Advertisement

Marine Biology

, 164:95 | Cite as

Genomic organization and spatio-temporal expression of the hemoglobin genes in European sea bass (Dicentrarchus labrax)

  • L. Cadiz
  • E. Desmarais
  • A. Servili
  • P. Quazuguel
  • L. Madec
  • C. Huelvan
  • O. Andersen
  • J. Zambonino-Infante
  • D. MazuraisEmail author
Original paper

Abstract

Hemoglobins (Hb) play a critical role in satisfying the oxygen demand of vertebrate aerobic metabolism. The present study reports the characterization of the European sea bass (Dicentrarchus labrax) Hb genes, including genomic organization, phylogeny, and spatio-temporal gene expression. These Hb genes are divided into two unlinked clusters, the “MN” cluster containing eleven genes (five Hbα genes named MN-Hbα1-5 and six Hbβ genes named MN-Hbβ1–6) and the “LA” cluster consisting of three genes (two Hbα genes named LA-Hbα1-2 and one Hbβ gene named LA-Hbβ1). Comparative analysis of Hb amino acid sequences indicates that most of the important amino acid residues involved in hemoglobin-oxygen binding, particularly in the Bohr and Root effects, are generally well conserved, except in MN-Hbβ3. Six genes were mainly expressed during early life (MN-Hbα3-5, MN-Hbβ4–6), while the others were predominantly expressed at juvenile–adult stages. Adult fish expressed Hb genes at high levels in the head kidney and spleen; the main organs involved in blood formation. The Hb genes expressed in non-hematopoietic organs (intestine, gills, heart, brain, and liver) may facilitate oxygen homeostasis or be involved in antimicrobial defense. Stage- and tissue-specific gene expression patterns, together with the sequence features of the different Hb proteins, suggest a broad range of roles in European sea bass.

