Effects of moderate exercise on hepatic amino acid and fatty acid composition, liver transcriptome, and intestinal microbiota in channel catfish (Ictalurus punctatus)

Amagai, 2015, Dihomo-γ-linolenic acid prevents the development of atopic dermatitis through prostaglandin D1 production in NC/Tnd mice, J. Dermatol. Sci., 79, 30, 10.1016/j.jdermsci.2015.03.010 Andreelli, 2006, Liver adenosine monophosphate-activated kinase-alpha 2 catalytic subunit is a key target for the control of hepatic glucose production by adiponectin and leptin but not insulin, Endocrinology, 147, 2432, 10.1210/en.2005-0898 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics (Oxford, England), 30, 2114 Brown, 2011, Do swimming fish always grow fast? Investigating the magnitude and physiological basis of exercise-induced growth in juvenile New Zealand yellowtail kingfish, Seriola lalandi, Fish Physiol. Biochem., 37, 327, 10.1007/s10695-011-9500-5 Brown, 2016, Mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) and serine biosynthetic pathway genes are co-ordinately increased during anabolic agent-induced skeletal muscle growth, Sci. Rep., 6, 28693, 10.1038/srep28693 Charlton, 2006, Branched-chain amino acid enriched supplements as therapy for liver disease, J. Nutr., 136, 295s, 10.1093/jn/136.1.295S Dai, 2011, Amino acid metabolism in intestinal bacteria: links between gut ecology and host health, Front. Biosci. (Landmark Ed.), 16, 1768, 10.2741/3820 Dai, 2015, Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction, Mol. Hum. Reprod., 21, 389, 10.1093/molehr/gav003 de Antueno, 2001, Activity of human Δ5 and Δ6 desaturases on multiple n-3 and n-6 polyunsaturated fatty acids, FEBS Lett., 509, 77, 10.1016/S0014-5793(01)03135-0 Dermaku-Sopjani, 2014, AMPK-sensitive cellular transport, J. Biochem., 155, 147, 10.1093/jb/mvu002 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics (Oxford, England), 29, 15 Duan, 2018, The functional properties and application of gelatin derived from the skin of channel catfish (Ictalurus punctatus), Food Chem., 239, 464, 10.1016/j.foodchem.2017.06.145 Enes, 2009, Nutritional regulation of hepatic glucose metabolism in fish, Fish Physiol. Biochem., 35, 519, 10.1007/s10695-008-9259-5 Fenkes, 2016, The potential impacts of migratory difficulty, including warmer waters and altered flow conditions, on the reproductive success of salmonid fishes, Comp. Biochem. Physiol. A Mol. Integr. Physiol., 193, 11, 10.1016/j.cbpa.2015.11.012 Fouts, 2012, Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen, PLoS One, 7, 10.1371/journal.pone.0048289 Grigorakis, 2007, Compositional and organoleptic quality of farmed and wild gilthead sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax) and factors affecting it: a review, Aquaculture, 272, 55, 10.1016/j.aquaculture.2007.04.062 Hardy, 2010, 31, 43 Harimana, 2019, Effect of long-term moderate exercise on muscle cellularity and texture, antioxidant activities, tissue composition, freshness indicators and flavor characteristics in largemouth bass (Micropterus salmoides), Aquaculture, 510, 100, 10.1016/j.aquaculture.2019.05.051 Hemre, 2002, Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes, Aquac. Nutr., 8, 175, 10.1046/j.1365-2095.2002.00200.x Hullar, 2014, Diet, the gut microbiome, and epigenetics, Cancer J., 20, 170, 10.1097/PPO.0000000000000053 Ibarz, 2011, Sustained swimming improves muscle growth and cellularity in gilthead sea bream, J. Comp. Physiol. B, 181, 209, 10.1007/s00360-010-0516-4 Jang, 2019, Effects of probiotic supplementation of a plant-based protein diet on intestinal microbial diversity, digestive enzyme