Abstract
During the mouth-opening stage, fish larvae are susceptible to delayed first feeding (DFF). In this study, we explored the effects of DFF for two days on later growth and energy metabolism in larval fish. Results showed that DFF chronically impaired larval growth performance, thereby reducing the efficiency of feed utilization by larvae. In DFF larvae, the mRNA levels of growth inhibitors (i.e., igfbp1a and igfbp1b) were significantly upregulated and consistently maintained at high expression levels, which may be an important attribution of larval growth retardation. Concomitantly, DFF retarded the growth of adipose tissue and reduced lipid deposition in larval viscera, suggesting lipid metabolism is disordered in DFF larvae and generates inefficient lipid reserves. In the liver, we observed that DFF resulted in a significant accumulation of neutral lipids, and this phenotype did not disappear rapidly after DFF larvae received exogenous nutrition. As to the transcript analyses, we found that the expression of genes related to hepatic lipid synthesis (e.g., srebf1, srebf2, dgat1a, dgat1b, fasn, and scdb) in DFF larvae was consistently upregulated, while the expression of genes involved in lipid transport (e.g., apoa2, apoa4b.1, and apoa4b.3) was downregulated. Therefore, it appears that the inefficient lipid reserves in DFF larvae are associated with their hepatic lipid transport dysfunction. Taken together, our findings contribute to understanding the impairments to fish larvae caused by delayed first feeding during the mouth-opening stage and to aiding larval management in the aquaculture industry.
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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Blaxter JHS, Hempel G (1963) The influence of egg size on herring larvae (Clupea harengus L.). J Cons Int Explor Mer 28:211–240
Brown JD, Horton JD (2004) Molecular mediators of hepatic steatosis and liver injury. J Clin Investig 114:147–152
Cahill GF Jr (2006) Fuel metabolism in starvation. Annu Rev Nutr 26:1–22
China V, Holzman R (2014) Hydrodynamic starvation in first feeding larval fishes. Proc Natl Acad Sci U S A 111:8083–8088
Ching FF, Nakagawa Y, Kato K, Murata O, Miyashita S (2012) Effects of delayed first feeding on the survival and growth of tiger grouper, epinephelus fuscoguttatus (forsskål, 1775), larvae. Aquac Res 43:303–310
Choi CS, Ghoshal P, Srinivasan M, Kim S, Cline G, Patel MS (2010) Liver-specific pyruvate dehydrogenase complex deficiency upregulates lipogenesis in adipose tissue and improves peripheral insulin sensitivity. Lipids 45:987–995
Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306–314
Fan XT, Wang LJ, Wei XF, Zhang J, Su XY, Cui L, Wang ZZ (2021) The impairment of continuous malnutrition on larval fish swimming performance at the mouth-opening stage. Aquaculture 544:737053
Fausten RM, Bohnert M (2021) A move in response to starvation. Elife 10:e69680
Flynn EJ, Trent CM, Rawls JF (2009) Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). J Lipid Res 50:1641–1652
Geng XF, Guo JL, Zhang L, Sun JY, Zang XY, Qiao ZG, Xu CS (2020) Differential proteomic analysis of Chinese Giant Salamander liver in response to fasting. Front Physiol 11:208
Greenspan P, Fowler SD (1985) Spectrofluorometric studies of the lipid probe, Nile red. J Lipid Res 26:781–789
Gu Q, Yang X, Lin L, Li S, Li Q, Zhong S, Peng J, Cui Z (2014) Genetic ablation of solute carrier family 7a3a leads to hepatic steatosis in zebrafish during fasting. Hepatology 60:1929–1941
Guevara-Aguirre J (1996) Insulin-like growth factor I–an important intrauterine growth factor. N Engl J Med 335:1389–1391
He Z, Agostini M, Liu H, Melino G, Simon HU (2015) p73 regulates basal and starvation-induced liver metabolism in vivo. Oncotarget 6:33178–33190
Jones JG (2016) Hepatic glucose and lipid metabolism. Diabetologia 59:1098–1103
Kajimura S, Aida K, Duan CM (2005) Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci U S A 102:1240–1245
Kamei H, Lu L, Jiao S, Li Y, Gyrup C, Laursen LS, Oxvig C, Zhou JF, Duan CM (2008) Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS ONE 3:e3091
Kim DH, Jung IH, Kim DH, Park SW (2019) Knockout of longevity gene Sirt1 in zebrafish leads to oxidative injury, chronic inflammation, and reduced life span. PLoS ONE 14:e0220581
Kolb H, Kempf K, Röhling M, Lenzen-Schulte M, Schloot NC, Martin S (2021) Ketone bodies: from enemy to friend and guardian angel. BMC Med 19:313
Lee J, Choi J, Scafidi S, Wolfgang MJ (2016) Hepatic fatty acid oxidation restrains systemic catabolism during starvation. Cell Rep 16:201–212
Li JZ, Chu LH, Sun X, Liu Y, Cheng CHK (2015) IGFs mediate the action of LH on oocyte maturation in zebrafish. Mol Endocrinol 29:373–383
Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59–72