Keywords

Markov Chain Monte Carlo Supplementary File Link Group Head Kidney Root Effect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The first author was supported by a joint Ifremer–Région Bretagne doctoral grant and by the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19). The authors are very grateful to Laure Quintric and Fanny Marquer (Cellule bioinformatique, Centre Ifremer Bretagne) for bioinformatic assistance, to Dorothée Vincent for correcting the manuscript and to Helen Mc Combie for correcting the English. This is publication ISE-M 2017-058.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2017_3128_MOESM1_ESM.pdf (365 kb)
Supplementary material 1 (PDF 365 KB)
227_2017_3128_MOESM2_ESM.pdf (320 kb)
Supplementary material 2 (PDF 319 KB)
227_2017_3128_MOESM3_ESM.pdf (238 kb)
Supplementary material 3 (PDF 237 KB)
227_2017_3128_MOESM4_ESM.pdf (357 kb)
Supplementary material 4 (PDF 357 KB)
227_2017_3128_MOESM5_ESM.pdf (440 kb)
Supplementary material 5 (PDF 439 KB)
227_2017_3128_MOESM6_ESM.pdf (428 kb)
Supplementary material 6 (PDF 427 KB)
227_2017_3128_MOESM7_ESM.pdf (425 kb)
Supplementary material 7 (PDF 425 KB)
227_2017_3128_MOESM8_ESM.pdf (427 kb)
Supplementary material 8 (PDF 426 KB)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105CrossRefGoogle Scholar
  2. Bellelli A, Brunori M (2011) Hemoglobin allostery: variations on the theme. Biochim Biophys Acta (BBA) Bioenergetics 1807:1262–1272Google Scholar
  3. Biagioli M, Pinto M, Cesselli D, Zaninello M, Lazarevic D, Roncaglia P, Simone R, Vlachouli C, Plessy C, Bertin N, Beltrami A, Kobayashi K, Gallo V, Santoro C, Ferrer I, Rivella S, Beltrami CA, Carninci P, Raviola E, Gustincich S (2009) Unexpected expression of alpha- and beta-globin in mesencephalic dopaminergic neurons and glial cells. Proc Natl Acad Sci USA 106:15454–15459CrossRefGoogle Scholar
  4. Bonaventura C, Crumbliss AL, Weber RE (2004) New insights into the proton-dependent oxygen affinity of root effect haemoglobins. Acta Physiol Scand 182:245–258CrossRefGoogle Scholar
  5. Brownlie A, Zon L (1999) The Zebrafish as a model system for the study of hematopoiesis: Zebrafish mutants point the way to novel genes involved in the generation of vertebrate blood cells. Bioscience 49:382–392CrossRefGoogle Scholar
  6. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94CrossRefGoogle Scholar
  7. Campo S, Nastasi G, D'Ascola A, Campo GM, Avenoso A, Traina P, Calatroni A, Burrascano E, Ferlazzo A, Lupidi G, Gabbianelli R, Falcioni G (2008) Hemoglobin system of Sparus aurata: changes in fishes farmed under extreme conditions. Sci Total Environ 403:148–153Google Scholar
  8. Claireaux G, Lagardère JP (1999) Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. J Sea Res 42:157–168CrossRefGoogle Scholar
  9. Darias MJ, Zambonino-Infante JL, Hugot K, Cahu CL, Mazurais D (2008) Gene expression patterns during the larval development of European sea bass (dicentrarchus labrax) by microarray analysis. Mar Biotechnol (NY) 10: 416–428CrossRefGoogle Scholar
  10. Esteban MA, Meseguer J, Garcia Ayala A, Agulleiro B (1989) Erythropoiesis and thrombopoiesis in the head-kidney of the sea bass (Dicentrarchus labrax L.): an ultrastructural study. Arch Histol Cytol 52:407–419CrossRefGoogle Scholar
  11. Feng J, Liu S, Wang X, Wang R, Zhang J, Jiang Y, Li C, Kaltenboeck L, Li J, Liu Z (2014) Channel catfish hemoglobin genes: identification, phylogenetic and syntenic analysis, and specific induction in response to heat stress. Comp Biochem Physiol Part D Genomics Proteomics 9:11–22CrossRefGoogle Scholar
  12. Gabbianelli R, Zolese G, Bertoli E, Falcioni G (2004) Correlation between functional and structural changes of reduced and oxidized trout hemoglobins I and IV at different pHs. A circular dichroism study. Eur J Biochem 271:1971–1979CrossRefGoogle Scholar
  13. Hardison RC (2008) Globin genes on the move. J Biol 7:35CrossRefGoogle Scholar
  14. Helfman G, Collete B, Facey D (1997) The Diversity of Fishes Malden, MassGoogle Scholar