activity, intestinal structure, and immunity in olive flounder (Paralichthys olivaceus), Fish Shellfish Immunol, 92, 719, 10.1016/j.fsi.2019.06.056 Jiang, 2001, Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1, Cell growth Differ., 12, 363 Jiang, 2020, Liver transcriptome analysis and cortisol immune-response modulation in lipopolysaccharide-stimulated in channel catfish (Ictalurus punctatus), Fish Shellfish Immunol., 101, 19, 10.1016/j.fsi.2020.03.024 Jin, 2017, Effects of environmental pollutants on gut microbiota, Environ. Pollut., 222, 1, 10.1016/j.envpol.2016.11.045 Kamalam, 2017, Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies, Aquaculture, 467, 3, 10.1016/j.aquaculture.2016.02.007 Keenan, 2011 Khan, 2014, Accommodating the cost of growth and swimming in fish-the applicability of exercise-induced growth to juvenile hapuku (Polyprion oxygeneios), Front. Physiol., 5, 10.3389/fphys.2014.00448 Kielak, 2016, The ecology of acidobacteria: moving beyond genes and genomes, Front. Microbiol., 7, 744, 10.3389/fmicb.2016.00744 Kiessling, 2005, Age, ration level, and exercise affect the fatty acid profile of Chinook salmon (Oncorhynchus tshawytscha) muscle differently, Aquaculture, 243, 345, 10.1016/j.aquaculture.2004.10.003 Klase, 2019, The microbiome and antibiotic resistance in integrated fishfarm water: implications of environmental public health, Sci. Total Environ., 649, 1491, 10.1016/j.scitotenv.2018.08.288 Koletzko, 2019, FADS1 and FADS2 polymorphisms modulate fatty acid metabolism and dietary impact on health, Annu. Rev. Nutr., 39, 21, 10.1146/annurev-nutr-082018-124250 Kozich, 2013, Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform, Appl. Environ. Microbiol., 79, 5112, 10.1128/AEM.01043-13 Lattka, 2010, Genetic variants of the FADS1 FADS2 gene cluster as related to essential fatty acid metabolism, Curr. Opin. Lipidol., 21, 64, 10.1097/MOL.0b013e3283327ca8 Li, 2010, Cancer therapy by targeting hypoxia-inducible factor-1, Curr. Cancer Drug Targets, 10, 782, 10.2174/156800910793605857 Li, 2013, The effect of aerobic exercise training on growth performance, digestive enzyme activities and postprandial metabolic response in juvenile qingbo (Spinibarbus sinensis), Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 166, 8, 10.1016/j.cbpa.2013.04.021 Li, 2016, The effect of sustained swimming exercise on the growth performance, muscle cellularity and flesh quality of juvenile qingbo (Spinibarbus sinensis), Aquaculture, 465, 287, 10.1016/j.aquaculture.2016.09.021 Liao, 2014, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics (Oxford, England), 30, 923 Liu, 2016, The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts, Nat. Commun., 7, 11757, 10.1038/ncomms11757 Lu, 2021, Generation of knockout and transgenic zebrafish to characterize Abcc4 functions in detoxification and efflux of Lead, Int. J. Mol. Sci., 22, 2054, 10.3390/ijms22042054 Magnoni, 2012, AMP-activated protein kinase plays an important evolutionary conserved role in the regulation of glucose metabolism in fish skeletal muscle cells, PLoS One, 7, 10.1371/journal.pone.0031219 Marques, 2008, Transcriptome analysis of the response to chronic constant hypoxia in zebrafish hearts, J. Comp. Physiol. B., 178, 77, 10.1007/s00360-007-0201-4 Marszalek, 2005, Docosahexaenoic acid, fatty acid-interacting proteins, and neuronal function: breastmilk and fish are good for you, Annu. Rev. Cell Dev. Biol., 21, 633, 10.1146/annurev.cellbio.21.122303.120624 Martinez, 1992, Tissue levels of polyunsaturated fatty acids during early human development, J. Pediatr., 120, S129, 10.1016/S0022-3476(05)81247-8 Metón, 1999, Effect