three specific objectives to determine: (1) tissue-specific glycine- and creatine-synthetic pathways in HSB; (2) roles of glutathione (the most abundant low-molecular weight anti-oxidant) and creatine in mediating the effect of dietary glycine to improve growth, anti-oxidative responses, intestinal integrity, metabolic health, and immunity in HSB; and (3) roles of the target of rapamycin (TOR; the master regulator of protein synthesis) and autophagy/proteasomes (intracellular machineries for protein degradation) in mediating the effect of dietary glycine to promote protein synthesis and inhibit proteolysis in tissues of HSB. We expect that: (1) in contrast to land mammals, skeletal muscle is the major site for creatine synthesis from glycine in HSB; (2) glycine activates the TOR cell signaling pathway to promote protein synthesis in skeletal muscle, while reducing intramuscular protein breakdown via the autophagy/proteasomes pathways, to promote muscle growth; and (3) supplementing 2% glycine to soybean meal (58%)-based diets can replace 45% fishmeal in HSB diets. Our findings will have a significant impact on U.S. aquaculture by generating new fundamental knowledge about the crucial role of glycine in improving the growth of HSB and providing a new nutritional method for the use of glycine to substantially reduce the inclusion level of fishmeal in soybean meal-based diets for the fish.
Animal Health Component
15%
Research Effort Categories
Basic
85%
Applied
15%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30237131010100%
Knowledge Area
302 - Nutrient Utilization in Animals;

Subject Of Investigation
3713 - Striped bass;