  15. Ishibashi Y, Kotaki T, Yamada Y, Ohta H (2007) Ontogenic changes in tolerance to hypoxia and energy metabolism of larval and juvenile Japanese flounder Paralichthys olivaceus. J Exp Mar Biol Ecol 352:42–49CrossRefGoogle Scholar
  16. Kulkeaw K, Sugiyama D (2012) Zebrafish erythropoiesis and the utility of fish as models of anemia. Stem Cell Res Ther 3:55Google Scholar
  17. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320CrossRefGoogle Scholar
  18. Lu W, Mayolle A, Cui G, Luo L, Balment RJ (2011) Molecular characterization and expression of alpha-Globin and beta-Globin Genes in the Euryhaline Flounder (Platichthys flesus). Evid Based Complement Alternat Med 965153Google Scholar
  19. Marinakis P, Tamburrini M, Carratore V, di Prisco G (2003) Unique features of the hemoglobin system of the Antarctic notothenioid fish Gobionotothen gibberifrons. Eur J Biochem 270:3981–3987CrossRefGoogle Scholar
  20. Maruyama K, Yasumasu S, Naruse K, Mitani H, Shima A, Iuchi I (2004) Genomic organization and developmental expression of globin genes in the teleost Oryzias latipes. Gene 335:89–100CrossRefGoogle Scholar
  21. Mazzarella L, Bonomi G, Lubrano MC, Merlino A, Riccio A, Vergara A, Vitagliano L, Verde C, di Prisco G (2006) Minimal structural requirements for root effect: crystal structure of the cathodic hemoglobin isolated from the antarctic fish Trematomus newnesi. Proteins 62:316–321CrossRefGoogle Scholar
  22. McKenzie DJ, Lund I, Pedersen PB (2008) Essential fatty acids influence metabolic rate and tolerance of hypoxia in Dover sole (Solea solea) larvae and juveniles. Marine Biology 154:1041–1051CrossRefGoogle Scholar
  23. Mylvaganam SE, Bonaventura C, Bonaventura J, Getzoff ED (1996) Structural basis for the root effect in haemoglobin. Nat Struct Mol Biol 3:275–283CrossRefGoogle Scholar
  24. Near TJ, Parker SK, Detrich HW 3rd (2006) A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes. Mol Biol Evol 23:2008–2016CrossRefGoogle Scholar
  25. Nishi H, Inagi R, Kato H, Tanemoto M, Kojima I, Son D, Fujita T, Nangaku M (2008) Hemoglobin is expressed by mesangial cells and reduces oxidant stress. J Am Soc Nephrol 19:1500–1508CrossRefGoogle Scholar
  26. Opazo JC, Butts GT, Nery MF, Storz JF, Hoffmann FG (2013) Whole-genome duplication and the functional diversification of teleost fish hemoglobins. Mol Biol Evol 30:140–153CrossRefGoogle Scholar
  27. Perez JE, Maclean N (1976) Multiple globins and haemoglobins in the bass, Dicentrarchus labrax (L.) (Serranidae: Teleostei). J Fish Biol 8:413–417CrossRefGoogle Scholar
  28. Perez-Ruzafa A, Marcos C (2014) Ecology and distribution of Dicentrarchus labrax (Linnaeus 1758). In: Sanchez Vazquey J, Munoz-Cueto J (eds) Biology of European Sea Bass. CRC Press, Boca Raton, FL, pp 3–33Google Scholar
  29. Perutz MF (1983) Species adaptation in a protein molecule. Mol Biol Evol 1:1–28Google Scholar
  30. Quesada J, Villena MI, Navarro V (1994) Ontogeny of the sea bass spleen (Dicentrarchus labrax): a light and electron microscopic study. J Morphol 221:161–176CrossRefGoogle Scholar
  31. Quinn NL, Boroevich KA, Lubieniecki KP, Chow W, Davidson EA, Phillips RB, Koop BF, Davidson WS (2010) Genomic organization and evolution of the Atlantic salmon hemoglobin repertoire. BMC Genomics 11:539CrossRefGoogle Scholar
  32. Rinaldi L, Basso P, Tettamanti G, Grimaldi A, Terova G, Saroglia M, de Eguileor M (2005) Oxygen availability causes morphological changes and a different VEGF/FIk-1/HIF-2 expression pattern in sea bass gills. Ital J Zool 72:103–111Google Scholar
  33. Rutjes HA, Nieveen MC, Weber RE, Witte F, Van den Thillart GE (2007) Multiple strategies of Lake Victoria cichlids to cope with lifelong hypoxia include hemoglobin switching. Am J Physiol Regul Integr Comp Physiol 293:R1376–R1383CrossRefGoogle Scholar
  34. Saha D, Patgaonkar M, Shroff A, Ayyar K, Bashir T, Reddy KV (2014) Hemoglobin expression in nonerythroid cells: novel or ubiquitous? Int J Inflam 803237Google Scholar
  35. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  36. Terova G, Cattaneo AG, Preziosa E, Bernardini G, Saroglia M (2011) Impact of acute stress on antimicrobial polypeptides mRNA copy number in several tissues of marine sea bass (Dicentrarchus labrax). BMC Immunol 12:69CrossRefGoogle Scholar
