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Intestinal metabolomics of juvenile lenok (Brachymystax lenok) in response to heat stress

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Abstract

Changes in the metabolic profile within the intestine of lenok (Brachymystax lenok) when challenged to acute and lethal heat stress (HS) are studied using no-target HPLC–MS/MS metabonomic analysis. A total of 51 differentially expressed metabolites (VIP > 1, P < 0.05) were identified in response to HS, and 34 occurred in the positive ion mode and 17 in negative ion mode, respectively. After heat stress, changes in metabolites related to glycolysis (i.e., alpha-D-glucose, stachyose, and L-lactate) were identified. The metabolites (acetyl carnitine, palmitoylcarnitine, carnitine, and erucic acid) related to fatty acid β-oxidation accumulated significantly, and many amino acids (L-tryptophan, D-proline, L-leucine, L-phenylalanine, L-aspartate, L-tyrosine, L-methionine, L-histidine, and L-glutamine) were significantly decreased in HS-treated lenok. The mitochondrial β-oxidation pathway might be inhibited, while severe heat stress might activate the anaerobic glycolysis and catabolism of amino acid for energy expenditure. Oxidative damage in HS-treated lenok was indicated by the decreased glycerophospholipid metabolites (i.e., glycerophosphocholine, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine, 1-palmitoyl-sn-glycero-3-phosphocholine, 1-stearoyl-2-oleoyl-sn-glycero-3-phosphocholine, and 1, 2-dioleoyl-sn-glycero-3-phosphatidylcholine) and the increased oxylipin production (12-HETE and 9R, 10S-EpOME). The minor oxidative pathways (omega-oxidation and peroxisomal beta-oxidation) were likely to be induced in HS-treated lenok.

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Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

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References

  • Baldissera MD, Souza CF, Bottari NB, Verdi CM, Santos RCV, Vizzotto BS, Baldisserotto B (2018) Purinergic signalling displays an anti-inflammatory profile in the spleen of fish experimentally infected with Aeromonas caviae: modulation of the immune response. J Fish Dis 41:683–687

    Article  CAS  PubMed  Google Scholar 

  • Banh S, Wiens L, Sotiri E, Treberg JR (2016) Mitochondrial reactive oxygen species production by fish muscle mitochondria: potential role in acute heat-induced oxidative stress. Comp Biochem Physiol b: Biochem Mol Biol 191:99–107

    Article  CAS  Google Scholar 

  • Chen Y, Liu E, Li C, Pan C, Zhao X, Wang Y, Ling Q (2021) Effects of heat stress on histopathology, antioxidant enzymes, and transcriptomic profiles in gills of pikeperch Sander lucioperca. Aquaculture 534:736277

    Article  CAS  Google Scholar 

  • Clark TD, San Db Lom E, Cox GK, Hinch SG, Farrell AP (2008) Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha). Am J Physiol Regul Integr Comp Physiol 295:R1631-1639

    Article  CAS  PubMed  Google Scholar 

  • Cqza B, Peng ZA, Ylr A, Lhc B, Jlw A (2019) Physiological response and miRNA-mRNA interaction analysis in the head kidney of rainbow trout exposed to acute heat stress. J Therm Biol 83:134–141

    Article  Google Scholar 

  • Duan Y, Xiong D, Wang Y, Li H, Dong H, Zhang J (2021) Toxic effects of ammonia and thermal stress on the intestinal microbiota and transcriptomic and metabolomic responses of Litopenaeus vannamei. Sci Total Environ 754:141867

    Article  CAS  PubMed  Google Scholar 

  • Forgati M, Kandalski PK, Herrerias T, Zaleski T, Machado C, Souza MRDP, Donatti L (2017) Effects of heat stress on the renal and branchial carbohydrate metabolism and antioxidant system of Antarctic fish. J Comp Physiol B 187:1137–1154

    Article  CAS  PubMed  Google Scholar 

  • Guzman-Guillen R, Prieto AI, Vazquez CM, Vasconcelos V, Camean AM (2013) The protective role of L-carnitine against cylindrospermopsin-induced oxidative stress in tilapia (Oreochromis niloticus). Aquat Toxicol 132:141–150

    Article  PubMed  Google Scholar 

  • Hermann BT, Wuertz S, Vanselow KH, Schulz C, Stiller KT (2019) Divergent gene expression in the gills of juvenile turbot (Psetta maxima) exposed to chronic severe hypercapnia indicates dose-dependent increase in intracellular oxidative stress and hypoxia. Aquat Toxicol 206:72–80

    Article  CAS  PubMed  Google Scholar 

  • Hildreth K, Kodani SD, Hammock BD, Zhao L (2020) Cytochrome P450-derived linoleic acid metabolites EpOMEs and DiHOMEs: a review of recent studies. J Nutr Biochem 86:108484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Li Y, Liu Z, Kang Y, Wang J (2018) Transcriptomic responses to heat stress in rainbow trout Oncorhynchus mykiss head kidney. Fish Shellfish Immunol 82:32–40

