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Transcriptomic analysis reveals putative osmoregulation mechanisms in the kidney of euryhaline turbot Scophthalmus maximus responded to hypo-saline seawater

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Abstract

Turbot harbor a relatively remarkable ability to adapt to opposing osmotic challenges and are an excellent model species to study the physiological adaptations of flounder associated with osmoregulatory plasticity. The kidney transcriptome of turbot treated 24 h in water of hypo-salinity(salinity 5) and seawater(salinity 30) was sequenced and characterized. In silico analysis indicated that all unigenes had significant hits in seven databases. The functional annotation analysis of the transcriptome showed that the immune system and biological processes associated with digestion, absorption, and metabolism played an important role in the osmoregulation of turbot in response to hypo-salinity. Analysis of biological processes associated with inorganic channels and transporters indicated that mineral absorption and bile secretion contributed to iono-osmoregulation resulting in cell volume regulation and cell phenotypic plasticity. Moreover, we analyzed and predicted the mechanisms of canonical signaling transduction. Biological processes involved in renin secretion, ECM-receptor interaction, adherens junction, and focal adhesion played an important role in the plasticity phenotype in hypo-stress, while the signal transduction network composed of the MAPK signaling pathway and PI3K-Akt signaling pathway with GABAergic synapse, worked in hypo-osmoregulation signal transduction in the turbot. In addition, analysis of the tissue specificity of targeted gene expression using qPCR during salinity stress was carried out. The results showed that the kidney, gill, and spleen were vital regulating organs of osmotic pressure, and the osmoregulation pattern of euryhaline fish differed among species.

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Data Availability Statement

The raw reads for the next generation sequencing data have been deposited in NCBI Sequence Read Archive (SRA) with the GenBank number SRP153594.

References

  • Alves-Costa F A, Denovan-Wright E M, Thisse C, Thisse B, Wright J M. 2008. Spatio-temporal distribution of fatty acid-binding protein 6(fabp6) gene transcripts in the developing and adult zebrafish (Danio rerio). FEBS J., 275(13): 3 325–3 334.

    Article  Google Scholar 

  • Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol., 11(10): R106, https://doi.org/10.1186/gb-2010-11-10-r106.

    Article  Google Scholar 

  • Arden K C. 2004. FoxO: linking new signaling pathways. Mol. Cell, 14(4): 416–418.

    Article  Google Scholar 

  • Babey M, Kopp P, Robertson G L. 2011. Familial forms of diabetes insipidus: clinical and molecular characteristics. Nat. Rev. Endocrinol., 7(12): 701–714.

    Article  Google Scholar 

  • Bakir B, Sezerman O U. 2006. Functional classification of G-protein coupled receptors, based on their specific ligand coupling patterns. In: Rothlauf F, Branke J, Cagnoni S, Costa E, Cotta C, Drechsler R, Lutton E, Machado P, Moore J H, Romero J, Smith G D, Squillero G, Takagi H eds. Applications of Evolutionary Computing. Springer, Berlin, Heidelberg. p. 1–12.

    Google Scholar 

  • Beyenbach K W. 1986. Secretory NaCl and volume flow in renal tubules. Am. J. Physiol., 250(5): R753–R763.

    Google Scholar 

  • Beyenbach K W. 2004. Kidneys sans glomeruli. Am. J. Physiol. Renal Physiol., 286(5): F811–F827.

    Article  Google Scholar 

  • Bhattacharya S. 2004. Handbook of cell signaling. J. Anat., 205(1): 77.

    Article  Google Scholar 

  • Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank D A, Rozovsky I, Stahl N, Yancopoulos G D, Greenberg M E. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science, 278(5337): 477–483.

    Article  Google Scholar 

  • Brennan R S, Galvez F, Whitehead A. 2015. Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus. J. Exp. Biol., 218(8): 1 212–1 222.

    Article  Google Scholar 

  • Cutler C P, Cramb G. 2002. Branchial expression of an aquaporin 3 (AQP-3) homologue is downregulated in the European eel Anguilla anguilla following seawater acclimation. J. Exp. Biol., 205(17): 2 643–2 651.

    Google Scholar 

  • Cutler C P, Philips C, Hazon N, Cramb G. 2009. Aquaporin 8 (AQP8) intestinal mRNA expression increases in response to salinity acclimation in yellow and silver European eels (Anguilla anguilla). Comp. Biochem. Physiol. A Mol. Integr. Physiol., 153(S2): S78.

    Article  Google Scholar 

  • Dietz C, Stiller K T, Griese M, Schulz C, Susenbeth A. 2013. Influence of salinity on energy metabolism in juvenile turbot, Psetta maxima(L.). Aquacult. Nutr., 19(S1): 135–150.

    Article  Google Scholar 

  • Edwards S L, Marshall W S. 2012. Principles and patterns of osmoregulation and euryhalinity in fishes. Fish Physiol., 32: 1–44.

    Article  Google Scholar 

  • Ehebauer M, Hayward P, Martinez-Arias A. 2006. Notch signaling pathway. Sci. STKE, 2006(364): cm7.

