Effects of Tributyrin Supplementation on Growth Performance, Intestinal Digestive Enzyme Activity, Antioxidant Capacity, and Inflammation-Related Gene Expression of Large Yellow Croaker (Larimichthys crocea) Fed with a High Level of Clostridium autoethanogenum Protein

An 8-week growth experiment was conducted to investigate effects of tributyrin (TB) supplementation on growth performance, intestinal digestive enzyme activity, antioxidant capacity, and inflammation-related gene expression of juvenile large yellow croaker (Larimichthys crocea) (initial weight of 12.90 ± 0.02 g) fed diets with high level of Clostridium autoethanogenum protein (CAP). In the negative control diet, 40% fish meal was used as the major source of protein (named as FM), while 45% fish meal protein of FM was substituted with CAP (named as FC) to form a positive control diet. Based on the FC diet, grade levels of 0.05%, 0.1%, 0.2%, 0.4%, and 0.8% tributyrin were added to formulate other five experimental diets. Results showed that fish fed diets with high levels of CAP significantly decreased the weight gain rate (WGR) and specific growth rate (SGR) compared with fish fed the FM diet (P < 0.05). WGR and SGR were significantly higher than in fish fed diets with 0.05% and 0.1% tributyrin that fed the FC diet (P < 0.05). Supplementation of 0.1% tributyrin significantly elevated fish intestinal lipase and protease activities compared to FM and FC diets (P < 0.05). Meanwhile, compared to fish fed the FC diet, fish fed diets with 0.05% and 0.1% tributyrin showed remarkably higher intestinal total antioxidant capacity (T-AOC). Malondialdehyde (MDA) content in the intestine of fish fed diets with 0.05%-0.4% tributyrin was remarkably lower than those in the fish fed the FC diet (P < 0.05). The mRNA expressions of tumor necrosis factor α (tnfα), interleukin-1β (il-1β), interleukin-6 (il-6), and interferon γ (ifnγ) were significantly downregulated in fish fed diets with 0.05%-0.2% tributyrin, and the mRNA expression of il-10 was significantly upregulated in fish fed the 0.2% tributyrin diet (P < 0.05). In regard to antioxidant genes, as the supplementation of tributyrin increased from 0.05% to 0.8%, the mRNA expression of nuclear factor erythroid 2-related factor 2 (nrf2) demonstrated a trend of first rising and then decreasing. However, the mRNA expression of Kelch-like ECH-associated protein 1 (keap1) was remarkably lower in fish fed the FC diet than that fed diets with tributyrin supplementation (P < 0.05). Overall, fish fed tributyrin supplementation diets can ameliorate the negative effects induced by high proportion of CAP in diets, with an appropriate supplementation of 0.1%.

[1]  K. Mai,et al.  Replacement of dietary fish meal with Clostridium autoethanogenum meal on growth performance, intestinal amino acids transporters, protein metabolism and hepatic lipid metabolism of juvenile turbot (Scophthalmus maximus L.) , 2022, Frontiers in Physiology.

[2]  K. Mai,et al.  Effects of dietary lysolecithin on growth performance, serum biochemical indexes, antioxidant capacity, lipid metabolism and inflammation-related genes expression of juvenile large yellow croaker (Larimichthys crocea). , 2022, Fish & shellfish immunology.

[3]  K. Mai,et al.  Nrf2 pathway in vegetable oil-induced inflammation of large yellow croaker (Larimichthys crocea). , 2022, Fish & shellfish immunology.

[4]  M. Yandigeri,et al.  Use of black soldier fly (Hermetia illucens) prepupae reared on organic waste as feed or as an ingredient in a pellet-feed formulation for Nile tilapia (Oreochromis niloticus) , 2022, Environmental Science and Pollution Research.

[5]  M. Longshaw,et al.  Evaluation of methanotroph (Methylococcus capsulatus, Bath) bacteria meal as an alternative protein source for growth performance, digestive enzymes, and health status of Pacific white shrimp (Litopenaeus vannamei) , 2022, Aquaculture International.

[6]  Wenbing Zhang,et al.  Effects of dietary vitamin E supplementation on growth, feed utilization and flesh quality of large yellow croaker Larimichthys crocea fed with different levels of dietary yellow mealworm Tenebrio molitor meal , 2022, Aquaculture.