    Article  CAS  PubMed  Google Scholar 

  • Ikeda K, Prein A, Rasmussen R, Liu C, Holland GJ (2012) Impact of climate change on heavy precipitation events: application of Extreme Value Theory to a Future Climate Simulation over the Colorado Headwaters Region. AGU Fall Meeting Abstracts 2012:A41H-0070

    Google Scholar 

  • Islam MJ, Slater MJ, Kunzmann A (2020) What metabolic, osmotic and molecular stress responses tell us about extreme ambient heatwave impacts in fish at low salinities: the case of European seabass, Dicentrarchus labrax. Sci Total Environ 749:141458

    Article  CAS  PubMed  Google Scholar 

  • Jia S, Li X, Zheng S, Wu G (2017) Amino acids are major energy substrates for tissues of hybrid striped bass and zebrafish. Amino Acids 49:1–11

    Article  Google Scholar 

  • Kang Y, Liu Z, Shi H, Wang J, Huang J, Li Y, Li J, Wang Y (2019) Label-free quantification of protein expression in the rainbow trout (Oncorhynchus mykiss) in response to short-term exposure to heat stress. Comparative biochemistry and physiology. Part d, Genomics & Proteomics 30:158–168

    CAS  Google Scholar 

  • Kaur M, Atif F, Ali M, Rehman H, Raisuddin S (2010) Heat stress-induced alterations of antioxidants in the freshwater fish Channa punctata Bloch. J Fish Biol 67:1653–1665

    Article  Google Scholar 

  • Kibler SR, Tester PA, Kunkel KE, Moore SK, Litaker RW (2015) Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean. Ecol Model 316:194–210

    Article  Google Scholar 

  • Kullgren A, Jutfelt F, Fontanillas R, Sundell K, Samuelsson L, Wiklander K, Kling P, Koppe W, Larsson DJ, Björnsson BT (2013) The impact of temperature on the metabolome and endocrine metabolic signals in Atlantic salmon (Salmo salar). Comp Biochem Physiol a: Mol Integr Physiol 164:44–53

    Article  CAS  Google Scholar 

  • Lardon I, Nilsson GE, Stecyk JA, Vu TN, Laukens K, Dommisse R, De Boeck G (2013) 1 H-NMR study of the metabolome of an exceptionally anoxia tolerant vertebrate, the crucian carp (Carassius carassius). Metabolomics 9:311–323

    Article  CAS  Google Scholar 

  • Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53

    Article  PubMed  Google Scholar 

  • Li JM, Li LY, Zhang YX, Jiang ZY, Limbu SM, Qiao F, Degrace P, Chen LQ, Zhang ML, Du ZY (2019) Functional differences between l- and d-carnitine in metabolic regulation evaluated using a low-carnitine Nile tilapia model. Br J Nutr 122:625–638

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zheng S, Jia S, Song F, Zhou C, Wu G (2020) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1017–1032

    Article  CAS  PubMed  Google Scholar 

  • Li P, Liu Q, Li J, Wang F, Wen S, Li N (2021) Transcriptomic responses to heat stress in gill and liver of endangered brachymystax lenok tsinlingensis. Comp Biochem Physiol d: Genomics Proteomics 38:100791

    CAS  PubMed  Google Scholar 

  • Liu Y, Mou ZB, Xu GF, Li YF (2011) Effects of water temperature on activities of digestive enzymes in juvenile lenok Brachymystax lenok. Chin J Fish 24:6–9 (in Chinese with English abstract)

    Google Scholar 

  • Liu Y, Liu H, Xu G, Mou Z, Yin J (2018) Effects of water temperature on feeding and growth of the lenok Brachymystax lenok (Pallas) with different sizes. J Fish Sci China 25:286–293

    Google Scholar 

  • Logan CA, Somero GN (2011) Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol: Regul Integr Comp Physiol 300(6):R1373-83

    CAS  Google Scholar 

  • Lu Y, Wu Z, Song Z, Xiao P, Liu Y, Zhang P, You F (2016) Insight into the heat resistance of fish via blood: effects of heat stress on metabolism, oxidative stress and antioxidant response of olive flounder Paralichthys olivaceus and turbot Scophthalmus maximus. Fish Shellfish Immunol 58:125–135

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Shi Y, Cai S, Feng J (2017) Metabolic responses of Haliotis diversicolor to Vibrio parahaemolyticus infection. Fish Shellfish Immunol 60:265–274

