Marine Biotechnology

, Volume 12, Issue 2, pp 214–229 | Cite as

Effect of Early Introduction of Microencapsulated Diet to Larval Atlantic Halibut, Hippoglossus hippoglossus L. Assessed by Microarray Analysis

  • H. M. Murray
  • S. P. Lall
  • R. Rajaselvam
  • L. A. Boutilier
  • R. M. Flight
  • B. Blanchard
  • S. Colombo
  • V. Mohindra
  • M. Yúfera
  • S. E. Douglas
Original Article

Abstract

An experimental microdiet prepared using an internal gelation method was used to partially replace the traditional live feed (Artemia) for larval Atlantic halibut, Hippoglossus hippoglossus L. Three trials were conducted with microdiet introduced at 20, 32, and 43 days post first feeding and larvae were sampled at approximately 2, 13, 23, and 33 days after microdiet introduction in each trial. The success of feeding was assessed by morphometrics and histological analysis of gut contents. Microdiet particles were readily consumed after a period of adaptation and provided an adequate source of nutrients with no significant increase in mortality in the microdiet-fed group compared to the control group. However, growth was limited and there was an increased incidence of malpigmentation of the eye and skin. Subtle changes in underlying digestive and developmental physiology were revealed by microarray analysis of RNA from control and experimental fish given microdiet from day 20 post first feeding. Fifty-eight genes were differentially expressed over the four sampling times in the course of the trial and the 28 genes with annotated functions fell into five major categories: metabolism and biosynthesis, cell division and proliferation, protein trafficking, cell structure, and stress. Interestingly, several of these genes were involved in pigmentation and eye development, in agreement with the phenotypic abnormalities seen in the larvae.