[7]  Wenbing Zhang,et al.  Effects of Clostridium autoethanogenum protein as substitute for dietary fishmeal on the growth, feed utilization, intestinal health and muscle quality of large yellow croaker Larimichthys crocea , 2022, Aquaculture.

[8]  Dong Han,et al.  Effects of Dietary Inclusion of Clostridium autoethanogenum Protein on the Growth Performance and Liver Health of Largemouth Bass (Micropterus salmoides) , 2021, Frontiers in Marine Science.

[9]  X. Leng,et al.  Dietary effects of Clostridium autoethanogenum protein substituting fish meal on growth, intestinal histology and immunity of Pacific white shrimp (Litopenaeus vannamei) based on transcriptome analysis. , 2021, Fish & shellfish immunology.

[10]  X. Leng,et al.  The potential of Clostridium autoethanogenum, a new single cell protein, in substituting fish meal in the diet of largemouth bass (Micropterus salmoides): Growth, feed utilization and intestinal histology , 2021 .

[11]  K. Mai,et al.  Effects of High Levels of Dietary Linseed Oil on the Growth Performance, Antioxidant Capacity, Hepatic Lipid Metabolism, and Expression of Inflammatory Genes in Large Yellow Croaker (Larimichthys crocea) , 2021, Frontiers in Physiology.

[12]  K. Mai,et al.  Effects of dietary tributyrin on growth performance, body composition, serum biochemical indexes and lipid metabolism‐related genes expression of juvenile large yellow croaker ( Larimichthys crocea ) fed with high level soybean oil diets , 2020, Aquaculture Nutrition.

[13]  Yuanyou Li,et al.  Dietary tributyrin modifies intestinal function by altering morphology, gene expression and microbiota profile in common carp ( Cyprinus carpio ) fed all‐plant diets , 2020 .

[14]  X. Zou,et al.  A STAT3 palmitoylation cycle promotes TH17 differentiation and colitis , 2020, Nature.

[15]  Bao Lou,et al.  Supplementation of a soybean oil-based diet with tributyrin influences growth, muscle composition, intestinal morphology, and expression of immune-related genes of juvenile yellow drum (Nibea albiflora Richardson, 1846) , 2020, Aquaculture International.

[16]  Yun Wang,et al.  Effect of dietary sodium butyrate on growth performance, enzyme activities and intestinal proliferation‐related gene expression of juvenile golden pompanoTrachinotus ovatus , 2019, Aquaculture Nutrition.

[17]  Wenbing Zhang,et al.  Replacement of dietary fishmeal by Antarctic krill meal on growth performance, intestinal morphology, body composition and organoleptic quality of large yellow croaker Larimichthys crocea , 2019, Aquaculture.

[18]  E. Márquez‐Ríos,et al.  Advances in the use of alternative protein sources for tilapia feeding , 2019 .

[19]  Wenbing Zhang,et al.  Sodium butyrate supplementation in high‐soybean meal diets for turbot (Scophthalmus maximus L.): Effects on inflammatory status, mucosal barriers and microbiota in the intestine , 2019, Fish & shellfish immunology.

[20]  Lei Wang,et al.  Tributyrin‐supplemented high‐soya bean meal diets of juvenile black sea bream, Acanthopagrus schlegelii : Study on growth performance and intestinal morphology and structure , 2019, Aquaculture Research.

[21]  Xun Wu,et al.  Effects of dietary sodium butyrate on growth, diet conversion, body chemical compositions and distal intestinal health in yellow drum ( Nibea albiflora , Richardson) , 2019, Aquaculture Research.

[22]  Chunchun Wang,et al.  Dietary Tributyrin Attenuates Intestinal Inflammation, Enhances Mitochondrial Function, and Induces Mitophagy in Piglets Challenged with Diquat. , 2019, Journal of agricultural and food chemistry.

[23]  Yanbin Hou,et al.  Effects of chromium yeast, tributyrin and bile acid on growth performance, digestion and metabolism of Channa argus , 2018, Aquaculture Research.

[24]  H. Dai,et al.  Sodium butyrate improves antioxidant stability in sub-acute ruminal acidosis in dairy goats , 2018, BMC Veterinary Research.

[25]  J. Felip,et al.  Comparison of Tributyrin and Coated Sodium Butyrate as Sources of Butyric Acid for Improvement of Growth Performance in Ross 308 Broilers , 2018 .