    Article  CAS  PubMed  Google Scholar 

  • Machado C, Zaleski T, Rodrigues E, dos Santos Carvalho C, Cadena SMSC, Gozzi GJ, Krebsbach P, Rios FSA, Donatti L (2014) Effect of temperature acclimation on the liver antioxidant defence system of the Antarctic nototheniids Notothenia coriiceps and Notothenia rossii. Comp Biochem Physiol b: Biochem Mol Biol 172:21–28

    Article  Google Scholar 

  • Maha IF, Xie X, Zhou S, Yu Y, Liu X, Zahid A, Lei Y, Ma R, Yin F, Qian D (2019) Skin metabolome reveals immune responses in yellow drum Nibea albiflora to Cryptocaryon irritans infection. Fish Shellfish Immunol 94:661–674

    Article  CAS  PubMed  Google Scholar 

  • Martyniuk CJ, Simmons DB (2016) Spotlight on environmental omics and toxicology: a long way in a short time. Comp Biochem Physiol d: Genomics Proteomics 19:97–101

    CAS  PubMed  Google Scholar 

  • Melvin SD, Lanctôt CM, Doriean NJ, Carroll AR, Bennett WW (2018) Untargeted NMR-based metabolomics for field-scale monitoring: temporal reproducibility and biomarker discovery in mosquitofish (Gambusia holbrooki) from a metal (loid)-contaminated wetland. Environ Pollut 243:1096–1105

    Article  CAS  PubMed  Google Scholar 

  • Melvin SD, Lanctot CM, Doriean NJC, Bennett W, Carroll AR (2019) NMR-based lipidomics of fish from a metal (loid) contaminated wetland show differences consistent with effects on cellular membranes and energy storage. Sci Total Environ 654:284–291

    Article  CAS  PubMed  Google Scholar 

  • Mou Z, Liu Y, Xu G, Li Y (2011) The optimum temperature for growth and feeding in Brachymystax lenok. Chin J Fish 24:6–8 (in Chinese with English abstract)

    Google Scholar 

  • Mueller CA, Eme J, Manzon RG, Somers CM, Boreham DR, Wilson JY (2015) Embryonic critical windows: changes in incubation temperature alter survival, hatchling phenotype, and cost of development in lake whitefish (Coregonus clupeaformis). J Comp Physiol B 185:315–331

    Article  PubMed  Google Scholar 

  • Neto EV, Fonseca AA, Almeida RF, Figueiredo MP, Porto M, Ribeiro MG (2012) Analysis of acylcarnitine profiles in umbilical cord blood and during the early neonatal period by electrospray ionization tandem mass spectrometry. Braz J Med Biol Res 45:546–556

    Article  Google Scholar 

  • Newton JR, Santis CD, Jerry DR (2012) The gene expression response of the catadromous perciform barramundi Lates calcarifer to an acute heat stress. J Fish Biol 81:81–93

    Article  CAS  PubMed  Google Scholar 

  • Ozorio R, Ginneken V, Rui J, Verstegen M, Huisman EA (2010) Effects of exercise on l-carnitine and lipid metabolism in African catfish (Clarias gariepinus) fed different dietary l-carnitine and lipid levels. Br J Nutr 103:1139–1150

    Article  CAS  PubMed  Google Scholar 

  • Qian B, Xue L (2016) Liver transcriptome sequencing and de novo annotation of the large yellow croaker (Larimichthy crocea) under heat and cold stress. Mar Genomics 25:95–102

    Article  PubMed  Google Scholar 

  • Rocha PN, Plumb TJ, Coffman TM (2003) Eicosanoids: lipid mediators ofinflammation in transplantation. Springer Semin Immunopathol 25:215–227

    Article  CAS  PubMed  Google Scholar 

  • Sabzi E, Mohammadiazarm H, Salati AP (2017) Effect of dietary l-carnitine and lipid levels on growth performance, blood biochemical parameters and antioxidant status in juvenile common carp (Cyprinus carpio). Aquaculture 480:89–93

    Article  CAS  Google Scholar 

  • Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci 109:14247–14252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semenza G (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma S, Black SM (2009) Carnitine homeostasis, mitochondrial function and cardiovascular disease. Drug Discovery Today: Disease Mechanisms 6:e31–e39

    Article  CAS  PubMed  Google Scholar 

  • Shimura M, Shindou H, Szyrwiel L, Tokuoka SM, Hamano F, Matsuyama S, Okamoto M, Matsunaga A, Kita Y, Ishizaka Y, Yamauchi K, Kohmura Y, Lobinski R, Shimizu I, Shimizu T (2016) Imaging of intracellular fatty acids by scanning X-ray fluorescence microscopy. FASEB J 30:4149–4158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun YC, Wu S, Du NN, Song Y, Xu W (2018) High-throughput metabolomics enables metabolite biomarkers and metabolic mechanism discovery of fish in response to alkalinity stress. RSC Adv 8:14983–14990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Susan GL, Mervyn EA, Bruce LT (2003) Red blood cell Hsp 70 mRNA and protein as bio-indicators of temperature stress in the brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60:460–470