Keywords

Microencapsulated diet Larvae Atlantic halibut Microarray 

References

  1. Applebaum S (1985) Rearing of Dover sole, Solea solea (L.), through its larval stages using artificial diets. Aquaculture 49:209–221CrossRefGoogle Scholar
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis aP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29CrossRefPubMedGoogle Scholar
  3. Barrowman J, Wang W, Zhang Y, Ferro-Novick S (2003) The Yip1p.Yif1p complex is required for the fusion competence of endoplasmic reticulum-derived vesicles. J Biol Chem 278:19878–19884CrossRefPubMedGoogle Scholar
  4. Bell JG, Mcevoy LA, Estevez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220CrossRefGoogle Scholar
  5. Berg L (1997) Commercial feasibility of semi-intensive larviculture of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 155:333–340CrossRefGoogle Scholar
  6. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, Kuo WP, Weber G, Lee K, Fraioli RE, Cho SH, Yung R, Asch E, Ohno-Machado L, Wong WH, Cepko CL (2004) Genomic analysis of mouse retinal development. PLoS Biol 2:1411–1431CrossRefGoogle Scholar
  7. Blanchard B, Scarratt D (2002) Finely-tuned hatchery the key to halibut success. Hatch Int 3:9–13Google Scholar
  8. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G (2004) GO::TermFinder—open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20:3710–3715CrossRefPubMedGoogle Scholar
  9. Cameron DA, Gentile KL, Middleton FA, Yurco P (2005) Gene expression profiles of intact and regenerating zebrafish retina. Mol Vis 11:775–191PubMedGoogle Scholar
  10. Cañavate JP, Fernández-Díaz C (1999) Influence of co-feeding larvae with live and inert diets on weaning the sole Solea senegalensis onto commercial dry feeds. Aquaculture 17:255–263CrossRefGoogle Scholar
  11. Chang H, Gilbert W (1997) A novel zebrafish gene expressed specifically in the photoreceptor cells of the retina. Biochem Biophys Res Commun 237:84–89CrossRefPubMedGoogle Scholar
  12. Chi A, Valencia JC, Hu ZZ, Watabe H, Yamaguchi H, Mangini NJ, Huang H, Canfield VA, Cheng KC, Yang F, Abe R, Yamagishi S, Shabanowitz J, Hearing VJ, Wu C, Appella E, Hunt DF (2006) Proteomic and bioinformatic characterization of the biogenesis and function of melanosomes. J Proteome Res 5:3135–3144CrossRefPubMedGoogle Scholar
  13. Curnow J, King J, Bosmans J, Kolkovski S (2006) The effect of reduced Artemia and rotifer use facilitated by a new microdiet in the rearing of barramundi Lates calcarifer (BLOCH) larvae. Aquaculture 257:204–213CrossRefGoogle Scholar
  14. 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
  15. Deng JM, Behringer RR (1995) An insertional mutation in the BTF3 transcription factor gene leads to an early postimplantation lethality in mice. Transgenic Res 4:264–269CrossRefPubMedGoogle Scholar
  16. Douglas SE, Knickle LC, Williams J, Flight RM, Reith ME (2008) A first generation Atlantic halibut microarray: application to developmental studies. J Fish Biol 72:2393–2408CrossRefGoogle Scholar
  17. Engrola S, Figueira L, Conceiçao LEC, Gavaia PJ, Ribeiro L, Dinis MT (2009) Co-feeding in Senegalese sole larvae with inert diet from mouth opening promotes growth at weaning. Aquaculture 288:264–272CrossRefGoogle Scholar
  18. Evjemo JO, Reitan KI, Olsen Y (2003) Copepods as live food organisms in the larval rearing of halibut larvae (Hippoglossus hippoglossus L.) with special emphasis on the nutritional value. Aquaculture 227:191–210CrossRefGoogle Scholar
  19. Fatma N, Kubo E, Chylack LTJ, Shinohara T, Akagi Y, Singh DP (2004) LEDGF regulation of alcohol and aldehyde dehydrogenases in lens epithelial cells: stimulation of retinoic acid production and protection from ethanol toxicity. Am J Physiol Cell Physiol 287:C508–C516CrossRefPubMedGoogle Scholar