Field Of Science
1010 - Nutrition and metabolism;
Goals / Objectives
The overall goal of our research is to improve the growth and productivity of hybrid striped bass (HSB), while developing effective nutritional strategies to replace fishmeal in their diets. In the current project, we will pursue three specific objectives to determine: (1) tissue-specific glycine- and creatine-synthetic pathways in HSB; (2) roles of glutathione (the most abundant low-molecular weight anti-oxidant) and creatine in mediating the effect of dietary glycine to improve growth, anti-oxidative responses, intestinal integrity, metabolic health, and immunity in HSB; and (3) roles of the target of rapamycin (TOR; the master regulator of protein synthesis) and autophagy/proteasomes (intracellular machineries for protein degradation) in mediating the effect of dietary glycine to promote protein synthesis and inhibit proteolysis in tissues of HSB.
Project Methods
Juvenile HSB (Morone saxatilis ?) x white bass (M. chrysops ?) with a body weight (BW) of ~ 3 g will be obtained from Keo Fish Farms (Keo, AR), and maintained in our indoor water recirculation system (55 L water per tank) at 26°C. Water is circulated through mechanical and biological filters and changed regularly (30-50% every 3 days). Air is supplied to the water through air stones connected to air pumps. The dissolved oxygen in water is maintained above 6 mg/L, its salinity at 1 ppt, and the photoperiod of the housing facility at 12 h per day. Water quality parameters (pH, ammonia, nitrite, and nitrate) are monitored daily and maintained within acceptable limits. Upon arrival at Texas A&M University, fish will be fed twice daily with 60% fishmeal diet for 1 week during the period of adaptation. Thereafter, the fish will be used for our study and fed our experimental diets.Specific Aim 1: HSB will be fed a low (15%)-fishmeal, soybean meal (58%)-based practical diet. On Days 0, 30, 60, 120, 180, HSB will be euthanized to obtain the stomach, proximal intestine, liver, skeletal muscle, kidney, heart, gill, skin, spleen, pancreas, and brain for enzyme assays. There will be 8 fish per age group. Frozen tissue (0.5 g), which will be combined from several fish at young ages, will be homogenized in 2 ml of freshly prepared buffer consisting of 300 mM sucrose, 5 mM HEPES (pH 7.4), 1 mM EDTA, 3 mM dithiothreitol, 0.5% (vol:vol) Triton X-100, and 0.1% (wt:vol) protease inhibitor (aprotinin, chymostatin, pepstatin A, and phenylmethylsulfonyl fluoride; 5 µg/ml each) for 2 min on ice. The whole homogenization mixture will be transferred to a tube. All tubes will be centrifuged at 600 × g for 10 min at 4°C. The supernatant fluid will be subjected to three cycles of freezing in liquid nitrogen and thawing in a 26°C water bath before use for determining the activities of the following enzymes: 4-hydroxyproline oxidase, 4-hydroxy-2-oxoglutarate aldolase, glutamate-pyruvate transaminase, alanine:glyoxylate transaminase, threonine dehydrogenase, serine hydroxymethyltransferase, arginine:glycine amidinotransferase (AGAT), guanidinoacetate N-methyltransferase (GAMT), S-adenosylmethionine synthetase, and creatine kinase. Furthermore, we will use (proximal intestine, liver, skeletal muscle, kidney, and skin) for incubation to directly determine the conversion of 4-hydroxyproline into glycine. The tissue extracts will be used for the HPLC analysis of glycine and other amino acids.Specific Aim 2: Beginning at ~5 g of BW, HSB will be fed a low (15%)-fishmeal, soybean meal (58%)-based practical diet supplemented with: 0% glycine, 2% glycine, 0.1% L-buthionine sulfoximine (BSO), 2% glycine + 0.1% BSO, 2% glycine + 0.1% BSO + 0.2% glutathione, 0.2% guanidine, 2% glycine + 0.2% guanidine, and 2% glycine + 0.2% guanidine + 1% creatine. BSO or glutathione will be included in the pelleted diet as a convenient way to administer the chemical to fish. An appropriate amount of alanine will be added to the diets other than the 2% glycine group, so that all diets will be isonitrogenous. There will be 8 tanks of fish (15 fish/tank) in each treatment group (a total of 960 fish; i.e., 8 groups x 8 tanks/group x 15 fish/tank = 960 fish for the trial). Fish will be fed their diets twice daily (8:00 AM and 8:00 PM) to apparent satiety for 8 weeks. Feed intakes of fish in each tank will be measured daily and their BWs be recorded every 4 weeks, respectively. At the end of the feeding period, the following procedures will be performed: (1) calculations of growth performance and feed efficiency, as well as measurements of the body composition of fish; (2) blood collection for analyses of amino acids, glutathione, and malonaldehyde (a product of lipid peroxidation); (3) analyses of intestinal morphology, expression of glycine transporters, and tight-junction proteins; (4) determination of intestinal amino acid transport using Ussing chambers and labeled amino acids; (5) analyses of concentrations of amino acids and glutathione, as well as the activities of glycine-synthetic enzymes in skeletal muscle, liver, kidney, and proximal intestine; (6) analyses of concentrations of creatine, creatine phosphate, and the activities of related enzymes in the skeletal muscle, liver, pancreas, kidney, and proximal intestine; and (7) immunological assessments of HSB challenged with 100 µg of trinitrophenyl-lipopolysaccharide.Specific Aim 3: Beginning at ~5 g of BW, HSB will be fed a low (15%)-fishmeal, soybean meal (58%)-based practical diet supplemented with: 0% glycine, 2% glycine, 10 ppm rapamycin, 2% glycine + 10 ppm rapamycin. Rapamycin (a specific inhibitor of TOR) will be included in the pelleted diet as a convenient way to administer the substance to fish. An appropriate amount of alanine will be added to the diets other than the 2% glycine group, so that all diets will be isonitrogenous. There will be 8 tanks of fish (15 fish/tank) in each treatment group (a total of 480 fish; i.e., 4 groups x 8 tanks/group x 15 fish/tank = 480 fish for the trial). Fish will be fed their diets twice daily (8:00 AM and 8:00 PM) to apparent satiety for 8 weeks. Feed intakes of fish in each tank will be recorded daily and BWs of fish will be measured every 4 weeks. At the end of the 8-week feeding period, the following procedures will be performed: (1) calculations of growth performance and feed efficiency, as well as measurements of the body composition of fish; (2) collection of blood and other tissues for analyses of amino acids and glutathione; (3) determination of protein synthesis in skeletal muscle, liver, kidney, and proximal intestine, using the [3H]phenylalanine flooding dose method; (4) analysis of TOR cell signaling proteins in skeletal muscle, liver, kidney, and proximal intestine, using western blot techniques. In addition, we will determine rates of proteolysis in the skeletal muscle, liver, kidney, and proximal intestine of HSB via the autophagy-lysosomal pathway and ubiquitin-dependent proteasomes.