    Article  Google Scholar 

  • Thomsen MT, Wang T, Milsom WK, Bayley M (2017) Lactate provides a strong pH-independent ventilatory signal in the facultative air-breathing teleost Pangasianodon hypophthalmus. Sci Rep 7:6378

    Article  PubMed  PubMed Central  Google Scholar 

  • Thorne MAS, Burns G, Fraser KPP, Hillyard G, Clark MS (2010) Transcription profiling of acute temperature stress in the Antarctic plunderfish Harpagifer antarcticus. Mar Genomics 3:35–44

    Article  CAS  PubMed  Google Scholar 

  • Van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124

    Article  PubMed  PubMed Central  Google Scholar 

  • Vatanparast M, Ahmed S, Lee DH, Hwang SH, Hammock B, Kim Y (2020) EpOMEs act as immune suppressors in a lepidopteran insect, Spodoptera exigua. Sci Rep 10:20183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetter W, Darwisch V, Lehnert K (2020) Erucic acid in Brassicaceae and salmon – an evaluation of the new proposed limits of erucic acid in food. NFS Journal 19:9–15

    Article  Google Scholar 

  • Wang QJ, Ju X, Chen YK, Dong XQ, Luo S, Liu HJ, Zhang DM (2016) Effects of L-carnitine against H2O2-induced oxidative stress in grass carp ovary cells (Ctenopharyngodon idellus). Fish Physiol Biochem 42:845–857

    Article  CAS  PubMed  Google Scholar 

  • Windisch HS, Frickenhaus S, John U, Knust R, PöRtner HO, Lucassen M (2014) Stress response or beneficial temperature acclimation: transcriptomic signatures in Antarctic fish (Pachycara brachycephalum). Mol Ecol 23:3469–3482

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Peng JL, Fu SJ (2017) The behavioral response of juvenile Brachymystax lenok tsinlingensis to heating stress. Journal of Chongqing Normal University (Natural Science) (in Chinese with English abstract).

  • Xu GF, Wang YY, Han Y, Xiang LI, Bo MA., Liu Y, Mou ZB (2014). Effect of locomotion and feeding on metabolic mode of juvenile lenok, Brachymystax lenok (Pallas) under different water temperatures. Chinese Journal of Applied Ecology. (in Chinese with English abstract)

  • Yang PY, Klein RD, Chan D, Felix E, Madden T, Shureiqi I, Cheo XX, Dannenberg AJ, Newman RA (2006) LC/MS/MS based determination of tissue inflammation profiles: simultaneous determination of COX and LOX derived bioactive lipids. Prostaglandins Other Lipid Mediat 79:187–187

    Google Scholar 

  • Yeo SR, Kim KY (2014) Global warming, low-frequency variability, and biennial oscillation: an attempt to understand the physical mechanisms driving major ENSO events. Clim Dyn 43:771–786

    Article  Google Scholar 

  • Zarini S, Hankin JA, Murphy RC, Gijon MA (2014) Lysophospholipid acyltransferases and eicosanoid biosynthesis in zebrafish myeloid cells. Prostaglandins Other Lipid Mediat 113:52–61

    Article  PubMed  Google Scholar 

  • Zhang W, Song Y, Chai TT, Liao GQ, Zhang L, Jia Q, Qian YZ, Qiu J (2020) Lipidomics perturbations in the brain of adult zebrafish (Danio rerio) after exposure to chiral ibuprofen. Sci Total Environ 713:136565

    Article  CAS  PubMed  Google Scholar 

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Funding

The work was fund support by Beijing technical industry system project (pxm2021 179303 000022), Qinghai Science and Technology Department Project (No. 2018-ZJ-703), and National Natural Science Foundation of China (No. 31760763).

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Yan Chen was responsible for experimental design and manuscript writing. Yang Liu took part in sampling and funding acquisition. Yucen Bai supervised the research project and supervised the writing of the manuscript. Shaogang Xu was responsible for preliminary investigation and funding acquisition. Xiaofei Yang took part in experimental procedures. Bo Cheng was responsible for supervising the research project.

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Correspondence to Yucen Bai or Bo Cheng.

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This study was approved by the Institutional Animal Care and Use Committee of Beijing Fisheries Research Institute, Beijing Academy of Agriculture and Forestry Sciences. All experimental procedures were in compliance with the guidelines of Yanqing site of the Beijing Academy of Agriculture and Forestry Sciences, Institute of Fisheries Research, Beijing, China.

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Chen, Y., Liu, Y., Bai, Y. et al. Intestinal metabolomics of juvenile lenok (Brachymystax lenok) in response to heat stress. Fish Physiol Biochem 48, 1389–1400 (2022). https://doi.org/10.1007/s10695-022-01128-7

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