  37. Tezel G, Yang X, Luo C, Cai J, Kain AD, Powell DW, Kuehn MH, Pierce WM (2010) Hemoglobin expression and regulation in glaucoma: insights into retinal ganglion cell oxygenation. Invest Ophthalmol Vis Sci 51:907–919CrossRefGoogle Scholar
  38. Tiedke J, Gerlach F, Mitz SA, Hankeln T, Burmester T (2011) Ontogeny of globin expression in zebrafish (Danio rerio). J Comp Physiol B 181:1011–1021CrossRefGoogle Scholar
  39. Tine M, Kuhl H, Gagnaire PA, Louro B, Desmarais E, Martins RS, Hecht J, Knaust F, Belkhir K, Klages S, Dieterich R, Stueber K, Piferrer F, Guinand B, Bierne N, Volckaert FA, Bargelloni L, Power DM, Bonhomme F, Canario AV, Reinhardt R (2014) European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun 5:5770CrossRefGoogle Scholar
  40. Tortonese E (1986) Moronidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J ET (eds) Fishes of the North-eastern Atlantic and the Mediterranean, Paris, pp 793–796Google Scholar
  41. Ullal AJ, Wayne Litaker R, Noga EJ (2008) Antimicrobial peptides derived from hemoglobin are expressed in epithelium of channel catfish (Ictalurus punctatus, Rafinesque). Developmental and Comparative. Immunology 32:1301–1312Google Scholar
  42. Verde C, Carratore V, Riccio A, Tamburrini M, Parisi E, Di Prisco G (2002) The functionally distinct hemoglobins of the Arctic spotted wolffish Anarhichas minor. J Biol Chem 277:36312–36320CrossRefGoogle Scholar
  43. Verde C, Balestrieri M, de Pascale D, Pagnozzi D, Lecointre G, di Prisco G (2006) The oxygen transport system in three species of the boreal fish family Gadidae. Molecular phylogeny of hemoglobin. J Biol Chem 281:22073–22084CrossRefGoogle Scholar
  44. Verde C, Vergara A, Mazzarella L, di Prisco G (2008) The hemoglobins of fishes living at polar latitudes—current knowledge on structural adaptations in a changing environment. Curr Protein Pept Sci 9:578–590CrossRefGoogle Scholar
  45. von der Heyden S, Toms JA, Teske PR, Lamberth SJ, Holleman W (2015) Contrasting signals of genetic diversity and historical demography between two recently diverged marine and estuarine fish species. Mar Ecol Prog Ser 526:157–167Google Scholar
  46. Weber RE (1990) Functional significance and structural basis of multiple hemoglobins with special reference to ectothermic vertebrates. In: Animal Nutrition and Transport Processes. 2. Transport, Respiration and Excretion: Comparative and Environmental Aspects. Comparative Physiology. Karger, Basel, pp 58–75Google Scholar
  47. Weber RE (2000) Adaptations for oxygen transport: lessons from Fish Hemoglobins hemoglobin function in vertebrates: molecular adaptation in extreme and temperate environments. Springer Milan, Milano, pp 23–37Google Scholar
  48. Wetten OF, Nederbragt AJ, Wilson RC, Jakobsen KS, Edvardsen RB, Andersen O (2010) Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters. BMC Evol Biol 10:315CrossRefGoogle Scholar
  49. Zambonino-Infante JL, Cahu CL, Peres A, Quazuguel P, Le Gall MM (1996) Sea bass (Dicentrarchus labrax) larvae fed different Artemia rations: growth, pancreas enzymatic response and development of digestive functions. Aquaculture 139:129–138CrossRefGoogle Scholar
  50. Zhou J, Qiao X, Xiao L, Sun W, Wang L, Li H, Wu Y, Ding X, Hu X, Zhou C, Zhang J (2010) Identification and characterization of the novel protein CCDC106 that interacts with p53 and promotes its degradation. FEBS Lett 584:1085–1090CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • L. Cadiz
    • 1
  • E. Desmarais
    • 2
  • A. Servili
    • 1
  • P. Quazuguel
    • 1
  • L. Madec
    • 1
  • C. Huelvan
    • 1
  • O. Andersen
    • 3
    • 4
  • J. Zambonino-Infante
    • 1
  • D. Mazurais
    • 1
    Email author
  1. 1.Ifremer, Unité de Physiologie Fonctionnelle des Organismes MarinsPlouzanéFrance
  2. 2.Institut des Sciences de l’Evolution (UMR 5554), Université de Montpellier, CNRS-UM-IRD-EPHEMontpellierFrance
  3. 3.NofimaÅsNorway
  4. 4.Department of Animal and Aquaculture SciencesNorwegian University of Life SciencesÅsNorway

Personalised recommendations