Progress 02/01/24 to 01/31/25

Outputs
Target Audience:fish scientists; fish producers; and students in aquaculture, immunology, and nutrition Changes/Problems:None. What opportunities for training and professional development has the project provided?One PhD and one M.S. students received training from this project. How have the results been disseminated to communities of interest?The results were published in peer-reviewed journals and presented in scientific meetings. What do you plan to do during the next reporting period to accomplish the goals?We will use the 3H-phenylalanine flooding dose technique developed in our laboratory to determine effects of dietary glycine supplementation on the rates of protein synthesis in tissues. In addition, we will determine how HSB with or without glycine supplementation will respond to an immunological challenge with trinitrophenyl-lipopolysaccharide. Furthermore, we will use 14C-glycine and 14C-hydroxyproline and Ussing chambers to determine their transport by the intestine.

Impacts
What was accomplished under these goals? We found that glycine is a nutritionally essential amino acid for juvenile hybrid striped bass (HSB). When fed a 60%-fishmeal diet, about 40% of the glycine needed by the fish must be synthesized from its precursors. When fed a soybean meal-based diet, the fish must synthesized over 65%glycine. We found that a major source of glycine in HSB istrans-4-Hydroxy-L-Proline (Hyp), which is a major amino acid in the collagen of fish. The turnover of this protein releases a large amount of Hyp, which has traditionally been considered as a metabolic waste. However, results of recent studies have identified the conversion of Hyp into glycine in piglets. The present study test this hypothesis that hybrid striped bass (HSB, a carnivorous fish species) can form glycine from Hyp. Fish were fed a standard diet containing 60% fishmeal. Slices (~ 50 to 100 mg) of skeletal muscle, liver, proximal intestine, gill, and brain were obtained from approximately 45 g (n = 6) and 200 g (n = 6) HSB and incubated at 26 °C for 2 h in 1 ml of oxygenated (95% O2/5% CO2) Krebs-Henseleit bicarbonate buffer (pH 7.4, with 5 mM D-glucose) containing 0, 0.2 or 2 mM Hyp. Slices were also obtained for samples that received no incubation time. After a period of 2 h incubation, 200 μl of 1.5 M HClO4 was added into the incubation medium to stop the reaction. The acidified medium plus tissue together was homogenized and the homogenizer was rinsed with 1 ml water, followed by the addition of 100 μl of 2 M K2CO3. The neutralized extract was analyzed for amino acids using our HPLC method involving o-phthaldialdehyde. Data were statistically analyzed by the paired t-test. For 45-g HSB, glycine was produced from 0.2 and 2 mM Hyp by the liver and skeletal muscle, and 2 mM Hyp by the intestine (Table 1). For 200-g HSB, increasing medium Hyp concentrations from 0 to 0.2 and 2 mM Hyp enhanced (P < 0.05) the formation of glycine by the intestine in a dose-dependent manner, but there was no production of glycine from 0.2 and 2 mM Hyp by the liver or skeletal muscle. These results indicate the synthesis of glycine from Hyp by HSB in an age- and tissue-specific manner.

Publications

  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: He, W.L., X.Y. Li, and G. Wu. 2024. Dietary glycine supplementation enhances syntheses of creatine and glutathione by tissues of hybrid striped bass (Morone saxatilis ?� Morone chrysops ?) fed soybean meal-based diets. J. Anim. Sci. Biotechnol. 15:67.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Glycine nutrition and biochemistry from an aquaculture perspective. Anim. Front. 14:17-23.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2024 Citation: Connolly, E.D., B. Suehs, K. Hissen, M. Criscitiello, D. Gatlin, and G. Wu. 2024. Synthesis of glycine from trans-4-hydroxy-L-proline in tissues of juvenile hybrid striped bass (Morone chrysops x M. Saxatilis). J. Anim. Sci. 102 (Suppl. 3): 115116.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2025 Citation: Connolly, E.D., B.A. Suehs, K.L. Hissen, M.F. Criscitiello, D.M. Gatlin, and G. Wu. 2025. Glycine is a nutritionally essential amino acid in juvenile hybrid-striped bass (Morone chrysops x Morone saxatilis). The Conference of Research Workers in Animal Diseases (CRWAD), Chicago, Illinois, January 18-21, 2025.