  20. Fernández-Díaz C, Pascual E, Yúfera M (1994) Feeding behavior and prey size selection of gilthead seabream, Sparus aurata, larvae fed on inert and live food. Mar Biol 118:323–328CrossRefGoogle Scholar
  21. Flight RM, Wentzell PD (2009) Potential bias in GO::TermFinder. Brief Bioinform 10:289–294. doi:10.1093/bib/bbn054 CrossRefPubMedGoogle Scholar
  22. Gale SE, Frolov A, Han X, Bickel PE, Cao L, Bowcock A, Schaffer JE, Ory DS (2006) A regulatory role for 1-acylglycerol-3-phosphate-O-acyltransferase 2 in adipocyte differentiation. J Biol Chem 281:11082–11089CrossRefPubMedGoogle Scholar
  23. Ganz T (2006) Hepcidin—a peptide hormone at the interface of innate immunity and iron metabolism. Curr Top Microbiol Immunol 306:183–198CrossRefPubMedGoogle Scholar
  24. Gara B, Shields RJ, Mcevoy L (1998) Feeding strategies to achieve correct metamorphosis of Atlantic halibut, Hippoglossus hippoglossus L., using enriched Artemia. Aquac Res 29:935–948CrossRefGoogle Scholar
  25. Glasgow E, Druger RK, Levine EM, Fuchs C, Schechter N (1992) Plasticin, a novel type III neurofilament protein from goldfish retina: increased expression during optic nerve regeneration. Neuron 9:373–381CrossRefPubMedGoogle Scholar
  26. Hamre K, Næss T, Espe M, Holm JC, Lie Ø (2001) A formulated diet for Atlantic halibut (Hippoglossus hippoglossus, L.) larvae. Aquac Nutr 7:123–132CrossRefGoogle Scholar
  27. Hamre K, Opstad I, Espe M, Solbakken J, Hemre G-I, Pittman K (2002) Nutrient composition and metamorphosis sucess of Atlantic halibut (Hippoglossus hippoglossus, L.) larvae fed natural zooplankton or Artemia. Aquac Nutr 8:139–148CrossRefGoogle Scholar
  28. Hamre K, Øfsti A, Næss T, Nortvedt R, Holm JC (2003) Macronutrient composition of formulated diets for Atlantic halibut (Hippoglossus hippoglossus, L.) juveniles. Aquaculture 227:233–244CrossRefGoogle Scholar
  29. Hamre K, Moren M, Solbakken J, Opstad I, Pittman K (2005) The impact of nutrition on metamorphosis in Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 250:555–565CrossRefGoogle Scholar
  30. Heyninck K, Beyaert R (1999) The cytokine-inducible zinc finger protein A20 inhibits IL-1-induced NF-kappaB activation at the level of TRAF6. FEBS Lett 442:147–150CrossRefPubMedGoogle Scholar
  31. Hokamp K, Roche FM, Acab M, Rousseau M-E, Kuo B, Goode D, Aeschliman D, Bryan J, Babiuk LA, Hancock REW, Brinkman FSL (2004) ArrayPipe: a flexible processing pipeline for microarray data. Nucleic Acids Res 32:W457–459CrossRefPubMedGoogle Scholar
  32. Howell BJ, Hoffman DB, Fang G, Murray AW, Salmon ED (2000) Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J Cell Biol 150:1233–1250CrossRefPubMedGoogle Scholar
  33. Infante C, Matsuoka MP, Asensio E, Cañavate JP, Reith M, Manchado M (2008) Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol Biol 9:28CrossRefPubMedGoogle Scholar
  34. Joglekar aP, Xu D, Rigotti DJ, Fairman R, Hay JC (2003) The SNARE motif contributes to rbet1 intracellular targeting and dynamics independently of SNARE interactions. J Biol Chem 278:14121–14133CrossRefPubMedGoogle Scholar
  35. Jones D, Munford J, Gabbott P (1974) Microcapsules as artificial food particles for aquatic filter feeders. Nature 247:233–235CrossRefGoogle Scholar
  36. Kolkovski S, Tandler A, Izquierdo MS (1997) Effects of live food and dietary digestive enzymes on the efficiency of microdiets for seabass (Dicentrarchus labrax) larvae. Aquaculture 148:313–322CrossRefGoogle Scholar
  37. Langdon C (2003) Microparticle types for delivering nutrients to marine fish larvae. Aquaculture 227:259–275CrossRefGoogle Scholar
  38. Leaver MJ, Wright J, George SG (1997) Structure and expression of a cluster of glutathione S-transferase genes from a marine fish, the plaice (Pleuronectes platessa). Biochem J 321:405–412PubMedGoogle Scholar