    Article  Google Scholar 

  • Farrell A P. 2011. Encyclopedia of Fish Physiology: from Genome to Environment. Academic Press, San Diego.

    Google Scholar 

  • Fielding C J, Shore V G, Fielding P E. 1972. A protein cofactor of lecithin:cholesterol acyltransferase. Biochem. Biophys. Res. Commun., 46(4): 1 493–1 498.

    Article  Google Scholar 

  • Fiol D F, Kültz D. 2007. Osmotic stress sensing and signaling in fishes. FEBS J., 274(22): 5 790–5 798.

    Article  Google Scholar 

  • Fouchs A, Ollivier H, Haond C, Roy S, Calvès P, Pichavant-Rafini K. 2010. Activation of the MAPKs ERK1/2 by cell swelling in turbot hepatocytes. Biol. Cell, 102(8): 447–456.

    Article  Google Scholar 

  • Götz S, García-Gómez J M, Terol J, Williams T D, Nagaraj S H, Nueda M J, Robles M, Talón M, Dopazo J, Conesa A. 2008. High-throughput functional annotation and data mining with the blast2go suite. Nucleic Acids Res., 36(10): 3 420–3 435.

    Article  Google Scholar 

  • Goward C R, Nicholls D J. 1994. Malate dehydrogenase: a model for structure, evolution, and catalysis. Protein Sci., 3(10): 1 883–1 888.

    Article  Google Scholar 

  • Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, Di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Trinity: reconstructing a ful-llength transcriptome without a genome from RNA-Seq data. Nat. Biotechnol., 29(7): 644–652.

    Article  Google Scholar 

  • Grant S, Qiao L, Dent P. 2002. Roles of ERBB family receptor tyrosine kinases, and downstream signaling pathways, in the control of cell growth and survival. Front Biosci., 7: d376–389.

    Article  Google Scholar 

  • Hoffmann E K, Lambert I H, Pedersen S F. 2009. Physiology of cell volume regulation in vertebrates. Physiol. Rev., 89(1): 193–277.

    Article  Google Scholar 

  • Hummel C S, Lu C, Loo D D F, Hirayama B A, Voss A A, Wright E M. 2011. Glucose transport by human renal Na+/d-glucose cotransporters SGLT1 and SGLT2. Am. J. Physiol. Cell Physiol., 300(1): C14–C21.

    Article  Google Scholar 

  • Imsland A K, Foss A, Gunnarsson S, Berntssen M H G, FitzGerald R, Bonga S W, v Ham E, Nævdal G, Stefansson S O. 2001. The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture, 198(3-4): 353–367.

    Article  Google Scholar 

  • Inokuchi M, Hiroi J, Watanabe S, Lee K M, Kaneko T. 2008. Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria-rich cells of mozambique tilapia (Oreochromis mossambicus) acclimated to a wide range of salinities. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 151(2): 151–158.

    Article  Google Scholar 

  • Kalujnaia S, McWilliam I S, Zaguinaiko V A, Feilen A L, Nicholson J, Hazon N, Cutler C P, Cramb G. 2007. Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla Physiol. Genomics, 31(3): 385–401.

    Google Scholar 

  • Karaica D, Breljak D, Brzica H, Lončar J, Herak-Kramberger C M, Micek V, Vrhovac I, Ivković D J, Mihaljević I, Marić P, Smital T, Burckhardt B C, Burckhardt G, Sabolić I. 2015. CFEX (slc26a6) in rat kidneys, liver, and small intestine in an experimental model of oxalate nephrolitiasis. Arch. Ind. Hyg. Toxicol., 66(3): 228.

  • Kasprowicz A. 2011. Osmosensing. In: Wojtaszek P ed. Mechanical Integration of Plant Cells and Plants. Springer, Berlin, Heidelberg. p. 225–240.

    Chapter  Google Scholar 

  • Kültz D, Avila K. 2001. Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 129(4): 821–829.

    Article  Google Scholar 

  • Kültz D, Burg M. 1998. Evolution of osmotic stress signaling via MAP kinase cascades. J. Exp. Biol., 201(22): 3 015–3 021.

    Google Scholar 

  • Kültz D. 2015. Physiological mechanisms used by fish to cope with salinity stress. J. Exp. Biol., 218(12): 1 907–1 914.

    Article  Google Scholar 

  • Kurt B, Kurtz L, Sequeira-Lopez M L, Gomez R A, Willecke K, Wagner C, Kurtz A. 2011. Reciprocal expression of connexin 40 and 45 during phenotypical changes in renin-secreting cells. Am. J. Physiol. Renal Physiol., 300(3): F743–F748.

    Article  Google Scholar 

  • Kurtz A, Wagner C. 1999. Cellular control of renin secretion. J. Exp. Biol., 202(3): 219–225.

    Google Scholar 

  • Lam S H, Lui E Y, Li Z J, Cai S J, Sung W K, Mathavan S, Lam T J, Ip Y K. 2014. Differential transcriptomic analyses revealed genes and signaling pathways involved in ionoosmoregulation and cellular remodeling in the gills of euryhaline mozambique tilapia, Oreochromis mossambicus. BMC Genomics, 15(1): 921.