Progress 02/01/23 to 01/31/24

Outputs
Target Audience:fish scientists; fish producers; and students in aquaculture, immunology, and nutrition Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two PhD students received training from this project. How have the results been disseminated to communities of interest?The results were published as peer-reviewed journal articles. What do you plan to do during the next reporting period to accomplish the goals?We will use our established method to determine effects of dietary glycine supplementation on glutathione and creatine synthesis in HSB, as well as cell signaling involving mechanistic target of rapamycin (MTOR), tissue protein synthesis, and tissue protein degradation. Furthermore, we will determine how HSB with or without glycine supplementation will respond to an immunological challenge with trinitrophenyl-lipopolysaccharide.

Impacts
What was accomplished under these goals? Feeding Experiment 1: The BW, weight gain, protein efficiency ratio (PER), and retention of dietary lipids in fish were enhanced (P < 0.05) by dietary supplementation with 1% or 2% glycine. In addition, dietary supplementation with glycine did not affect (P > 0.05) the feed intake of fish but increased (P < 0.05) the retention of dietary nitrogen, most AAs, and phosphorus in the body, compared to the 0% glycine group. Dietary supplementation with 1% and 2% glycine dose-dependently augmented (P < 0.05) the villus height of the intestine and reduced the submucosal thickness of the gut, while preventing submucosal and lamina propria hemorrhages. Compared with the 0% glycine group, dietary supplementation with 1% or 2% glycine decreased (P < 0.05) the proportion of skeletal-muscle fibers with diameters of 40-60 µm but increased (P < 0.05) the proportion of skeletal-muscle fibers with diameters of 80-100 µm and > 100 µm. Collectively, these findings indicate that glycine in SBM-based diets is inadequate for maximum growth of juvenile HSB and that dietary supplementation with 1% or 2% glycine is required to improve their weight gain and feed efficiency. Glycine is a conditionally essential AA for this fish. Feeding Experiment 2: Dietary supplementation with 1% and 2% glycine dose-dependently increased (P ? 0.05) the concentration of glycine in the plasma of HSB by 48% and 99%, respectively. Compared with the 0%-glycine group, dietary supplementation with 1% glycine did not affect (P ? 0.05) the feed intake of HSB but increased (P ? 0.05) their final BW, weight gain, and gain:feed ratios during the whole period by 13%, 29%, and 21%, respectively. Compared with the 1% glycine group, dietary supplementation with 2% glycine increased (P ? 0.05) the feed intake, final BW, and weight gain of HSB by 13%, 7%, and 14%, respectively. Compared with the 0%-glycine group, fish fed the 1%-glycine and 2%-glycine diets had a greater (P ? 0.05) villus height in the proximal intestine, when compared with the 0%-glycine group. The composition of AAs in the whole body of HSB was not affected by dietary glycine supplementation (Supplemental Table 1), suggesting that the types of proteins deposited in the body did not differ among the different dietary groups. However, with more gains of tissue proteins (including collagens), more dietary AAs including glycine were used for HSB growth in response to glycine supplementation. Based on BW gain, HSB weighing 5 to ~40 g (Feeding Experiment 1) responded to dietary supplementation with 2% glycine differently than older HSB weighing approximately 110 to 240 g. Specifically, the growth rate of Phase-II HSB fed the 2%-glycine diet was faster than that for fish fed the 1%-glycine diet, but this variable did not differ between younger HSB (5 to 40 g) fed the 1%-glycine and 2%-glycine diets. Thus, as fish grow, their ability to synthesize glycine is reduced and, therefore, they need more dietary glycine for protein (including collagen) accretion. In support of this, the content of total proteins in HSB weighing approximately 240 g was 6% greater than that in HSB weighing ~40 g. Collectively, these results indicated that SBM-based diets did not provide sufficient glycine for Phase-II HSB (110 to 240 g) and that dietary glycine supplementation is essential for their optimum growth and intestinal structure.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Li, X.Y., W.L. He, and G. Wu. 2023. Dietary glycine supplementation enhances the growth performance of hybrid striped bass (Morone saxatilis ?� Morone chrysops ?) fed soybean meal-based diets. J. Anim. Sci. 101:skad345, pp. 1-13.
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: He, W.L., X.Y. Li and G. Wu. Dietary glycine supplementation improves the growth performance of 110- to 240-g (phase-II) hybrid striped bass (Morone saxatilis ?� Morone chrysops ?) fed soybean meal-based diets. J. Anim. Sci. 101:skad400, pp. 1-13.