  39. Lewis LM, Lall SP, Witten PE (2004) Morphological descriptions of the early stages of spine and vertebral development in hatchery-reared larval and juvenile Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 241:47–59CrossRefGoogle Scholar
  40. Lewis-Mccrea LM, Lall SP (2007) Effects of moderately oxidized dietary lipid and the role of vitamin E on the development of skeletal abnormalities in juvenile Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 262:142–155CrossRefGoogle Scholar
  41. Lie Ø, Lambertsen G (1985) Digestive lipolytic enzymes in cod (Gadus morhua): fatty acid specificity. Comp Biochem Physiol 80B:447–450Google Scholar
  42. Ma CT, Velazquez-Dones A, Hagopian JC, Ghosh G, Fu XD, Adams JA (2008) Ordered multi-site phosphorylation of the splicing factor ASF/SF2 by SRPK1. J Mol Biol 376:55–68CrossRefPubMedGoogle Scholar
  43. Mangor-Jenson A, Harboe T, Shields RJ, Gara B, Naas KE (1998) Atlantic halibut, Hippoglossus hippoglossus L., larvae cultivation literature, including a bibliography. Aquac Res 29:857–886CrossRefGoogle Scholar
  44. Murray HM, Gallant JW, Johnson SC, Douglas SE (2006) Cloning and expression analysis of three digestive enzymes from Atlantic halibut (Hippoglossus hippoglossus) during early development: predicting gastrointestinal functionality. Aquaculture 252:394–408CrossRefGoogle Scholar
  45. Naess T, Hamre K, Holm JC (2001) Successful early weaning of Atlantic halibut (Hippoglossus hippoglossus L.) in small shallow raceway systems. Aquac Res 32:163–168CrossRefGoogle Scholar
  46. Naess T, Lie O (1998) A sensitive period during first feeding for the determination of pigmentation pattern in Atlantic halibut, Hippoglossus hippoglossus L., juveniles: the role of diet. Aquac Res 29:925–934CrossRefGoogle Scholar
  47. Nakaniwa M, Hirayama M, Shimizu A, Sasaki T, Asakawa S, Shimizu N, Watabe S (2005) Genomic sequences encoding two types of medaka hemopexin-like protein Wap65, and their gene expression profiles in embryos. J Exp Biol 208:1915–1925CrossRefPubMedGoogle Scholar
  48. O.-Jordal a-E, Torstensen BE, Tsoi SC, Tocher DR, Lall S, Douglas SE (2005) Small scale cDNA microarray analysis of expression of genes for lipid metabolism in liver of Atlantic salmon (Salmo salar L.)—effect of dietary rapeseed oil replacement. J Nutr 135:2355–2361Google Scholar
  49. Önal U, Langdon C (2005) Perfomance of zein-boud particles for delivery of riboflavin to early fish larvae. Aquac Nutr 11:351–258CrossRefGoogle Scholar
  50. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36CrossRefPubMedGoogle Scholar
  51. Rise ML, Douglas SE, Sakhrani D, Williams J, Ewart KV, Rise M, Davidson WS, Koop BF, Devlin RH (2006) Multiple microarray platforms utilized for hepatic gene expression profiling of GH transgenic coho salmon with and without ration restriction. J Mol Endocrinol 37:259–82CrossRefPubMedGoogle Scholar
  52. Ronnestad I, Helland S, Lie Ø (1998) Feeding Artemia to larvae of Atlantic halibut (Hippoglossus hippoglossus L.) results in lower larval vitamin A content compared with feeding copepods. Aquaculture 165:159–164CrossRefGoogle Scholar
  53. Rosenlund G, Stoss J, Talbot C (1997) Co-feeding marine fish larvae with inert and live diets. Aquaculture 155:183–191CrossRefGoogle Scholar
  54. Sarrapoulou E, Kotoulas G, Power DM, Geisler R (2005) Gene expression profiling of gilthead sea bream during early development and detection of stress-related genes by the application of cDNA microarray technology. Physiol Genomics 23:182–191CrossRefGoogle Scholar
  55. Sharpe CR, Pluck A, Gurdon JB (1989) XIF3, a Xenopus peripherin gene, requires an inductive signal for enhanced expression in anterior neural tissue. Devel 107:701–714Google Scholar