    Article  Google Scholar 

  • Lee K M, Kaneko T, Katoh F, Aida K. 2006. Prolactin gene expression and gill chloride cell activity in fugu Takifugu rubripes exposed to a hypoosmotic environment. Gen. Comp. Endocrinol., 149(3): 285–293.

    Article  Google Scholar 

  • Li B, Dewey C N. 2011. Rsem: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12: 323.

    Article  Google Scholar 

  • Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics, 21(19): 3 787–3 793.

    Article  Google Scholar 

  • Marshall W, Grosell M. 2005. Ion transport, osmoregulation, and acid-base balance. In: {Evans D H, Claiborne J B} eds. The Physiology of Fishes. 3rd ed. CRC Press, Boca Raton. p. 177–230.

    Google Scholar 

  • Narnaware B Y K, Kelly S P, Woo N Y S. 2000. Effect of salinity and ration size on macrophage phagocytosis in juvenile black sea bream (Mylio macrocephalus). J. Appl. Ichthyol., 16(2): 86–88.

    Article  Google Scholar 

  • Nishimoto G, Sasaki G, Yaoita E, Nameta M, Li H, Furuse K, Fujinaka H, Yoshida Y, Mitsudome A, Yamamoto T. 2007. Molecular characterization of water-selective AQP (EbAQP4) in hagfish: insight into ancestral origin of AQP4. Am. J. Physiol. Regul. Integr. Comp. Physiol., 292(1): R644–R651.

    Article  Google Scholar 

  • Oelkers P, Kirby L C, Heubi J E, Dawson P A. 1997. Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene(SLC10A2). J. Clin. Invest., 99(8): 1 880–1 887.

    Article  Google Scholar 

  • Pereiro P, Balseiro P, Romero A, Dios S, Forn-Cuni G, Fuste B, Planas J V, Beltran S, Novoa B, Figueras A. 2012. High-throughput sequence analysis of turbot (Scophthalmus maximus) transcriptome using 454-pyrosequencing for the discovery of antiviral immune genes. PLoS One , 7(5): e35369.

    Article  Google Scholar 

  • Pickford G E, Phillips J G. 1959. Prolactin, a factor in promoting survival of hypophysectomized killifish in fresh water. Science , 130(3373): 454–455.

    Article  Google Scholar 

  • Prodocimo, V, Souza C F, Pessini C, Fernandes L C, Freire C A. 2008. Metabolic substrates are not mobilized from the osmoregulatory organs (gills and kidney) of the estuarine pufferfishes Sphoeroides greeleyi and S. testudineus upon short-term salinity reduction. Neotrop. Ichthyol., 6(4): 613–620, https://doi.org/10.1590/S1679-62252008000400009.

    Article  Google Scholar 

  • Rappolee D A, Armant D R. 2009. Cell signaling. In: Krawetz S ed. Bioinformatics for Systems Biology. Humana Press, New York. p. 89–104.

    Chapter  Google Scholar 

  • Schmittgen T D, Zakrajsek B A. 2000. Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J. Biochem. Biophys. Methods , 46(1-2): 69–81.

    Article  Google Scholar 

  • Shibata Y, Kumai M, Nishii K, Nakamura K. 2001. Diversity and molecular anatomy of gap junctions. Med. Electron Microsc., 34(3): 153–159.

    Article  Google Scholar 

  • Tang X M, Sui Z, Tian J B, Wang G F. 2006. Effects of salinity on metabolic rate of juvenile turbot (Scophamus maximus). South China Fish. Sci., 2(4): 54–58. (in Chinese with English abstract)

    Google Scholar 

  • Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, Van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28(5): 511–515.

    Article  Google Scholar 

  • Vojtek A B, Der C J. 1998. Increasing complexity of the Ras signaling pathway. J. Biol. Chem., 273(32): 19 925–19 928.

    Article  Google Scholar 

  • Xu Z Z, Gan L, Li T Y, Xu C, Chen K, Wang X D, Qin J G, Chen L Q, Li E C. 2015. Transcriptome profiling and molecular pathway analysis of genes in association with salinity adaptation in Nile tilapia Oreochromis niloticus. PLoS One , 10(8): e0136506.

    Article  Google Scholar 

  • Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol., 11(2): R14.

    Article  Google Scholar 

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Correspondence to Aijun Ma.

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Supported by the Earmarked Fund for Modern Agro-Industry Technology Research System(No. CARS-47-G01), the AoShan Talents Cultivation Program supported by Qingdao National Laboratory for Marine Science and Technology(No. 2017ASTCP-OS04), the National Natural Science Foundation of China(No. 41706168), the Agricultural Fine Breed Project of Shandong(No. 2019LZGC013), the Basal Research Fund, Chinese Academy of Fishery Sciences(No. 2016HY-JC0301), and the Yantai Science and Technology Project(No. 2018ZDCX021)

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Cui, W., Ma, A., Huang, Z. et al. Transcriptomic analysis reveals putative osmoregulation mechanisms in the kidney of euryhaline turbot Scophthalmus maximus responded to hypo-saline seawater. J. Ocean. Limnol. 38, 467–479 (2020). https://doi.org/10.1007/s00343-019-9056-2

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