Liu Q, Bengmark S, Qu S (2010) The role of hepatic fat accumulation in pathogenesis of non-alcoholic fatty liver disease (NAFLD). Lipid Health Dis 9:42
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆Ct method. Methods 25:402–408
Long Y, Song G, Yan J, He X, Li Q, Cui Z (2013) Transcriptomic characterization of cold acclimation in larval zebrafish. BMC Genomics 14:612
Louvi A, Accili D, Efstratiadis A (1997) Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol 189:33–48
Maures T, Chan SJ, Xu B, Sun HS, Ding J, Duan CM (2002) Structural, biochemical, and expression analysis of two distinct insulin-like growth factor I receptors and their ligands in zebrafish. Endocrinology 143:1858–1871
Mazurais D, Darias M, Zambonino-Infante JL, Cahu CL (2011) Transcriptomics for understanding marine fish larval development. Can J Zool 89:599–611
Mcgarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244:1–14
Minchin JEN, Rawls JF (2017) A classification system for zebrafish adipose tissues. Dis Model Mech 10:797–809
Qian B, Xue L, Huang H (2016) Liver transcriptome analysis of the Large yellow croaker (Larimichthys crocea) during fasting by using RNA-seq. PLoS ONE 11:e0150240
Quinlivan VH, Farber SA (2017) Lipid uptake, metabolism, and transport in the larval zebrafish. Front Endocrinol 8:319
Reinecke M, Björnsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutiérrez J (2005) Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142:20–24
Salmerón C (2018) Adipogenesis in fish. J Exp Biol 221:jeb161588
Sapp V, Gaffney L, EauClaire SF, Matthews RP (2014) Fructose leads to hepatic steatosis in zebrafish that is reversed by mechanistic target of rapamycin (mTOR) inhibition. Hepatology 60:1581–1592
Shan X, Quan H, Dou S (2008) Effects of delayed first feeding on growth and survival of rock bream Oplegnathus fasciatus larvae. Aquaculture 277:14–23
Uhal BD, Roehrig KL (1982) Effect of dietary state on hepatocyte size. Bioscience Rep 2:1003–1007
Xie L, Tao YX, Wu RH, Ye Q, Xu H, Li Y (2019) Congenital asplenia due to a tlx1 mutation reduces resistance to Aeromonas hydrophila infection in zebrafish. Fish Shellfish Immunol 95:538–545
Xu H, Fan SQ, Wang G, Miao XM, Li Y (2021a) Transcriptome analysis reveals the importance of exogenous nutrition in regulating antioxidant defenses during the mouth-opening stage in oviparous fish. Fish Physiol Biochem 47:1087–1103
Xu H, Jiang Y, Miao XM, Tao YX, Xie L, Li Y (2021b) A model construction of starvation induces hepatic steatosis and transcriptome analysis in zebrafish larvae. Biology (Basel) 10:29
Xu H, Liu EX, Li Y, Li XJ, Ding CY (2017) Transcriptome analysis reveals increases in visceral lipogenesis and storage and activation of the antigen processing and presentation pathway during the mouth-opening stage in zebrafish larvae. Int J Mol Sci 18:1634
Yoseda K, Dan S, Sugaya T, Yokogi K, Tanaka M, Tawada S (2006) Effects of temperature and delayed initial feeding on the growth of Malabar grouper (Epinephelus malabaricus) larvae. Aquaculture 256:192–200
Zhang WF, Wu CY, Ni R, Yang QF, Luo LF, He JB (2021) Formimidoyltransferase cyclodeaminase prevents the starvation-induced liver hepatomegaly and dysfunction through downregulating mTORC1. PLoS Genet 17:e1009980
Funding
This work was supported by a grant from the Fundamental Research Funds for the Central Universities (NO. SWU-KQ22015) and the Chongqing Aquatic Science and Technology Innovation Alliance (NO. 4322200053).
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Hao Xu and Yun Li designed and conceived the whole experiment. Hao Xu conducted the experiments, collated the data, and wrote the original. Wenbo Wang provided guidance on methods and software and checked the manuscript. Xiaomin Miao provided help with conceptualization and methodology. Zhentao Nie and Hao Xu provided the experimental sample and supervision. Yun Li provided guidance on methods, conception, writing, and project support and checked the manuscript. All authors read and approved the final manuscript.
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All animal experiments were performed in accordance with the guiding principles for the Care and Use of Laboratory Animals and were approved by the Committee for Laboratory Animal Experimentation at Southwest University, China (Approval ID: 2021112601).
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Xu, H., Wang, W., Nie, Z. et al. Delayed First Feeding Chronically Impairs Larval Fish Growth Performance, Hepatic Lipid Metabolism, and Visceral Lipid Deposition at the Mouth-Opening Stage. Mar Biotechnol 25, 140–149 (2023). https://doi.org/10.1007/s10126-022-10187-z
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DOI: https://doi.org/10.1007/s10126-022-10187-z