of diet composition and ration size on key enzyme activities of glycolysis-gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata), Br. J. Nutr., 82, 223, 10.1017/S0007114599001403 Moon, 2001, Identification of a mammalian long chain fatty acyl elongase regulated by sterol regulatory element-binding proteins, J. Biol. Chem., 276, 45358, 10.1074/jbc.M108413200 Morale, 2005, Duration of long-chain polyunsaturated fatty acids availability in the diet and visual acuity, Early Hum. Dev., 81, 197, 10.1016/j.earlhumdev.2004.09.008 Moriwaki, 2004, Branched-chain amino acids as a protein- and energy-source in liver cirrhosis, Biochem. Biophys. Res. Commun., 313, 405, 10.1016/j.bbrc.2003.07.016 Nayak, 2010, Role of gastrointestinal microbiota in fish, Aquac. Res., 41, 1553, 10.1111/j.1365-2109.2010.02546.x Ngoc Tuan, 2018, Altered gut microbiota associated with intestinal disease in grass carp (Ctenopharyngodon idellus), World J. Microbiol. Biotechnol., 34 Nguyen, 2008, Liver lipid metabolism, J. Anim. Physiol. Anim. Nutr., 92, 272, 10.1111/j.1439-0396.2007.00752.x Nilsen, 2017, The prognostic utility of dihomo-gamma-linolenic acid (DGLA) in patients with acute coronary heart disease, Int. J. Cardiol., 249, 12, 10.1016/j.ijcard.2017.09.202 Nunes, 2013, Growth and hematology of pacu subjected to sustained swimming and fed different protein levels, Pesq. Agrop. Brasileira, 48, 645, 10.1590/S0100-204X2013000600010 O'Neill, 2013, AMPK and exercise: glucose uptake and insulin sensitivity, Diabetes Metab. J., 37, 1, 10.4093/dmj.2013.37.1.1 Ortí, 2019, Special issue on fish transcriptomics, Genomics, 111, 213, 10.1016/j.ygeno.2019.05.014 Palstra, 2010, Establishing zebrafish as a novel exercise model: swimming economy, swimming-enhanced growth and muscle growth marker gene expression, PLos One, 5, 10.1371/journal.pone.0014483 Palstra, 2015, Forced sustained swimming exercise at optimal speed enhances growth of juvenile yellowtail kingfish (Serbia lalandi), Front. Physiol., 5, 10.3389/fphys.2014.00506 Pereboom, 2014, Translation of branched-chain aminotransferase-1 transcripts is impaired in cells haploinsufficient for ribosomal protein genes, Exp. Hematol., 42, 394, 10.1016/j.exphem.2013.12.010 Robinson, 2010, edgeR: a bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Sanchez-Gurmaches, 2013, Insulin, IGF-I, and muscle MAPK pathway responses after sustained exercise and their contribution to growth and lipid metabolism regulation in gilthead sea bream, Domest. Anim. Endocrinol., 45, 145, 10.1016/j.domaniend.2013.08.001 Sawai, 2017, The 3-hydroxyacyl-CoA dehydratases HACD1 and HACD2 exhibit functional redundancy and are active in a wide range of fatty acid elongation pathways, J. Biol. Chem., 292, 15538, 10.1074/jbc.M117.803171 Schloss, 2011, Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies, PLoS One, 6, 10.1371/journal.pone.0027310 Semova, 2012, Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish, Cell Host Microbe, 12, 277, 10.1016/j.chom.2012.08.003 Shengming, 2016, Comparative proteomic study of the response to hypoxia in the muscle of oriental river prawn (Macrobrachium nipponense), J. Proteome, 138, 115, 10.1016/j.jprot.2016.02.023 Shi, 2015, Investigation of intertidal wetland sediment as a novel inoculation source for anaerobic saline wastewater treatment, Environ. Sci. Technol., 49, 6231, 10.1021/acs.est.5b00546 Shrivastava, 2018, Exercise improves growth, alters physiological performance and gene expression in common carp (Cyprinus carpio), Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 226, 38, 10.1016/j.cbpa.2018.08.007 Smith, 1989, Eskimo plasma