Progress 02/01/22 to 01/31/23

Outputs
Target Audience:fish scientists; fish producers; and students in fish biology, aquaculture, and nutrition Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two PhD students at Texas A&M University received training on this project. How have the results been disseminated to communities of interest?Through publication in a peer-reviewed journal. What do you plan to do during the next reporting period to accomplish the goals?We will determine effects of dietary glycine intake on the growth of juvenile HSB. We will also determine whether the synthesis of creatine and glutathione from glycine mediate the effect of glycine on the growth and protein accretion in juvenile hybrid striped bass.

Impacts
What was accomplished under these goals? In Year 1, juvenile hybrid striped bass (HSB; Morone saxatilis ? x M. chrysops ?) were obtained from Keo Fish Farms (Keo, AR), and maintained in our indoor water recirculation system (55 L water per tank) at 26°C. We determined glycine and creatine syntheses in tissues of HSB. Our results are summarized as follows. 1. Synthesis of glycine from 4-hydroxyproline in tissues of HSB We determined the synthesis of glycine from 4-hydroxyproline in the stomach, proximal intestine, liver, skeletal muscle, kidney, heart, gill, skin, spleen, pancreas, and brain of 15, 50, and 150 g HSB. The proximal intestine, liver, skeletal muscle, kidney, skin, and pancreas of all the weight groups of HSB could convert 0.25, 1 and 5 mM 4-hydroxyproline into glycine in a dose-dependent manner. These tissues contained all the necessary enzymes for this synthetic pathway: 4-hydroxyproline oxidase, 4-hydroxy-2-oxoglutarate aldolase, glutamate-pyruvate transaminase, alanine:glyoxylate transaminase. Based on its size, skeletal muscle was the major tissue for glycine synthesis from 4-hydroxyproline. By contrast, there was no detectable production of glycine from 0.25, 1 and 5 mM 4-hydroxyproline in the stomach, heart, gill, spleen, and brain of 15 to 150 g HSB. Thus, HSB synthesized glycine from fishmeal- and endogenously (collagen turnover)-derived 4-hydroxyproline in a tissue-specific manner to compensate for a deficiency of glycine in plant protein (e.g., soybean meal). 2. Synthesis of creatine from arginine plus glycine plus methionine in tissues of HSB We also determined creatine synthesis from 2 mM arginine plus 2 mM glycine plus 2 mM methionine in the stomach, proximal intestine, liver, skeletal muscle, kidney, heart, gill, skin, spleen, pancreas, and brain of 15, 50, and 150 g HSB. The liver, kidney, pancreas, and skeletal muscle of all the weight groups of HSB could synthesize creatine, with the muscle quantitatively the major site for this synthetic pathway. The liver, kidney, pancreas, and skeletal muscle of 15- to 150-g HSB contained all the enzymes for creatine synthesis, but the enzymatic activities were the greatest in the skeletal muscle. This metabolic feature in HSB differs remarkably from that in terrestrial animals (e.g., pigs and chickens), where creatine synthesis is absent from skeletal muscle but occurs through the interorgan cooperation of the kidney and liver and pancreas. The stomach, proximal intestine, heart, gill, skin, spleen, and brain of 15- to 150-g HSB could not produce creatine from 2 mM arginine plus 2 mM glycine plus 2 mM methionine.

Publications

  • Type: Journal Articles Status: Published Year Published: 2022 Citation: Wu, G. and P. Li. 2022. The ideal protein concept is not ideal in animal nutrition. Exp. Biol. Med. 247:11911201.