[26]  L. Tang,et al.  Sodium butyrate enhanced physical barrier function referring to Nrf2, JNK and MLCK signaling pathways in the intestine of young grass carp (Ctenopharyngodon idella) , 2018, Fish & shellfish immunology.

[27]  J. Gong,et al.  Implications of butyrate and its derivatives for gut health and animal production , 2017, Animal nutrition.

[28]  S. Cooke,et al.  A comparative and evolutionary approach to oxidative stress in fish: A review , 2017 .

[29]  L. Tang,et al.  Sodium butyrate improved intestinal immune function associated with NF‐&kgr;B and p38MAPK signalling pathways in young grass carp (Ctenopharyngodon idella) , 2017, Fish & shellfish immunology.

[30]  Lili Zhang,et al.  Supplementation of tributyrin improves the growth and intestinal digestive and barrier functions in intrauterine growth-restricted piglets. , 2016, Clinical nutrition.

[31]  Joseph D. Donovan,et al.  Volatile Retention and Morphological Properties of Microencapsulated Tributyrin Varied by Wall Material and Drying Method. , 2016, Journal of food science.

[32]  Javid Iqbal,et al.  Recent advances in the role of organic acids in poultry nutrition , 2016 .

[33]  Sagar M. Utturkar,et al.  Sequence data for Clostridium autoethanogenum using three generations of sequencing technologies , 2015, Scientific Data.

[34]  S. Calsamiglia,et al.  Effect of sodium butyrate administered in the concentrate on rumen development and productive performance of lambs in intensive production system during the suckling and the fattening periods , 2014 .

[35]  G. Cresci,et al.  Tributyrin supplementation protects mice from acute ethanol-induced gut injury. , 2014, Alcoholism, clinical and experimental research.

[36]  Zhigang Zhou,et al.  Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidised oil , 2014, British Journal of Nutrition.

[37]  Zhang Chunxiao,et al.  Effects of Tributyrin and Mannan-Oligosaccharide on Growth Performance,Body Composition and Intestinal Health Indices of Tawny Puffer(Takifugu flavindus) , 2014 .

[38]  A. Astrup,et al.  Is butyrate the link between diet, intestinal microbiota and obesity‐related metabolic diseases? , 2013, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[39]  J. Walkowiak,et al.  Butyric acid in functional constipation , 2013, Przeglad gastroenterologiczny.

[40]  F. Moyano,et al.  Effect of partially protected butyrate used as feed additive on growth and intestinal metabolism in sea bream (Sparus aurata) , 2013, Fish Physiology and Biochemistry.

[41]  R. Curi,et al.  Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. , 2012, American journal of physiology. Endocrinology and metabolism.

[42]  R. Zabielski,et al.  Is rumen development in newborn calves affected by different liquid feeds and small intestine development? , 2011, Journal of dairy science.

[43]  R. Meli,et al.  Potential beneficial effects of butyrate in intestinal and extraintestinal diseases , 2011 .

[44]  W. Laurier Aquaculture Nutrition , 2011 .

[45]  Jae-ho Yang Perfluorooctanoic acid induces peroxisomal fatty acid oxidation and cytokine expression in the liver of male Japanese medaka (Oryzias latipes). , 2010, Chemosphere.

[46]  V. Loro,et al.  Protein sources and digestive enzyme activities in jundiá (Rhamdia quelen) , 2010 .

[47]  Y. S. D. Mitcheson,et al.  Profile of a fishery collapse: why mariculture failed to save the large yellow croaker , 2008 .

[48]  Yuming Guo,et al.  Effects of dietary sodium butyrate supplementation on the intestinal morphological structure, absorptive function and gut flora in chickens , 2007 .

[49]  Wei Xu,et al.  Replacement of fish meal by meat and bone meal in diets for large yellow croaker, Pseudosciaena crocea , 2006 .

[50]  J. Galmiche,et al.  Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation , 2003, Proceedings of the Nutrition Society.

[51]  J. Galmiche,et al.  Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. , 2000, Gut.

[52]  Hata,et al.  Counter‐regulatory effect of sodium butyrate on tumour necrosis factor‐alpha (TNF‐α)‐induced complement C3 and factor B biosynthesis in human intestinal epithelial cells , 1999, Clinical and experimental immunology.

[53]  E. N. Bergman Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. , 1990, Physiological reviews.