constituents, dihomo-gamma-linolenic acid, eicosapentaenoic acid and docosahexaenoic acid inhibit the release of atherogenic mitogens, Lipids, 24, 70, 10.1007/BF02535267 Song, 2012, Effects of upstream exercise training on feeding efficiency, growth and nutritional components of juvenile tinfoil barbs(Barbodes schwanenfeldi ), J. Fish. China, 36, 105, 10.3724/SP.J.1231.2012.27597 Sossai, 2012, Butyric acid: what is the future for this old substance?, Swiss. Med Wkly., 142, 1 Stevens, 2004 Thurlow, 2019, Bacillus velezensis AP193 exerts probiotic effects in channel catfish (Ictalurus punctatus) and reduces aquaculture pond eutrophication, Aquaculture, 503, 347, 10.1016/j.aquaculture.2018.11.051 Titchenell, 2017, Unraveling the regulation of hepatic metabolism by insulin, Trends Endocrinol. Metab., 28, 497, 10.1016/j.tem.2017.03.003 Tiwari, 2012, Intracellular trafficking and secretion of VLDL, Arterioscler. Thromb. Vasc. Biol., 32, 1079, 10.1161/ATVBAHA.111.241471 Umeda-Sawada, 2006, Distribution and metabolism of dihomo-gamma-linolenic acid (DGLA, 20:3n–6) by oral supplementation in rats, Biosci. Biotechnol. Biochem., 70, 2121, 10.1271/bbb.60057 Vaittinen, 2016, FADS2 genotype regulates delta-6 desaturase activity and inflammation in human adipose tissue, J. Lipid Res., 57, 56, 10.1194/jlr.M059113 Viollet, 2009, Targeting the AMPK pathway for the treatment of type 2 diabetes, Front. Biosci. Landmark, 14, 3380-+, 10.2741/3460 Viollet, 2010, AMPK inhibition in health and disease, Crit. Rev. Biochem. Mol. Biol., 45, 276, 10.3109/10409238.2010.488215 Wang, 2005, Characterization of HSCD5, a novel human stearoyl-CoA desaturase unique to primates, Biochem. Biophys. Res. Commun., 332, 735, 10.1016/j.bbrc.2005.05.013 Wang, 2012, Multiple roles of dihomo-γ-linolenic acid against proliferation diseases, Lipids Health Dis., 11, 25, 10.1186/1476-511X-11-25 Wang, 2019, Consumption of florfenicol-medicated feed alters the composition of the channel catfish intestinal microbiota including enriching the relative abundance of opportunistic pathogens, Aquaculture, 501, 111, 10.1016/j.aquaculture.2018.11.019 Wu, 2006, KOBAS server: a web-based platform for automated annotation and pathway identification, Nucleic Acids Res., 34, W720, 10.1093/nar/gkl167 Wu, 2016, The effects of dietary carbohydrate on the growth, antioxidant capacities, innate immune responses and pathogen resistance of juvenile black carp Mylopharyngodon piceus, Fish Shellfish Immunol., 49, 132, 10.1016/j.fsi.2015.12.030 Xiao, 2015, The hypoxia signaling pathway and hypoxic adaptation in fishes, Sci. China Life Sci., 58, 148, 10.1007/s11427-015-4801-z Xu, 2007, A BAC-based physical map of the channel catfish genome, Genomics, 90, 380, 10.1016/j.ygeno.2007.05.008 Xu, 2020, Transcriptome analysis revealed changes of multiple genes involved in muscle hardness in grass carp (Ctenopharyngodon idellus) fed with faba bean meal, Food Chem., 314, 126205-, 10.1016/j.foodchem.2020.126205 Yao, 2019, Effects of hexavalent chromium on intestinal histology and microbiota in Bufo gargarizans tadpoles, Chemosphere, 216, 313, 10.1016/j.chemosphere.2018.10.147 Zhang, 2017, glyA gene knock-out in Escherichia coli enhances L-serine production without glycine addition, Biotechnol. Bioprocess Eng., 22, 390, 10.1007/s12257-017-0084-5 Zhang, 2020, Transcriptional response of zebrafish larvae exposed to lindane reveals two detoxification genes of ABC transporter family (abcg5 and abcg8), Comp. Biochem. Physiol. C: Toxicol. Pharmacol., 232, 15 Zhu, 2013, Strategies for hypoxia adaptation in fish species: a review, J. Comp. Physiol. B, 183, 1005, 10.1007/s00360-013-0762-3