  56. Solbakken JS, Berntssen MHG, Norberg B, Pittman K, Hamre K (2002) Different iodine and thyroid levels between Atlantic halibut larvae fed wild zooplankton or Artemia from first exogenous feeding until post metamorphosis. J Fish Biol 61:1345–1362CrossRefGoogle Scholar
  57. Steffen LS, Guyon JR, Vogel ED, Howell MH, Zhou Y, Weber GJ, Zon LI, Kunkel LM (2007) The zebrafish runzel muscular dystrophy is linked to the titin gene. Dev Biol 309:180–192CrossRefPubMedGoogle Scholar
  58. Tusher V, Tibshirani R, Chu C (2001) Significance analysis of microarrays applied to ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121CrossRefPubMedGoogle Scholar
  59. Vilhelmsson O, Martin SAM, Medale F, Kaushik SJ, Houlihan DF (2004) Dietary plant-protein substitutes affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92:71–80CrossRefPubMedGoogle Scholar
  60. Wang H, Kesinger JW, Zhou Q, Wren JD, Martin G, Turner S, Tang Y, Frank MB, Centola M (2008) Identification and characterization of zebrafish ocular formation genes. Genome 51:222–235CrossRefPubMedGoogle Scholar
  61. Williams TD, Diab aM, George SG, Godfrey RE, Sabine V, Conesa A, Minchin SD, Watts PC, Chipman JK (2006) Development of the GENIPOL European flounder (Platichthys flesus) microarray and determination of temporal transcriptional responses to cadmium at low dose. Environ Sci Technol 40:6479–6488CrossRefPubMedGoogle Scholar
  62. Yang C-T, Hindes AE, Hultman KA, Johnson SL (2007) Mutations in gfpt1 and skiv2l2 cause distinct stage-specific defects in larval melanocyte regeneration in zebrafish. PLoS Genet 3:886–900Google Scholar
  63. Yúfera M, Fernández-Diaz C, Pascual E, Sarasquete C, Moyano FJ, Diaz M, Alarcon FJ, Garcia-Gallego M, Parra G (2000) Towards an inert diet for first-feeding gilthead seabream Sparus aurata L. larvae. Aquac Nutr 6:143–152CrossRefGoogle Scholar
  64. Yúfera M, Fernández-Diaz C, Pascual E (2005) Food microparticles for larval fish prepared by internal gelation. Aquaculture 248:253–262CrossRefGoogle Scholar
  65. Yúfera M, Kolkovski S, Fernández-Diaz C, Rinchard J, Lee KJ, Dabrowski K (2003) Delivering bioactive compounds to fish larvae using microencapsulated diets. Aquaculture 227:277–291CrossRefGoogle Scholar
  66. Yúfera M, Pascual E, Fernández-Diaz C (1999) A highly efficient microencapsulated food for rearing early larvae of marine fish. Aquaculture 177:249–256CrossRefGoogle Scholar
  67. Zhang H, Jia Y, Cooper JJ, Hale T, Zhang Z, Elbein SC (2004) Common variants in glutamine:fructose-6-phosphate amidotransferase 2 (GFPT2) gene are associated with type 2 diabetes, diabetic nephropathy, and increased GFPT2 mRNA levels. J Clin Endocrinol Metab 89:748–755CrossRefPubMedGoogle Scholar
  68. Zhang W, Colman RW (2007) Thrombin regulates intracellular cyclic AMP concentration in human platelets through phosphorylation/activation of phosphodiesterase 3A. Blood 110:1475–1482CrossRefPubMedGoogle Scholar

Copyright information

© Her Majesty the Queen in Right of Canada, as represented by the National Research Council of Canada 2009

Authors and Affiliations

  • H. M. Murray
    • 1
    • 4
  • S. P. Lall
    • 1
  • R. Rajaselvam
    • 2
  • L. A. Boutilier
    • 2
  • R. M. Flight
    • 1
    • 3
  • B. Blanchard
    • 4
  • S. Colombo
    • 4
  • V. Mohindra
    • 1
    • 5
  • M. Yúfera
    • 6
  • S. E. Douglas
    • 1
  1. 1.Institute for Marine BiosciencesHalifaxCanada
  2. 2.Genome AtlanticHalifaxCanada
  3. 3.Department of ChemistryDalhousie UniversityHalifaxCanada
  4. 4.Scotian Halibut Ltd.Clark’s HarbourCanada
  5. 5.National Bureau of Fish Genetic ResourcesLucknowIndia
  6. 6.Instituto de Ciencias Marinas de Andalucia (CSIC)Puerto RealSpain

Personalised recommendations